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Ileal and total tract digestibility in local (Mong Cai) and exotic (Landrace × Yorkshire) piglets fed low and high-fibre diets, with or without enzyme supplementation
Livestock Science 126 (2009) 73–79
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Livestock Science j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / l i v s c i
Ileal and total tract digestibility in local (Mong Cai) and exotic (Landrace × Yorkshire) piglets fed low and high-fibre diets, with or without enzyme supplementation Ninh Thi Len a, Tran Bich Ngoc a, Brian Ogle b, Jan Erik Lindberg b,⁎ a b
Department of Animal Feed and Nutrition, National Institute of Animal Husbandry, Hanoi, Vietnam Department of Animal Nutrition and Management, Swedish University of Agricultural Sciences, P.O. Box 7024, 750 07 Uppsala, Sweden
a r t i c l e
i n f o
Article history: Received 22 February 2008 Received in revised form 27 May 2009 Accepted 8 June 2009 Keywords: Breed Piglets Digestibility Enzyme supplementation Fibre
a b s t r a c t Ileal and total tract digestibility of low and high-fibre diets (100 and 200 g/kg neutral detergent fibre), with or without enzyme supplementation (mixture of cellulase, β-glucanase, α-amylase and protease) was determined in piglets of two breeds weaned at 30 days of age. The breeds were local (pure-breed Mong Cai, MC) and exotic (Landrace × Yorkshire, LY). The experimental diets were based on maize meal, soybean meal, fish meal, cassava residue meal, and rice bran. Cassava residue meal and rice bran were the main fibrous feeds in the high-fibre diet. The experiment was arranged according to a 2 × 2 × 2 factorial, completely randomized design with 4 replications, and lasted for 30 days. The coefficient of ileal apparent digestibility (CIAD) was measured by analyzing ileal digesta collected from piglets killed at 60 days of age. The coefficient of total tract apparent digestibility (CTTAD) was measured by analyzing faecal samples collected for 5 consecutive days immediately before the experiment finished. The CIAD and CTTAD of organic matter, crude protein, crude fibre, neutral detergent fibre, acid detergent fibre and amino acids in the high-fibre diet were lower than in the low-fibre diet (P b 0.01). The CIAD of nutrients and amino acids was similar (P N 0.05) between MC and LY, while the CTTAD of nutrients was higher for the MC than for LY (P b 0.05). Enzyme supplementation of the highfibre diet improved daily gain and the digestibility of all dietary components at the ileum and in the total tract (P b 0.05), but there was no effect of enzyme supplementation of the low-fibre diet (P N 0.05). © 2009 Elsevier B.V. All rights reserved.
1. Introduction Like other monogastric animals, pigs do not produce enzymes that are able to degrade non-starch polysaccharides (NSP) (Bach Knudsen and Jørgensen, 2001). These substrates are considered as indigestible in the small intestine but in the large intestine a variable fraction of fibre will be fermented by the microflora to short-chain fatty acids, and thereby serve as a source of energy for the host, and also to substantial amounts of gases. In piglets, however, the capacity of the microflora to degrade the NSP is less developed than in older pigs (Graham et al., 1988). Therefore, the lack of enzymatic ⁎ Corresponding author. Tel.: +46 18 672102; fax: +46 18 672995. E-mail address: [email protected] (J.E. Lindberg). 1871-1413/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.livsci.2009.06.002
capacity might be compensated for by supplementation of the diet with exogenous enzymes. The effects of genotype on the coefficient of total tract apparent digestibility (CTTAD) have been reported by a number of researchers (Fevrier et al., 1992; Ndindana et al., 2002). The results implied that indigenous pig breeds could digest fibre better than improved breeds. The explanation given is that indigenous pigs have a higher digestive capacity in the gastrointestinal tract and higher microbial activity in the hindgut than improved pigs (Jørgensen et al., 1996; Freire et al., 2000). For example, Freire et al. (2003) found that the Alentejano breed of Spain had a higher digestibility of fibrous diets than an improved breed (Duroc × Landrace), and this was attributed to a better ability of the hindgut microflora to degrade the cell wall constituents of the diets.
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Table 1 Chemical composition of feed ingredients (g or MJ/kg DM). Chemical composition a Ingredients
DM
ME b
CP
CF
NDF
Ca
P
Maize meal Soybean meal Full fat soybean meal Fish meal Cassava residue meal Rice bran Milk powder
891 879 902 877 891 891 890
15.3 15.7 17.6 16.2 10.8 9.4 16.4
102.1 521.0 423.5 776.5 20.2 89.8 204.5
34.8 80.8 75.4 8.0 163 253
107 150 172
1.5 3.9 6.1 52.5 1.2 2.2 14.0
3.1 6.5 9.8 23.9 2.2 11.2 12.4
450 464
a DM, dry matter; ME, metabolisable energy; CP, crude protein; CF, crude fibre; NDF, neutral detergent fibre; Ca, calcium; P, phosphorus. b Source, Chinh et al. (2001).
Several studies have shown that enzyme supplementation with fibre degrading enzymes may improve nutrient digestibility and growth performance in pigs, especially after weaning (Baidoo et al., 1998, Yin et al., 2001a,b; Fang et al., 2007). Högberg and Lindberg (2004) also indicated that an increased dietary content of NSP and supplementation with fibre degrading enzymes increased organic acids in the ileum, indicating an enhanced digestibility of fibre in the small intestine in weaned piglets in addition to that resulting from the substantial microflora. However, other researchers failed to obtain positive effects of exogenous enzymes on nutrient digestibility or growth performance in pigs (Mavromichalis et al., 2000; Medel et al., 2002; Diebold et al., 2005). In Vietnam, Mong Cai (MC) and Landrace × Yorkshire (LY) pigs are considered to be typical for local and improved breeds, which are commonly kept by smallholders in rural areas for reproduction and meat production, respectively. The main features of the feeding regimes for these pigs are mainly by-product based diets, which are rich in fibre. Previous studies (Borin et al., 2005; Len et al., 2007) showed that MC pigs had a higher total tract digestibility of nutrients and fibre components but poorer performance compared to improved breeds (LY). These studies raise the question of whether the higher total tract digestibility in MC than LY is partly a result of higher ileal digestibility and whether enzyme supplementation of high-fibre diets can improve growth performance and ileal and total tract digestibility to the same extent in the local (MC) and improved (LY) weaned pigs. 2. Materials and methods 2.1. Location and climate of the study area The experiment was conducted at the Experimental Farm of the National Institute of Animal Husbandry, Hanoi, Vietnam, from April to May 2006. The mean daily temperature at the time of the experiment was 25–28 °C and the relative humidity was around 81–82%. 2.2. Animals and management The animals in the experiment were weaned exotic (Large White × Yorkshire, LY) and indigenous piglets (Mong Cai, MC) at an age of 30 days and a mean body weight of 7.6 ± 0.3 and 4.6 ± 0.3 kg, respectively. Before the experiment started, the piglets were vaccinated against cholera and paratyphoid.
The piglets were housed in pairs in concrete floored pens with wooden slats in an open-sided house. They were fed ad-libitum throughout the experimental period, and had free access to water via automatic water nipples. The pens and the troughs were cleaned every day. 2.3. Experimental feeds The diets were based on extruded maize meal, fish meal, soybean meal, full fat soybean meal, soybean oil, rice bran and cassava residue meal. The diets were calculated to contain 100 (diet L) and 200 g (diet H) of neutral detergent fibre (NDF) kg− 1 DM and were formulated to contain equal concentrations of metabolisable energy, crude protein and essential amino acids to meet the requirements according to NRC (1998). The chemical composition of the ingredients is shown in Table 1 and the ingredient and chemical composition of the experimental diets in Table 2. Chromic oxide was included in the diets (5 g/kg as fed) as a marker for the determination of the digestibility of nutrients. A commercial enzyme mixture was
Table 2 Chemical (g or MJ/ kg DM) and diet composition (g/kg DM) of the experimental diets. Ingredients
Low fibre (L)
High fibre (H)
Maize meal Soybean meal Full fat soybean meal Fish meal Cassava residue meal Rice bran Soybean oil Milk powder Di-calcium phosphate Limestone Vitamin-mineral premix Lysine Methionine Glucose Salt (NaCl) Chemical composition DM ME (MJ/kg) a CP CF Neutral detergent fibre Acid detergent fibre Acid detergent lignin Ether extract Histidine Threonine Arginine Tyrosine Valine Methionine Phenylalanine Isoleucine Leucine Lysine Aspartic acid Proline Glutamic acid Serine Alanine Glycine Total amino acids
623.3 140.9 94.1 60.6 10.9 10.9 0.0 8.8 4.4 2.2 1.8 0.9 0.0 17.8 2.7
298.5 120.8 167.9 60.6 130.1 130.2 35.4 4.4 7.1 2.2 0.9 0.9 0.0 17.8 2.7
907 15.2 233 35 115 42 4 44 5.4 8.3 13.7 7.3 9.4 4 9.4 8.8 16.8 12.5 22 18.8 43.8 12.8 11.3 8.5 213
909 15.0 234 87 204 104 22 101 6.2 7.7 14.6 7.5 9.4 4.1 9.6 8.9 16.3 12.5 19.5 22.4 44.1 12.9 10.9 8.6 215
a
ME was calculated from values in Table 1.
N.T. Len et al. / Livestock Science 126 (2009) 73–79
included at a level of 1 g/kg of the diet, as fed. The enzyme mixture contained cellulase (9007 units/g), β-glucanase (5602 units/g), α-amylase (788 units/g) and protease (922 units/g) (Kemine Industries Pte Ltd, Singapore). Maize meal, fish meal, soybean meal, full fat soybean meal, cassava residue meal and rice bran were ground to pass through a 3 mm diameter sieve and stored in plastic bags to avoid moisture from entering before mixing the diets. The diets were mixed every 7 days and put into plastic bags in order to maintain the quality of the feed and prevent mould growth. The experiment lasted 30 days until the piglets reached 60 days of age. 2.4. Experimental design The experiment was arranged according to a completely randomized 2 × 2 × 2 factorial design, with two breeds (MC and LY), two dietary fibre levels (L and H), with and without enzyme supplementation. A total of 64 weaned piglets (32 MC and 32 LY) from 4 litters of each breed was used in the experiment. The pigs were allocated into 32 pens of 2 pigs (one male and one female). The piglets from different litters were distributed equally among the treatments. Each treatment consisted of 4 pens, with each pen as a replicate. The length of the experiment was 30 days. 2.5. Measurements and data collection During the 5 days before the end of the experiment faeces of individual pigs from each pen were monitored and collected every morning by one of the 10 technicians, each responsible for 3 or 4 pens. The backs of the pigs within each pen were marked with different colours for easy identification. The collected faeces were stored in a refrigerator at 4 °C. At the end of the study, the total faeces of each piglet were pooled and samples taken for analysis. Feed offer and refusals were recorded every day to calculate feed intake. At the beginning and the end of the experiment, the live body weight of the piglets was measured in the morning before they were fed to calculate weight gain and feed conversion ratio. At the age of 60 days, one piglet from each pen was slaughtered after fasting for 4 h. Immediately after slaughter, the digesta were taken from the ileum (about 100 and 80 cm of the small intestine before the ileo-caecal ostium for LY and MC, respectively), immediately transferred to plastic jars and frozen at − 20 °C until analysis. Within breed and treatment, samples of ileum contents and faeces from the same piglet were taken for analysis. Consequently, there were 4 samples of ileum digesta and 4 samples of faeces for each treatment within the breed. The digestibility of the diets at each sampling site was calculated using the indicator technique (Sauer et al., 2000) according to the equation: CADD = ð1 −ðDCF TID = DCD TIF ÞÞT100 where CADD is the coefficient of apparent digestibility of dietary components in the assay diet; DCF the dietary component concentration in ileal digesta or faeces (g/kg
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DM); ID the indicator concentration in the assay diet (g/kg DM); DCD: dietary component concentration in the assay diet (g/kg DM); and IF the indicator concentration in the ileal digesta or faeces (g/kg DM). 2.6. Chemical analysis All samples were dried at 60 °C for 24 h and ground to pass through a 1 mm diameter sieve before analysis. Dry matter (DM), crude protein (CP), crude fibre (CF), ether extract (EE) and ash were analyzed according to the standard methods of AOAC (1990), and CP content was calculated as nitrogen × 6.25. Amino acids (AA) were determined by high performance liquid chromatography using an ion exchange column (Amino Quant, 1990). NDF and acid detergent fibre (ADF) were determined by the method of Goering and Van Soest (1970). Chromium was determined by atomic absorption spectroscopy after ashing the samples (NMAM, 1994).
Table 3 Effects of breed (B), fibre level in diet (D) and enzyme supplementation (+ or −) on performance and the coefficient of ileal apparent digestibility in piglets. Factor
Performance DMI
Ileal apparent digestibility
ADG
FCR
OM
CP
EE
CF
NDF
ADF
Breed (B) MC 85 LY 78
213 312
1.93 1.55
0.76 0.74
0.75 0.75
0.54 0.53
0.18 0.17
0.22 0.21
0.17 0.16
Fibre level (D) L 78 H 80
268 257
1.70 1.78
0.77 0.74
0.76 0.73
0.54 0.52
0.19 0.16
0.22 0.21
0.18 0.16
Enzyme(E) − 79 + 79
250 274
1.79 1.69
0.74 0.77
0.73 0.76
0.52 0.54
0.17 0.18
0.21 0.22
0.16 0.18
B⁎D MC (L) MC (H) LY (L) LY (H)
84 86 72 74
217 209 318 305
1.89 1.98 1.50 1.60
0.77 0.75 0.76 0.73
0.76 0.74 0.76 0.73
0.55 0.52 0.54 0.52
0.19 0.17 0.18 0.16
0.23 0.21 0.22 0.20
0.18 0.16 0.17 0.16
B⁎E MC (−) MC (+) LY (−) LY (+)
85 76 73 73
205 221 295 329
1.96 1.90 1.62 1.48
0.75 0.77 0.73 0.76
0.74 0.76 0.73 0.76
0.53 0.55 0.52 0.54
0.17 0.19 0.17 0.18
0.21 0.23 0.20 0.22
0.16 0.18 0.15 0.17
D⁎E L (−) L (+) H (−) H (+) SE
78 78 79 81 1.071
264ab 271a 236b 279a 8.159
1.70 1.68 1.88 1.69 0.072
0.77a 0.76a 0.70b 0.77a 0.009
0.76a 0.76a 0.71b 0.76a 0.008
0.58 0.55 0.51 0.54 0.013
0.18a 0.19a 0.15b 0.18a 0.005
0.22a 0.22a 0.19b 0.22a 0.005
0.17a 0.18a 0.14b 0.17a 0.005
NS ⁎⁎ ⁎⁎ ⁎⁎
NS ⁎⁎ ⁎⁎ ⁎⁎
NS NS NS NS
NS ⁎⁎ ⁎⁎ ⁎
NS ⁎⁎ ⁎⁎ ⁎
NS ⁎⁎⁎ ⁎⁎⁎ ⁎
Significance ⁎⁎⁎ B
⁎⁎⁎
⁎⁎⁎
D E D⁎E
NS ⁎⁎ ⁎
NS NS NS
NS NS NS
Within a column and factor values with different letters are significantly different (P b 0.05); ⁎P b 0.05; ⁎⁎P b 0.01; ⁎⁎⁎P b 0.001; NS, non-significant. L, low-fibre diet; H, high-fibre diet; −, diet without enzyme supplementation; +, diet with enzyme supplementation; DMI, dry matter intake (g/kg metabolic body weight); ADG, average daily gain (g); FCR, feed conversion ratio (kg feed/kg gain).
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2.7. Statistical analysis
3.2. Ileal apparent digestibility
The data were analyzed statistically using the GLM procedure of Minitab Software, version 13.31 (Minitab, 2000). Treatment means which showed significant differences at the probability level of P b 0.05 were compared using Tukey's pairwise comparison procedure. The model used was as follows:
The coefficients of ileal apparent digestibility (CIAD) of nutrients are shown in Table 3. There were no significant differences in CIAD of nutrients between breeds (P N 0.05), although MC had higher numerical values of CIAD of all nutrients than LY. Fibre level and enzyme addition affected the CIAD of all nutrients (P b 001), with the exception of ether extract. In both breeds, enzyme supplementation of the lowfibre diet had no effect on CIAD, while there were considerable improvements for the high-fibre diet. The improvement in CIAD in the high-fibre diet of OM, CP, CF, NDF and ADF with enzyme supplementation was 6.4, 5.5, 2.9, 2.9 and 3.3% units, respectively (P b 0.01), while there was no effect of enzyme supplementation of the low-fibre diet. The CIAD of amino acids (AA) is shown in Table 4. The effects of breed, fibre level in the diet and enzyme addition on the CIAD of AA were similar to the effects on the CIAD of CP. The CIAD of AA was not different between the two breeds (P N 0.05). Fibre level in the diet had a negative effect, and enzyme supplementation had a positive effect on the CIAD of AA (P b 0.05). Supplementation of enzymes to the high-fibre diet improved the CIAD of almost all AA (P b 0.05), while this effect was not found on the low-fibre diet (P N 0.05). Among the essential AA, CIAD of histidine, methionine and lysine was higher than that of the other AA, while the CIAD of arginine, valine and leucine had the lowest values, with intermediate values for threonine, tyrosine, phenylalanine and isoleucine. Among the non-essential AA, the lowest CIAD was found for alanine, proline, and glycine, while the highest values were for glutamic acid, and with intermediate values for aspartic acid and serine.
Yijk = M + Bi + Dj + Ek + Bi × Dj + ðBi × Ek Þ + Dj × Ek + e Where Yijk is the growth performance or nutrient digestibility; M is the overall mean; Bi is the effect of breed i, Dj is the effect of fibre level, j; Ek is the effect of enzyme supplementation k; (Bi × Dj) is the interaction between breed i and fibre level j; (Bi × Ek) is the interaction between breed i and enzyme supplementation k; (Dj × Ek) is the interaction between fibre level j and enzyme supplementation k; e is the error. 3. Results 3.1. Performance The growth performance and feed conversion ratio (FCR) are shown in Table 3. The MC piglets had lower average daily gain (ADG) and poorer FCR (P b 0.05) but higher feed intake expressed as g/kg metabolic body weight than LY. Enzyme supplementation had a significant positive effect on ADG (P b 0.01). There was an interaction between diet and enzyme supplementation for ADG (P b 0.05), as the piglets fed the high-fibre diet supplemented with the enzyme mixture had 18% higher ADG compared to those fed the high-fibre diet without enzymes (P b 0.05), while there was no improvement in ADG and FCR in the piglets fed the low-fibre diet with enzyme supplementation (P N 0.05).
3.3. Total tract apparent digestibility Treatment effects on the CTTAD are shown in Table 5. In contrast to CIAD, there were significant differences in CTTAD of OM, CP, EE, CF, NDF and ADF between breeds, with higher
Table 4 Effect of breed (B), fibre level in diet (D) and enzyme supplementation (+ or −) on ileal digestibility of amino acids in piglets. Breed
Histidine Threonine Arginine Tyrosine Valine Methionine Phenylalanine Isoleucine Leucine Lysine Aspartic acid Glutamic acid Serine Alanine Proline Glycine
Fibre level
Enzyme
SE
MC
LY
L
H
−
+
0.80 0.73 0.72 0.75 0.70 0.77 0.73 0.73 0.72 0.76 0.74 0.80 0.72 0.71 0.66 0.70
0.79 0.72 0.71 0.74 0.70 0.77 0.73 0.74 0.72 0.77 0.74 0.79 0.72 0.71 0.76 0.70
0.80 0.74 0.73 0.77 0.71 0.78 0.74 0.74 0.73 0.78 0.75 0.80 0.73 0.72 0.77 0.71
0.77 0.71 0.70 0.73 0.69 0.76 0.72 0.73 0.71 0.75 0.73 0.78 0.71 0.70 0.74 0.69
0.77 0.71 0.70 0.73 0.69 0.76 0.71 0.68 0.71 0.75 0.75 0.78 0.71 0.69 0.75 0.69
0.80 0.74 0.72 0.77 0.71 0.78 0.75 0.78 0.73 0.78 0.73 0.81 0.74 0.72 0.77 0.71
0.054 0.081 0.068 0.033 0.068 0.068 0.034 0.061 0.066 0.058 0.063 0.073 0.044 0.005 0.075 0.053
⁎P b 0.05; ⁎⁎P b 0.01; ⁎⁎⁎P b 0.001; NS, non-significant. L, low-fibre diet; H, high-fibre diet; −, diet without enzyme supplementation; +, diet with enzyme supplementation.
Significance B
D
E
D⁎E
NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS
NS ⁎⁎ ⁎⁎⁎ ⁎⁎⁎ ⁎ ⁎ ⁎⁎ ⁎⁎ ⁎ ⁎⁎ ⁎ ⁎⁎ ⁎⁎
⁎ ⁎⁎ ⁎⁎⁎ ⁎⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎
NS ⁎
NS ⁎⁎ ⁎⁎
NS ⁎⁎ ⁎⁎ ⁎ ⁎⁎ ⁎⁎ ⁎ ⁎⁎
NS NS NS ⁎⁎ ⁎⁎ ⁎⁎ ⁎ ⁎⁎ NS ⁎ NS NS ⁎ ⁎
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Table 5 Effects of breed (B), fibre level in diet (D) and enzyme supplementation (+ or −) on the coefficient of total tract apparent digestibility in piglets.
NDF for LY was 2.0, 3.1, 3.0, 3.2, 3.0 and 2.2% units while for the MC it was 2.0, 1.1, 2.0, 1.4, 1.1 and 0.5% units, respectively.
Factor
OM
CP
EE
CF
NDF
ADF
4. Discussion
Breed (B) MC LY
0.87 0.83
0.83 0.80
0.65 0.60
0.55 0.49
0.55 0.51
0.43 0.41
Fibre level (D) L 0.86 H 0.84
0.83 0.80
0.64 0.61
0.53 0.52
0.54 0.52
0.43 0.41
Enzyme(E) − +
0.85 0.86
0.80 0.83
0.61 0.64
0.51 0.53
0.52 0.54
0.41 0.42
B⁎D MC (L) MC (H) LY (L) LY (H)
0.88 0.85 0.84 0.82
0.84 0.81 0.81 0.79
0.66 0.64 0.61 0.58
0.56 0.54 0.50 0.49
0.55 0.54 0.53 0.50
0.44 0.42 0.42 0.40
B⁎E MC (−) MC (+) LY (−) LY (+)
0.85 0.87 0.82 0.84
0.82 0.83 0.79 0.82
0.64 0.66 0.58 0.61
0.54 0.56 0.48 0.51
0.54 0.55 0.50 0.53
0.43 0.43 0.40 0.42
D⁎E L (−) L (+) H (−) H (+) SE
0.86a 0.86a 0.82b 0.86a 0.007
0.83a 0.83a 0.78b 0.82a 0.006
0.63a 0.64a 0.59b 0.63a 0.010
0.52a 0.53a 0.50b 0.53a 0.006
0.54a 0.55a 0.50b 0.54a 0.006
0.43a 0.42a 0.39b 0.43a 0.006
Significance B D E D⁎E
⁎⁎⁎ ⁎⁎ ⁎⁎ ⁎
⁎ ⁎⁎⁎ ⁎⁎ ⁎⁎
⁎⁎⁎ ⁎⁎ ⁎
⁎⁎⁎ ⁎ ⁎⁎ ⁎
⁎⁎ ⁎⁎ ⁎⁎ ⁎
⁎ ⁎⁎ ⁎ ⁎⁎
An increased level of dietary fibre to the weaned piglets did not affect feed intake or impair the ADG and FCR. Similar results were obtained in diets with cassava residue or rice bran as fibre sources in diets to weaned piglets of the same age (Len et al., 2009). However, increasing the fibre level in the diet resulted in a decrease in both the ileal and the total tract apparent digestibilities of OM, CP, CF, NDF, ADF and amino acids. This was in line with earlier studies on fibre inclusion in diets for weaned piglets (Högberg and Lindberg, 2004, 2006) and growing pigs (Noblet and Perez, 1993; Lindberg and Andersson, 1998; Le Goff et al., 2002; Len et al., 2007). However, the limitations of the slaughter technique used for determining ileal digestibility must be acknowledged, as there is a possibility of translocation of the digesta and shedding of the mucosal cells into the gut lumen, which would create an artifact in the determination of the composition of the ileal digesta (Fuller, 1991). The reduction in total tract digestibility of OM on diet H compared to diet L (0.4 units for each additional unit of CF) was much lower than reported by Lindberg and Andersson (1998) (2.0–2.7 units for each additional unit of CF), probably as a result of differences in the fibre components in the two studies. An additional factor could have been the inclusion of 3.5% soya oil in the high-fibre diet, as vegetable oils are known to be highly digestible (Freeman et al., 1968). It appears likely that both gut fill and the weight of the gastrointestinal tract (Jørgensen et al., 1996; Freire et al., 2003; Len et al., 2009) increased on the high-fibre diet. This would explain the unchanged ADG and FCR despite increased fibre intake (Högberg and Lindberg, 2006) and reduced nutrient digestibility. The improvement of nutrient digestibility in the high-fibre diet supplemented with an enzyme mixture, containing fibre degrading enzymes, may have been due to the disruption of intact cell walls and the release of entrapped nutrients (Hesselman and Åman, 1986). In addition, this may lead to the changes of physical properties of non-starch polysaccharides, such as reduced viscosity and water holding capacity, and to changes in the composition and concentrations of bacteria in the small and large intestine (Bedford and Classen, 1992; Jensen et al., 1998; O'Connell et al., 2005). The current results are in agreement with several previous studies (Inborr et al., 1993; Dierick and Decuypere, 1996; Diebold et al., 2004; Omogbenigun et al., 2004) and may be explained by a limited ability in young pigs to effectively utilize diets containing low quality ingredients with high-fibre content (Graham et al., 1988). However, with appropriate enzyme supplementation, this constraint can be alleviated, with a potential to improve the nutritional value of such diets for young pigs (Yin et al., 2001a,b, Omogbenigun et al., 2004) and for growing pigs (Kinh et al., 2001; Kinh et al., 2004). The extent and consistency of positive responses to enzyme supplementation in pigs varies, depending on a number of factors, such as age, physiological status, the capacity of the exogenous enzymes in the gut, and especially on the chemical composition of the diet. The interaction between enzyme supplementation and dietary fibre content in the present study could have been due
NS
Within a column and factor values with different letters are significantly different (P b 0.05). ⁎P b 0.05; ⁎⁎P b 0.01; ⁎⁎⁎P b 0.001; NS, non-significant. L, low-fibre diet; H, high-fibre diet; −, diet without enzyme supplementation; +, diet with enzyme supplementation.
values for MC (P b 0.05). Also, fibre level in the diet had a negative effect on CTTAD of OM, CP, CF, NDF, and ADF (P b 0.05), but not for CTTAD of EE (P N 0.05), while enzyme supplementation had a positive effect (P b 0.05). Overall, the supplementation of the enzyme mixture to the diet increased the CTTAD of OM, CP, EE, CF, NDF, and ADF by 1.1, 2.2, 2.5, 2.2, 2.1 and 1.4% units, respectively. The reduction of the CTTAD of OM, CP, CF, NDF and ADF with increased fibre content was 2.1, 2.5, 1.3, 2.4, and 1.6% units, respectively. Supplementation of enzymes to the high-fibre diet increased the CTTAD of OM, CP and fibre components (P b 0.05), while supplementation of the low-fibre diet had no effect (P N 0.05). The difference in the CTTAD of OM, CP, EE, CF, NDF and ADF between the highfibre diets with and without enzyme supplementation was 3.7, 4.3, 4.2, 3.7, 3.6 and 3.2% units, respectively. Although the interaction between breed and enzyme addition was not significant for CTTAD, the improvement of CTTAD of almost all nutrients in LY piglets fed diets with enzyme mixture was numerically higher than that in the MC. The improvement with enzyme addition of the CTTAD of OM, CP, EE, CF, NDF and
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to a change in the activity of the bacteria in the digestive tract of the piglets when fed a diet with enzyme supplementation. This is supported by the study of Garry et al. (2007) showing that enzyme supplementation to different cereal based pig diets resulted in changes in the activity of bacteria in the caecum and large intestine. A further possible explanation could have been the improvement of the morphology of small intestine with enzyme supplemented high-fibre diets, such as an increase of villus size in the small intestine. This was indicated by Mathlouthi et al. (2002) in a study with chickens fed with rye and maize based diets with and without xylanase and ß-glucanase supplementation. In the present study MC pigs had higher feed intake but lower ADG and thus poorer FCR than LY, mainly due to the different growth potentials of the breeds, as discussed previously (Len et al., 2008, 2009). The digestion of OM and dietary components in MC was higher than in LY, which is in agreement with previous findings that indigenous pig breeds can digest high-fibre diets more efficiently than exotic breeds. For example, Len et al. (2007) and Borin et al. (2005) indicated that the MC breed digested energy and dietary components more efficiently than LY, and concluded that fibrous diets are more appropriate for indigenous than for exotic pigs. Ndindana et al. (2002) concluded that the digestibility of diets containing graded levels of maize cobs was higher in indigenous Zimbabwean growing pigs than in an exotic breed (Large White). In a study performed by Fevrier et al. (1992), Chinese Meishan pigs digested highfibre diets more efficiently although there were no differences in digestibility between Chinese Meishan and Large White pigs fed low-fibre diets. Similarly, Freire et al. (2003) reported that Alentejano native young pigs utilized the cell wall components of the diet better than exotic breeds. Indigenous pigs in Southeast Portugal from an age of 21 days also showed a higher digestive potential towards fibrous dietary components than the Large White breed (Freire et al., 1998) and a higher activity of the microbial population present in the hindgut, which is particularly important for the degradation of dietary fibre (Bach Knudsen and Hansen, 1991). In contrast, Ly et al. (1998) found that the total tract digestibility of most dietary components in very fibrous diets was not higher in Cuban Creole than in Large White pigs. Kemp et al. (1991) also concluded that even when the diet was rich in fibre, the digestibility of CF in the indigenous Chinese Meishan was similar to the Dutch Landrace pigs. The lack of any effect of breed on ileal digestibility of amino acids in our study is in agreement with Hennig et al. (2004), who also found no differences in amino acid apparent ileal digestibilities between Minipigs and Saddleback pigs. 5. Conclusion It can be concluded that genotype had no influence on the ileal digestibility of OM, CP, CF, NDF, ADF and amino acids, whereas the total tract digestibility was higher for MC. Enzyme supplementation of the high-fibre diet improved the digestibility of all dietary components at the ileum and total tract, but there was no effect of enzyme supplementation of the low-fibre diet.
Acknowledgements The authors would like to thank Sida-SAREC (Swedish International Development Cooperation Agency — Department for Research Cooperation), through the regional MEKARN program and the Swedish University of Agricultural Sciences, Department of Animal Nutrition and Management, for their financial support of this study. Special thanks to the researchers in the Department of Animal Feeds and Nutrition of the National Institute of Animal Husbandry for their help in carrying out the study. Thanks also to Kemine Industries Pte Ltd for supplying the enzyme mixture. References Amino Quant (Operator, s Handbook). HP No 01090 90025, 1990. Printed in the Federal Republic of Germany. Hewlett Packard Company. AOAC, 1990. Official methods of analysis, Association of Official Analytical Chemists, Arlington, Virginia, 15th ed. Bach Knudsen, K.E., Hansen, I., 1991. Gastrointestinal implications in pigs of wheat and oat fractions. 1. Digestibility and bulking properties of polysaccharides and other major constituents. British Journal of Nutrition 65, 217–232. Bach Knudsen, K.E., Jørgensen, H., 2001. Intestinal degradation of dietary carbohydrates from birth to maturity. In: Lindberg, J.E., Ogle, B. (Eds.), Digestive Physiology of Pigs. CABI Publishing, Wallingford, pp. 109–121. Baidoo, S.K., Liu, Y.G., Yungblut, D., 1998. Effect of microbial enzyme supplementation on energy, amino acid digestibility and performance of pigs fed hulless barley based diets. Canadian Journal of Animal Science 78, 625–631. Bedford, M.R., Classen, H.L., 1992. Reduction of intestinal viscosity through manipulation of dietary rye and pentosanase concentration is effected through changes in the carbohydrate composition of the intestinal aqueous phase and results in improved growth rate and food conversion efficiency of broiler chicks. Journal of Nutrition 122, 560–569. Borin, K., Lindberg, J.E., Ogle, B., 2005. Effect of variety and preservation method of cassava leaves on diet digestibility by indigenous and improved pigs. Animal Science 80, 319–324. Chinh, B.V., Oanh, B.T., Ha, N.N., Viet, T.Q., Khang, D.T., Tinh, N.T., 2001. Chemical Composition and Nutritive Value of Animal Feeds in Vietnam. Agricultural Publishing House, Hanoi. Diebold, G., Mosenthin, R., Piepho, H.P., Sauer, W.C., 2004. Effect of supplementation of xylanase and phospholipase to a wheat-based diet for weanling pigs on nutrient digestibility and concentrations of microbial metabolites in ileal digesta and feces. Journal of Animal Science 82, 2647–2656. Diebold, G., Mosenthin, R., Sauer, W.C., Dugan, M.E.R., Lien, K.A., 2005. Supplementation of xylanase and phospholipase to wheat-based diets for weaner pigs. Journal of Animal Physiology and Animal Nutrition 89, 316–325. Dierick, N., Decuypere, J., 1996. Mode of action of exogenous enzymes in growing pig nutrition. Pig news and information 17, 41–48. Fang, Z.F., Peng, J., Liu, Z.L., Liu, Y.G., 2007. Responses of non-starch polysaccharide-degrading enzymes on digestibility and performance of growing pigs fed a diet based on corn, soya bean meal and Chinese double-low rapeseed meal. Journal of Animal Physiology and Animal Nutrition 91, 361–368. Fevrier, C., Bourdon, D., Aumaitre, A., 1992. Effects of level of dietary fibre from wheat bran on digestibility of nutrients, digestive enzymes and performance in the Large White and Chinese Meishan pigs. Journal of Animal Physiology and Animal Nutrition 68, 60–72. Freire, J.P.B., Peiniau, J., Cunha, L.F., Almeida, J.A.A., Aumaitre, A., 1998. Comparative effects of dietary fat and fibre in Alentejano and Large White piglets: digestibility, digestive enzymes and metabolic data. Livestock Production Science 53, 37–47. Freire, J.P.B., Guerreiro, A.J.G., Cunha, L.F., Aumaitre, A., 2000. Effect of dietary fibre source on total tract digestibility, caecum volatile fatty acids and digestive transit time in the weaned piglet. Animal Feed Science and Technology 87, 71–83. Freire, J.P.B., Dias, R.I.M., Cunha, L.F., Aumaitre, A., 2003. The effect of genotype and dietary fibre level on the caecal bacterial enzyme activity of young piglets: digestive consequences. Animal Feed Science and Technology 106, 119–130. Freeman, C.P., Holme, D.W., Annison, E.F., 1968. The determination of the true digestibilities of interesterified fats in young pig. British Journal of Nutrition 22, 651–660.
N.T. Len et al. / Livestock Science 126 (2009) 73–79 Fuller, M., 1991. Methodologies for the measurement of digestion. In: Verstegen, M.W.A., Huisman, J., den Hartog, L.A. (Eds.), Digestive Physiology in Pigs. Proceedings of 5th International Symposium. Wageningen Academic Publishers, Wageningen, the Netherlands, pp. 273–288. Garry, B.P., Fogarty, M., Curran, T.P., O Connell, M.J., O Doherty, J.V., 2007. The effect of cereal type and enzyme addition on pig performance, intestinal microflora, and ammonia and odour emissions. Animal 1, 751–757. Goering, H.K., Van Soest, P.J., 1970. Forage fibre analysis (apparatus, reagents and some applications). USDA Agri. Handbook. No. 379. National Academic Press, Washington DC, pp. 1–19. Graham, H., Löwgren, W., Pettersson, D., Åman, P., 1988. Effect of enzyme supplementation on digestion of a barley/pollard-based pig diet. Nutrition Reports International 38, 1073–1079. Hennig, U., Metges, C.C., Berk, A., Tuchscherer, A., Kwella, M., 2004. Relative ileal amino acid flows and microbial counts in intestinal effluents of Goettingen minipigs and Saddleback pigs are not different. Journal of Animal Science 82, 1976–1985. Hesselman, K., Åman, P., 1986. The effect of [beta]-glucanase on the utilization of starch and nitrogen by broiler chickens fed on barley of low- or high-viscosity. Animal Feed Science and Technology 15, 83–93. Högberg, A., Lindberg, J.E., 2004. Influence of cereal non-starch polysaccharides and enzyme supplementation on digestion site and gut environment in weaned piglets. Animal Feed Science and Technology 116, 113–128. Högberg, A., Lindberg, J.E., 2006. The effect of level and type of cereal nonstarch polysaccharides on the performance, nutrient utilization and gut environment of pigs around weaning. Animal Feed Science and Technology 127, 200–219. Inborr, J., Schmitz, M., Ahrens, F., 1993. Effect of adding fibre and starch degrading enzymes to a barley/wheat based diet on performance and nutrient digestibility in different segments of the small intestine of early weaned pigs. Animal Feed Science and Technology 44, 113–127. Jensen, M.S., Bach Knudsen, K.E., Inborr, J., Jakobsen, K., 1998. Effect of [beta]glucanase supplementation on pancreatic enzyme activity and nutrient digestibility in piglets fed diets based on hulled and hulless barley varieties. Animal Feed Science and Technology 72, 329–345. Jørgensen, H., Zhao, X., Eggum, B.O., Zhao, X.Q., 1996. The influence of dietary fibre and environmental temperature on the development of the gastrointestinal tract, digestibility, degree of fermentation in the hindgut and energy metabolism in pigs. British Journal of Nutrition 75, 365–378. Kemp, B., Hartog, L.A., den, K., Zandstra, T., 1991. The digestibility of nutrients, energy and nitrogen in Meishan and Dutch Landrace pigs. Journal of Animal Physiology and Animal Nutrition 65, 263–266. Kinh, L.V., Phuong, D.H., Vinh, D., 2004. Enhancing utilization of rice bran in diet for fattening pigs. Proceeding of Animal Science Workshop. Ministry of Agriculture and Rural Development, pp. 289–317 (in Vietnamese). Kinh, L.V., Thang, P.T., Phu, N.V., Vinh, D., 2001. Effect of supplementation of enzyme mixture to diets for fattening pigs. Proceeding of Animal Science Workshop. Ministry of Agriculture and Rural Development, 219–228 (in Vietnamese). Le Goff, G., van Milgen, J., Noblet, J., 2002. Influence of dietary fibre on digestive utilization and rate of passage in growing pigs, finishing pigs and adult sows. Animal Science 74, 503–515. Len, N.T., Lindberg, J.E., Ogle, B., 2007. Digestibility and nitrogen retention of diets containing different levels of fibre in local (Mong Cai), F1 (Mong Cai × Yorkshire) and exotic (Landrace × Yorkshire) growing pigs in Vietnam. Journal of Animal Physiology and Animal Nutrition 91, 297–303. Len, N.T., Lindberg, J.E., Ogle, B., 2008. Effect of fiber level in the diet on the performance and carcass traits of Mong Cai, F1 crossbred (Mong
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Livestock Science j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / l i v s c i
Ileal and total tract digestibility in local (Mong Cai) and exotic (Landrace × Yorkshire) piglets fed low and high-fibre diets, with or without enzyme supplementation Ninh Thi Len a, Tran Bich Ngoc a, Brian Ogle b, Jan Erik Lindberg b,⁎ a b
Department of Animal Feed and Nutrition, National Institute of Animal Husbandry, Hanoi, Vietnam Department of Animal Nutrition and Management, Swedish University of Agricultural Sciences, P.O. Box 7024, 750 07 Uppsala, Sweden
a r t i c l e
i n f o
Article history: Received 22 February 2008 Received in revised form 27 May 2009 Accepted 8 June 2009 Keywords: Breed Piglets Digestibility Enzyme supplementation Fibre
a b s t r a c t Ileal and total tract digestibility of low and high-fibre diets (100 and 200 g/kg neutral detergent fibre), with or without enzyme supplementation (mixture of cellulase, β-glucanase, α-amylase and protease) was determined in piglets of two breeds weaned at 30 days of age. The breeds were local (pure-breed Mong Cai, MC) and exotic (Landrace × Yorkshire, LY). The experimental diets were based on maize meal, soybean meal, fish meal, cassava residue meal, and rice bran. Cassava residue meal and rice bran were the main fibrous feeds in the high-fibre diet. The experiment was arranged according to a 2 × 2 × 2 factorial, completely randomized design with 4 replications, and lasted for 30 days. The coefficient of ileal apparent digestibility (CIAD) was measured by analyzing ileal digesta collected from piglets killed at 60 days of age. The coefficient of total tract apparent digestibility (CTTAD) was measured by analyzing faecal samples collected for 5 consecutive days immediately before the experiment finished. The CIAD and CTTAD of organic matter, crude protein, crude fibre, neutral detergent fibre, acid detergent fibre and amino acids in the high-fibre diet were lower than in the low-fibre diet (P b 0.01). The CIAD of nutrients and amino acids was similar (P N 0.05) between MC and LY, while the CTTAD of nutrients was higher for the MC than for LY (P b 0.05). Enzyme supplementation of the highfibre diet improved daily gain and the digestibility of all dietary components at the ileum and in the total tract (P b 0.05), but there was no effect of enzyme supplementation of the low-fibre diet (P N 0.05). © 2009 Elsevier B.V. All rights reserved.
1. Introduction Like other monogastric animals, pigs do not produce enzymes that are able to degrade non-starch polysaccharides (NSP) (Bach Knudsen and Jørgensen, 2001). These substrates are considered as indigestible in the small intestine but in the large intestine a variable fraction of fibre will be fermented by the microflora to short-chain fatty acids, and thereby serve as a source of energy for the host, and also to substantial amounts of gases. In piglets, however, the capacity of the microflora to degrade the NSP is less developed than in older pigs (Graham et al., 1988). Therefore, the lack of enzymatic ⁎ Corresponding author. Tel.: +46 18 672102; fax: +46 18 672995. E-mail address: [email protected] (J.E. Lindberg). 1871-1413/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.livsci.2009.06.002
capacity might be compensated for by supplementation of the diet with exogenous enzymes. The effects of genotype on the coefficient of total tract apparent digestibility (CTTAD) have been reported by a number of researchers (Fevrier et al., 1992; Ndindana et al., 2002). The results implied that indigenous pig breeds could digest fibre better than improved breeds. The explanation given is that indigenous pigs have a higher digestive capacity in the gastrointestinal tract and higher microbial activity in the hindgut than improved pigs (Jørgensen et al., 1996; Freire et al., 2000). For example, Freire et al. (2003) found that the Alentejano breed of Spain had a higher digestibility of fibrous diets than an improved breed (Duroc × Landrace), and this was attributed to a better ability of the hindgut microflora to degrade the cell wall constituents of the diets.
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N.T. Len et al. / Livestock Science 126 (2009) 73–79
Table 1 Chemical composition of feed ingredients (g or MJ/kg DM). Chemical composition a Ingredients
DM
ME b
CP
CF
NDF
Ca
P
Maize meal Soybean meal Full fat soybean meal Fish meal Cassava residue meal Rice bran Milk powder
891 879 902 877 891 891 890
15.3 15.7 17.6 16.2 10.8 9.4 16.4
102.1 521.0 423.5 776.5 20.2 89.8 204.5
34.8 80.8 75.4 8.0 163 253
107 150 172
1.5 3.9 6.1 52.5 1.2 2.2 14.0
3.1 6.5 9.8 23.9 2.2 11.2 12.4
450 464
a DM, dry matter; ME, metabolisable energy; CP, crude protein; CF, crude fibre; NDF, neutral detergent fibre; Ca, calcium; P, phosphorus. b Source, Chinh et al. (2001).
Several studies have shown that enzyme supplementation with fibre degrading enzymes may improve nutrient digestibility and growth performance in pigs, especially after weaning (Baidoo et al., 1998, Yin et al., 2001a,b; Fang et al., 2007). Högberg and Lindberg (2004) also indicated that an increased dietary content of NSP and supplementation with fibre degrading enzymes increased organic acids in the ileum, indicating an enhanced digestibility of fibre in the small intestine in weaned piglets in addition to that resulting from the substantial microflora. However, other researchers failed to obtain positive effects of exogenous enzymes on nutrient digestibility or growth performance in pigs (Mavromichalis et al., 2000; Medel et al., 2002; Diebold et al., 2005). In Vietnam, Mong Cai (MC) and Landrace × Yorkshire (LY) pigs are considered to be typical for local and improved breeds, which are commonly kept by smallholders in rural areas for reproduction and meat production, respectively. The main features of the feeding regimes for these pigs are mainly by-product based diets, which are rich in fibre. Previous studies (Borin et al., 2005; Len et al., 2007) showed that MC pigs had a higher total tract digestibility of nutrients and fibre components but poorer performance compared to improved breeds (LY). These studies raise the question of whether the higher total tract digestibility in MC than LY is partly a result of higher ileal digestibility and whether enzyme supplementation of high-fibre diets can improve growth performance and ileal and total tract digestibility to the same extent in the local (MC) and improved (LY) weaned pigs. 2. Materials and methods 2.1. Location and climate of the study area The experiment was conducted at the Experimental Farm of the National Institute of Animal Husbandry, Hanoi, Vietnam, from April to May 2006. The mean daily temperature at the time of the experiment was 25–28 °C and the relative humidity was around 81–82%. 2.2. Animals and management The animals in the experiment were weaned exotic (Large White × Yorkshire, LY) and indigenous piglets (Mong Cai, MC) at an age of 30 days and a mean body weight of 7.6 ± 0.3 and 4.6 ± 0.3 kg, respectively. Before the experiment started, the piglets were vaccinated against cholera and paratyphoid.
The piglets were housed in pairs in concrete floored pens with wooden slats in an open-sided house. They were fed ad-libitum throughout the experimental period, and had free access to water via automatic water nipples. The pens and the troughs were cleaned every day. 2.3. Experimental feeds The diets were based on extruded maize meal, fish meal, soybean meal, full fat soybean meal, soybean oil, rice bran and cassava residue meal. The diets were calculated to contain 100 (diet L) and 200 g (diet H) of neutral detergent fibre (NDF) kg− 1 DM and were formulated to contain equal concentrations of metabolisable energy, crude protein and essential amino acids to meet the requirements according to NRC (1998). The chemical composition of the ingredients is shown in Table 1 and the ingredient and chemical composition of the experimental diets in Table 2. Chromic oxide was included in the diets (5 g/kg as fed) as a marker for the determination of the digestibility of nutrients. A commercial enzyme mixture was
Table 2 Chemical (g or MJ/ kg DM) and diet composition (g/kg DM) of the experimental diets. Ingredients
Low fibre (L)
High fibre (H)
Maize meal Soybean meal Full fat soybean meal Fish meal Cassava residue meal Rice bran Soybean oil Milk powder Di-calcium phosphate Limestone Vitamin-mineral premix Lysine Methionine Glucose Salt (NaCl) Chemical composition DM ME (MJ/kg) a CP CF Neutral detergent fibre Acid detergent fibre Acid detergent lignin Ether extract Histidine Threonine Arginine Tyrosine Valine Methionine Phenylalanine Isoleucine Leucine Lysine Aspartic acid Proline Glutamic acid Serine Alanine Glycine Total amino acids
623.3 140.9 94.1 60.6 10.9 10.9 0.0 8.8 4.4 2.2 1.8 0.9 0.0 17.8 2.7
298.5 120.8 167.9 60.6 130.1 130.2 35.4 4.4 7.1 2.2 0.9 0.9 0.0 17.8 2.7
907 15.2 233 35 115 42 4 44 5.4 8.3 13.7 7.3 9.4 4 9.4 8.8 16.8 12.5 22 18.8 43.8 12.8 11.3 8.5 213
909 15.0 234 87 204 104 22 101 6.2 7.7 14.6 7.5 9.4 4.1 9.6 8.9 16.3 12.5 19.5 22.4 44.1 12.9 10.9 8.6 215
a
ME was calculated from values in Table 1.
N.T. Len et al. / Livestock Science 126 (2009) 73–79
included at a level of 1 g/kg of the diet, as fed. The enzyme mixture contained cellulase (9007 units/g), β-glucanase (5602 units/g), α-amylase (788 units/g) and protease (922 units/g) (Kemine Industries Pte Ltd, Singapore). Maize meal, fish meal, soybean meal, full fat soybean meal, cassava residue meal and rice bran were ground to pass through a 3 mm diameter sieve and stored in plastic bags to avoid moisture from entering before mixing the diets. The diets were mixed every 7 days and put into plastic bags in order to maintain the quality of the feed and prevent mould growth. The experiment lasted 30 days until the piglets reached 60 days of age. 2.4. Experimental design The experiment was arranged according to a completely randomized 2 × 2 × 2 factorial design, with two breeds (MC and LY), two dietary fibre levels (L and H), with and without enzyme supplementation. A total of 64 weaned piglets (32 MC and 32 LY) from 4 litters of each breed was used in the experiment. The pigs were allocated into 32 pens of 2 pigs (one male and one female). The piglets from different litters were distributed equally among the treatments. Each treatment consisted of 4 pens, with each pen as a replicate. The length of the experiment was 30 days. 2.5. Measurements and data collection During the 5 days before the end of the experiment faeces of individual pigs from each pen were monitored and collected every morning by one of the 10 technicians, each responsible for 3 or 4 pens. The backs of the pigs within each pen were marked with different colours for easy identification. The collected faeces were stored in a refrigerator at 4 °C. At the end of the study, the total faeces of each piglet were pooled and samples taken for analysis. Feed offer and refusals were recorded every day to calculate feed intake. At the beginning and the end of the experiment, the live body weight of the piglets was measured in the morning before they were fed to calculate weight gain and feed conversion ratio. At the age of 60 days, one piglet from each pen was slaughtered after fasting for 4 h. Immediately after slaughter, the digesta were taken from the ileum (about 100 and 80 cm of the small intestine before the ileo-caecal ostium for LY and MC, respectively), immediately transferred to plastic jars and frozen at − 20 °C until analysis. Within breed and treatment, samples of ileum contents and faeces from the same piglet were taken for analysis. Consequently, there were 4 samples of ileum digesta and 4 samples of faeces for each treatment within the breed. The digestibility of the diets at each sampling site was calculated using the indicator technique (Sauer et al., 2000) according to the equation: CADD = ð1 −ðDCF TID = DCD TIF ÞÞT100 where CADD is the coefficient of apparent digestibility of dietary components in the assay diet; DCF the dietary component concentration in ileal digesta or faeces (g/kg
75
DM); ID the indicator concentration in the assay diet (g/kg DM); DCD: dietary component concentration in the assay diet (g/kg DM); and IF the indicator concentration in the ileal digesta or faeces (g/kg DM). 2.6. Chemical analysis All samples were dried at 60 °C for 24 h and ground to pass through a 1 mm diameter sieve before analysis. Dry matter (DM), crude protein (CP), crude fibre (CF), ether extract (EE) and ash were analyzed according to the standard methods of AOAC (1990), and CP content was calculated as nitrogen × 6.25. Amino acids (AA) were determined by high performance liquid chromatography using an ion exchange column (Amino Quant, 1990). NDF and acid detergent fibre (ADF) were determined by the method of Goering and Van Soest (1970). Chromium was determined by atomic absorption spectroscopy after ashing the samples (NMAM, 1994).
Table 3 Effects of breed (B), fibre level in diet (D) and enzyme supplementation (+ or −) on performance and the coefficient of ileal apparent digestibility in piglets. Factor
Performance DMI
Ileal apparent digestibility
ADG
FCR
OM
CP
EE
CF
NDF
ADF
Breed (B) MC 85 LY 78
213 312
1.93 1.55
0.76 0.74
0.75 0.75
0.54 0.53
0.18 0.17
0.22 0.21
0.17 0.16
Fibre level (D) L 78 H 80
268 257
1.70 1.78
0.77 0.74
0.76 0.73
0.54 0.52
0.19 0.16
0.22 0.21
0.18 0.16
Enzyme(E) − 79 + 79
250 274
1.79 1.69
0.74 0.77
0.73 0.76
0.52 0.54
0.17 0.18
0.21 0.22
0.16 0.18
B⁎D MC (L) MC (H) LY (L) LY (H)
84 86 72 74
217 209 318 305
1.89 1.98 1.50 1.60
0.77 0.75 0.76 0.73
0.76 0.74 0.76 0.73
0.55 0.52 0.54 0.52
0.19 0.17 0.18 0.16
0.23 0.21 0.22 0.20
0.18 0.16 0.17 0.16
B⁎E MC (−) MC (+) LY (−) LY (+)
85 76 73 73
205 221 295 329
1.96 1.90 1.62 1.48
0.75 0.77 0.73 0.76
0.74 0.76 0.73 0.76
0.53 0.55 0.52 0.54
0.17 0.19 0.17 0.18
0.21 0.23 0.20 0.22
0.16 0.18 0.15 0.17
D⁎E L (−) L (+) H (−) H (+) SE
78 78 79 81 1.071
264ab 271a 236b 279a 8.159
1.70 1.68 1.88 1.69 0.072
0.77a 0.76a 0.70b 0.77a 0.009
0.76a 0.76a 0.71b 0.76a 0.008
0.58 0.55 0.51 0.54 0.013
0.18a 0.19a 0.15b 0.18a 0.005
0.22a 0.22a 0.19b 0.22a 0.005
0.17a 0.18a 0.14b 0.17a 0.005
NS ⁎⁎ ⁎⁎ ⁎⁎
NS ⁎⁎ ⁎⁎ ⁎⁎
NS NS NS NS
NS ⁎⁎ ⁎⁎ ⁎
NS ⁎⁎ ⁎⁎ ⁎
NS ⁎⁎⁎ ⁎⁎⁎ ⁎
Significance ⁎⁎⁎ B
⁎⁎⁎
⁎⁎⁎
D E D⁎E
NS ⁎⁎ ⁎
NS NS NS
NS NS NS
Within a column and factor values with different letters are significantly different (P b 0.05); ⁎P b 0.05; ⁎⁎P b 0.01; ⁎⁎⁎P b 0.001; NS, non-significant. L, low-fibre diet; H, high-fibre diet; −, diet without enzyme supplementation; +, diet with enzyme supplementation; DMI, dry matter intake (g/kg metabolic body weight); ADG, average daily gain (g); FCR, feed conversion ratio (kg feed/kg gain).
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2.7. Statistical analysis
3.2. Ileal apparent digestibility
The data were analyzed statistically using the GLM procedure of Minitab Software, version 13.31 (Minitab, 2000). Treatment means which showed significant differences at the probability level of P b 0.05 were compared using Tukey's pairwise comparison procedure. The model used was as follows:
The coefficients of ileal apparent digestibility (CIAD) of nutrients are shown in Table 3. There were no significant differences in CIAD of nutrients between breeds (P N 0.05), although MC had higher numerical values of CIAD of all nutrients than LY. Fibre level and enzyme addition affected the CIAD of all nutrients (P b 001), with the exception of ether extract. In both breeds, enzyme supplementation of the lowfibre diet had no effect on CIAD, while there were considerable improvements for the high-fibre diet. The improvement in CIAD in the high-fibre diet of OM, CP, CF, NDF and ADF with enzyme supplementation was 6.4, 5.5, 2.9, 2.9 and 3.3% units, respectively (P b 0.01), while there was no effect of enzyme supplementation of the low-fibre diet. The CIAD of amino acids (AA) is shown in Table 4. The effects of breed, fibre level in the diet and enzyme addition on the CIAD of AA were similar to the effects on the CIAD of CP. The CIAD of AA was not different between the two breeds (P N 0.05). Fibre level in the diet had a negative effect, and enzyme supplementation had a positive effect on the CIAD of AA (P b 0.05). Supplementation of enzymes to the high-fibre diet improved the CIAD of almost all AA (P b 0.05), while this effect was not found on the low-fibre diet (P N 0.05). Among the essential AA, CIAD of histidine, methionine and lysine was higher than that of the other AA, while the CIAD of arginine, valine and leucine had the lowest values, with intermediate values for threonine, tyrosine, phenylalanine and isoleucine. Among the non-essential AA, the lowest CIAD was found for alanine, proline, and glycine, while the highest values were for glutamic acid, and with intermediate values for aspartic acid and serine.
Yijk = M + Bi + Dj + Ek + Bi × Dj + ðBi × Ek Þ + Dj × Ek + e Where Yijk is the growth performance or nutrient digestibility; M is the overall mean; Bi is the effect of breed i, Dj is the effect of fibre level, j; Ek is the effect of enzyme supplementation k; (Bi × Dj) is the interaction between breed i and fibre level j; (Bi × Ek) is the interaction between breed i and enzyme supplementation k; (Dj × Ek) is the interaction between fibre level j and enzyme supplementation k; e is the error. 3. Results 3.1. Performance The growth performance and feed conversion ratio (FCR) are shown in Table 3. The MC piglets had lower average daily gain (ADG) and poorer FCR (P b 0.05) but higher feed intake expressed as g/kg metabolic body weight than LY. Enzyme supplementation had a significant positive effect on ADG (P b 0.01). There was an interaction between diet and enzyme supplementation for ADG (P b 0.05), as the piglets fed the high-fibre diet supplemented with the enzyme mixture had 18% higher ADG compared to those fed the high-fibre diet without enzymes (P b 0.05), while there was no improvement in ADG and FCR in the piglets fed the low-fibre diet with enzyme supplementation (P N 0.05).
3.3. Total tract apparent digestibility Treatment effects on the CTTAD are shown in Table 5. In contrast to CIAD, there were significant differences in CTTAD of OM, CP, EE, CF, NDF and ADF between breeds, with higher
Table 4 Effect of breed (B), fibre level in diet (D) and enzyme supplementation (+ or −) on ileal digestibility of amino acids in piglets. Breed
Histidine Threonine Arginine Tyrosine Valine Methionine Phenylalanine Isoleucine Leucine Lysine Aspartic acid Glutamic acid Serine Alanine Proline Glycine
Fibre level
Enzyme
SE
MC
LY
L
H
−
+
0.80 0.73 0.72 0.75 0.70 0.77 0.73 0.73 0.72 0.76 0.74 0.80 0.72 0.71 0.66 0.70
0.79 0.72 0.71 0.74 0.70 0.77 0.73 0.74 0.72 0.77 0.74 0.79 0.72 0.71 0.76 0.70
0.80 0.74 0.73 0.77 0.71 0.78 0.74 0.74 0.73 0.78 0.75 0.80 0.73 0.72 0.77 0.71
0.77 0.71 0.70 0.73 0.69 0.76 0.72 0.73 0.71 0.75 0.73 0.78 0.71 0.70 0.74 0.69
0.77 0.71 0.70 0.73 0.69 0.76 0.71 0.68 0.71 0.75 0.75 0.78 0.71 0.69 0.75 0.69
0.80 0.74 0.72 0.77 0.71 0.78 0.75 0.78 0.73 0.78 0.73 0.81 0.74 0.72 0.77 0.71
0.054 0.081 0.068 0.033 0.068 0.068 0.034 0.061 0.066 0.058 0.063 0.073 0.044 0.005 0.075 0.053
⁎P b 0.05; ⁎⁎P b 0.01; ⁎⁎⁎P b 0.001; NS, non-significant. L, low-fibre diet; H, high-fibre diet; −, diet without enzyme supplementation; +, diet with enzyme supplementation.
Significance B
D
E
D⁎E
NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS NS
NS ⁎⁎ ⁎⁎⁎ ⁎⁎⁎ ⁎ ⁎ ⁎⁎ ⁎⁎ ⁎ ⁎⁎ ⁎ ⁎⁎ ⁎⁎
⁎ ⁎⁎ ⁎⁎⁎ ⁎⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎ ⁎⁎
NS ⁎
NS ⁎⁎ ⁎⁎
NS ⁎⁎ ⁎⁎ ⁎ ⁎⁎ ⁎⁎ ⁎ ⁎⁎
NS NS NS ⁎⁎ ⁎⁎ ⁎⁎ ⁎ ⁎⁎ NS ⁎ NS NS ⁎ ⁎
N.T. Len et al. / Livestock Science 126 (2009) 73–79
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Table 5 Effects of breed (B), fibre level in diet (D) and enzyme supplementation (+ or −) on the coefficient of total tract apparent digestibility in piglets.
NDF for LY was 2.0, 3.1, 3.0, 3.2, 3.0 and 2.2% units while for the MC it was 2.0, 1.1, 2.0, 1.4, 1.1 and 0.5% units, respectively.
Factor
OM
CP
EE
CF
NDF
ADF
4. Discussion
Breed (B) MC LY
0.87 0.83
0.83 0.80
0.65 0.60
0.55 0.49
0.55 0.51
0.43 0.41
Fibre level (D) L 0.86 H 0.84
0.83 0.80
0.64 0.61
0.53 0.52
0.54 0.52
0.43 0.41
Enzyme(E) − +
0.85 0.86
0.80 0.83
0.61 0.64
0.51 0.53
0.52 0.54
0.41 0.42
B⁎D MC (L) MC (H) LY (L) LY (H)
0.88 0.85 0.84 0.82
0.84 0.81 0.81 0.79
0.66 0.64 0.61 0.58
0.56 0.54 0.50 0.49
0.55 0.54 0.53 0.50
0.44 0.42 0.42 0.40
B⁎E MC (−) MC (+) LY (−) LY (+)
0.85 0.87 0.82 0.84
0.82 0.83 0.79 0.82
0.64 0.66 0.58 0.61
0.54 0.56 0.48 0.51
0.54 0.55 0.50 0.53
0.43 0.43 0.40 0.42
D⁎E L (−) L (+) H (−) H (+) SE
0.86a 0.86a 0.82b 0.86a 0.007
0.83a 0.83a 0.78b 0.82a 0.006
0.63a 0.64a 0.59b 0.63a 0.010
0.52a 0.53a 0.50b 0.53a 0.006
0.54a 0.55a 0.50b 0.54a 0.006
0.43a 0.42a 0.39b 0.43a 0.006
Significance B D E D⁎E
⁎⁎⁎ ⁎⁎ ⁎⁎ ⁎
⁎ ⁎⁎⁎ ⁎⁎ ⁎⁎
⁎⁎⁎ ⁎⁎ ⁎
⁎⁎⁎ ⁎ ⁎⁎ ⁎
⁎⁎ ⁎⁎ ⁎⁎ ⁎
⁎ ⁎⁎ ⁎ ⁎⁎
An increased level of dietary fibre to the weaned piglets did not affect feed intake or impair the ADG and FCR. Similar results were obtained in diets with cassava residue or rice bran as fibre sources in diets to weaned piglets of the same age (Len et al., 2009). However, increasing the fibre level in the diet resulted in a decrease in both the ileal and the total tract apparent digestibilities of OM, CP, CF, NDF, ADF and amino acids. This was in line with earlier studies on fibre inclusion in diets for weaned piglets (Högberg and Lindberg, 2004, 2006) and growing pigs (Noblet and Perez, 1993; Lindberg and Andersson, 1998; Le Goff et al., 2002; Len et al., 2007). However, the limitations of the slaughter technique used for determining ileal digestibility must be acknowledged, as there is a possibility of translocation of the digesta and shedding of the mucosal cells into the gut lumen, which would create an artifact in the determination of the composition of the ileal digesta (Fuller, 1991). The reduction in total tract digestibility of OM on diet H compared to diet L (0.4 units for each additional unit of CF) was much lower than reported by Lindberg and Andersson (1998) (2.0–2.7 units for each additional unit of CF), probably as a result of differences in the fibre components in the two studies. An additional factor could have been the inclusion of 3.5% soya oil in the high-fibre diet, as vegetable oils are known to be highly digestible (Freeman et al., 1968). It appears likely that both gut fill and the weight of the gastrointestinal tract (Jørgensen et al., 1996; Freire et al., 2003; Len et al., 2009) increased on the high-fibre diet. This would explain the unchanged ADG and FCR despite increased fibre intake (Högberg and Lindberg, 2006) and reduced nutrient digestibility. The improvement of nutrient digestibility in the high-fibre diet supplemented with an enzyme mixture, containing fibre degrading enzymes, may have been due to the disruption of intact cell walls and the release of entrapped nutrients (Hesselman and Åman, 1986). In addition, this may lead to the changes of physical properties of non-starch polysaccharides, such as reduced viscosity and water holding capacity, and to changes in the composition and concentrations of bacteria in the small and large intestine (Bedford and Classen, 1992; Jensen et al., 1998; O'Connell et al., 2005). The current results are in agreement with several previous studies (Inborr et al., 1993; Dierick and Decuypere, 1996; Diebold et al., 2004; Omogbenigun et al., 2004) and may be explained by a limited ability in young pigs to effectively utilize diets containing low quality ingredients with high-fibre content (Graham et al., 1988). However, with appropriate enzyme supplementation, this constraint can be alleviated, with a potential to improve the nutritional value of such diets for young pigs (Yin et al., 2001a,b, Omogbenigun et al., 2004) and for growing pigs (Kinh et al., 2001; Kinh et al., 2004). The extent and consistency of positive responses to enzyme supplementation in pigs varies, depending on a number of factors, such as age, physiological status, the capacity of the exogenous enzymes in the gut, and especially on the chemical composition of the diet. The interaction between enzyme supplementation and dietary fibre content in the present study could have been due
NS
Within a column and factor values with different letters are significantly different (P b 0.05). ⁎P b 0.05; ⁎⁎P b 0.01; ⁎⁎⁎P b 0.001; NS, non-significant. L, low-fibre diet; H, high-fibre diet; −, diet without enzyme supplementation; +, diet with enzyme supplementation.
values for MC (P b 0.05). Also, fibre level in the diet had a negative effect on CTTAD of OM, CP, CF, NDF, and ADF (P b 0.05), but not for CTTAD of EE (P N 0.05), while enzyme supplementation had a positive effect (P b 0.05). Overall, the supplementation of the enzyme mixture to the diet increased the CTTAD of OM, CP, EE, CF, NDF, and ADF by 1.1, 2.2, 2.5, 2.2, 2.1 and 1.4% units, respectively. The reduction of the CTTAD of OM, CP, CF, NDF and ADF with increased fibre content was 2.1, 2.5, 1.3, 2.4, and 1.6% units, respectively. Supplementation of enzymes to the high-fibre diet increased the CTTAD of OM, CP and fibre components (P b 0.05), while supplementation of the low-fibre diet had no effect (P N 0.05). The difference in the CTTAD of OM, CP, EE, CF, NDF and ADF between the highfibre diets with and without enzyme supplementation was 3.7, 4.3, 4.2, 3.7, 3.6 and 3.2% units, respectively. Although the interaction between breed and enzyme addition was not significant for CTTAD, the improvement of CTTAD of almost all nutrients in LY piglets fed diets with enzyme mixture was numerically higher than that in the MC. The improvement with enzyme addition of the CTTAD of OM, CP, EE, CF, NDF and
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to a change in the activity of the bacteria in the digestive tract of the piglets when fed a diet with enzyme supplementation. This is supported by the study of Garry et al. (2007) showing that enzyme supplementation to different cereal based pig diets resulted in changes in the activity of bacteria in the caecum and large intestine. A further possible explanation could have been the improvement of the morphology of small intestine with enzyme supplemented high-fibre diets, such as an increase of villus size in the small intestine. This was indicated by Mathlouthi et al. (2002) in a study with chickens fed with rye and maize based diets with and without xylanase and ß-glucanase supplementation. In the present study MC pigs had higher feed intake but lower ADG and thus poorer FCR than LY, mainly due to the different growth potentials of the breeds, as discussed previously (Len et al., 2008, 2009). The digestion of OM and dietary components in MC was higher than in LY, which is in agreement with previous findings that indigenous pig breeds can digest high-fibre diets more efficiently than exotic breeds. For example, Len et al. (2007) and Borin et al. (2005) indicated that the MC breed digested energy and dietary components more efficiently than LY, and concluded that fibrous diets are more appropriate for indigenous than for exotic pigs. Ndindana et al. (2002) concluded that the digestibility of diets containing graded levels of maize cobs was higher in indigenous Zimbabwean growing pigs than in an exotic breed (Large White). In a study performed by Fevrier et al. (1992), Chinese Meishan pigs digested highfibre diets more efficiently although there were no differences in digestibility between Chinese Meishan and Large White pigs fed low-fibre diets. Similarly, Freire et al. (2003) reported that Alentejano native young pigs utilized the cell wall components of the diet better than exotic breeds. Indigenous pigs in Southeast Portugal from an age of 21 days also showed a higher digestive potential towards fibrous dietary components than the Large White breed (Freire et al., 1998) and a higher activity of the microbial population present in the hindgut, which is particularly important for the degradation of dietary fibre (Bach Knudsen and Hansen, 1991). In contrast, Ly et al. (1998) found that the total tract digestibility of most dietary components in very fibrous diets was not higher in Cuban Creole than in Large White pigs. Kemp et al. (1991) also concluded that even when the diet was rich in fibre, the digestibility of CF in the indigenous Chinese Meishan was similar to the Dutch Landrace pigs. The lack of any effect of breed on ileal digestibility of amino acids in our study is in agreement with Hennig et al. (2004), who also found no differences in amino acid apparent ileal digestibilities between Minipigs and Saddleback pigs. 5. Conclusion It can be concluded that genotype had no influence on the ileal digestibility of OM, CP, CF, NDF, ADF and amino acids, whereas the total tract digestibility was higher for MC. Enzyme supplementation of the high-fibre diet improved the digestibility of all dietary components at the ileum and total tract, but there was no effect of enzyme supplementation of the low-fibre diet.
Acknowledgements The authors would like to thank Sida-SAREC (Swedish International Development Cooperation Agency — Department for Research Cooperation), through the regional MEKARN program and the Swedish University of Agricultural Sciences, Department of Animal Nutrition and Management, for their financial support of this study. Special thanks to the researchers in the Department of Animal Feeds and Nutrition of the National Institute of Animal Husbandry for their help in carrying out the study. Thanks also to Kemine Industries Pte Ltd for supplying the enzyme mixture. References Amino Quant (Operator, s Handbook). HP No 01090 90025, 1990. Printed in the Federal Republic of Germany. Hewlett Packard Company. AOAC, 1990. Official methods of analysis, Association of Official Analytical Chemists, Arlington, Virginia, 15th ed. Bach Knudsen, K.E., Hansen, I., 1991. Gastrointestinal implications in pigs of wheat and oat fractions. 1. Digestibility and bulking properties of polysaccharides and other major constituents. British Journal of Nutrition 65, 217–232. Bach Knudsen, K.E., Jørgensen, H., 2001. Intestinal degradation of dietary carbohydrates from birth to maturity. In: Lindberg, J.E., Ogle, B. (Eds.), Digestive Physiology of Pigs. CABI Publishing, Wallingford, pp. 109–121. Baidoo, S.K., Liu, Y.G., Yungblut, D., 1998. Effect of microbial enzyme supplementation on energy, amino acid digestibility and performance of pigs fed hulless barley based diets. Canadian Journal of Animal Science 78, 625–631. Bedford, M.R., Classen, H.L., 1992. Reduction of intestinal viscosity through manipulation of dietary rye and pentosanase concentration is effected through changes in the carbohydrate composition of the intestinal aqueous phase and results in improved growth rate and food conversion efficiency of broiler chicks. Journal of Nutrition 122, 560–569. Borin, K., Lindberg, J.E., Ogle, B., 2005. Effect of variety and preservation method of cassava leaves on diet digestibility by indigenous and improved pigs. Animal Science 80, 319–324. Chinh, B.V., Oanh, B.T., Ha, N.N., Viet, T.Q., Khang, D.T., Tinh, N.T., 2001. Chemical Composition and Nutritive Value of Animal Feeds in Vietnam. Agricultural Publishing House, Hanoi. Diebold, G., Mosenthin, R., Piepho, H.P., Sauer, W.C., 2004. Effect of supplementation of xylanase and phospholipase to a wheat-based diet for weanling pigs on nutrient digestibility and concentrations of microbial metabolites in ileal digesta and feces. Journal of Animal Science 82, 2647–2656. Diebold, G., Mosenthin, R., Sauer, W.C., Dugan, M.E.R., Lien, K.A., 2005. Supplementation of xylanase and phospholipase to wheat-based diets for weaner pigs. Journal of Animal Physiology and Animal Nutrition 89, 316–325. Dierick, N., Decuypere, J., 1996. Mode of action of exogenous enzymes in growing pig nutrition. Pig news and information 17, 41–48. Fang, Z.F., Peng, J., Liu, Z.L., Liu, Y.G., 2007. Responses of non-starch polysaccharide-degrading enzymes on digestibility and performance of growing pigs fed a diet based on corn, soya bean meal and Chinese double-low rapeseed meal. Journal of Animal Physiology and Animal Nutrition 91, 361–368. Fevrier, C., Bourdon, D., Aumaitre, A., 1992. Effects of level of dietary fibre from wheat bran on digestibility of nutrients, digestive enzymes and performance in the Large White and Chinese Meishan pigs. Journal of Animal Physiology and Animal Nutrition 68, 60–72. Freire, J.P.B., Peiniau, J., Cunha, L.F., Almeida, J.A.A., Aumaitre, A., 1998. Comparative effects of dietary fat and fibre in Alentejano and Large White piglets: digestibility, digestive enzymes and metabolic data. Livestock Production Science 53, 37–47. Freire, J.P.B., Guerreiro, A.J.G., Cunha, L.F., Aumaitre, A., 2000. Effect of dietary fibre source on total tract digestibility, caecum volatile fatty acids and digestive transit time in the weaned piglet. Animal Feed Science and Technology 87, 71–83. Freire, J.P.B., Dias, R.I.M., Cunha, L.F., Aumaitre, A., 2003. The effect of genotype and dietary fibre level on the caecal bacterial enzyme activity of young piglets: digestive consequences. Animal Feed Science and Technology 106, 119–130. Freeman, C.P., Holme, D.W., Annison, E.F., 1968. The determination of the true digestibilities of interesterified fats in young pig. British Journal of Nutrition 22, 651–660.
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