Abstract
A total of 96 finishing pigs [(Landrace × Yorkshire) × Duroc; 56.67 ± 2.69 kg] were used in a 10-week trial to evaluate the growth performance, nutrient digestibility, reduction of noxious gases, serum metabolites and meat quality. Pigs were allotted to dietary treatments based on body weight in a 2 × 2 factorial experiment, with the respective factors being fibre (low vs. high; 13.5, 16% non-starch polysaccharide, respectively) and benzoic acid (BA; 0, 0.5% BA) with six replicate pens consisting of four pigs per pen. Wheat bran and sugar beet pulp were used for dietary fibre sources with the level of 5%, respectively in the high fibre (HF) diet. All of the diets were mash type and formulated to contain net energy 9.80 MJ/kg and 16% crude protein. Throughout the experimental period, pigs fed HF diet had lower average daily gain than those fed low fibre (LF) diet (P = 0.02). However, fibre treatment did not affect the average daily feed intake. During the first five weeks, the apparent total tract digestibility (ATTD) of dry matter was higher in the pigs fed LF diet (P < 0.05). The ATTD of nitrogen and gross energy was increased when pigs fed LF included BA (P < 0.01 and P < 0.05, respectively). HF treatment showed the reduction of noxious gases such as NH3, R·SH and H2S detected at d 35 and 70 of this experiment (P < 0.05). Total cholesterol and low-density lipoprotein cholesterol were lower in the blood of pigs fed HF diet (P < 0.05). In the current study, marbling score was improved in the HF group compared to the LF group (P < 0.05). Finally, HF diet had an adverse effect on growth performance but a beneficial effect on reduction of noxious gas and cholesterol and meat quality.
Keywords:
1. Introduction
Dietary fibre (DF) is known as a vegetal origin material, resistant to hydrolysis by mammalian enzymes. This material has been reported that it has both beneficial and adverse effects on pigs. The beneficial effects of DF are ammonia emission reduction (Canh et al. Citation1998; Zervas & Zijlstra Citation2002; Nahm Citation2003), diarrhoea or constipation mitigation (Pierce et al. Citation2007; Wellock et al. Citation2008) and stereotype behaviour relaxation (Meunier-Salaun et al. Citation2001; Serena et al. Citation2009). Different kinds of fibre have negative effects on feed intake reduction and growth retardation due to early satiety and nutrient encapsulation (Graham et al. Citation1986; Zervas & Zijlstra Citation2002).
Microflora populations in the rumen are also responsible for DF digestion. If growth enhancing materials were added into the high fibre (HF) diets, the adverse effect on performance will be overcome. Benzoic acid (BA) is an acidifier, has antimicrobial activities (Knarreborg et al. Citation2002) and reduces gastrointestinal tract levels of lactic acid bacteria and Escherichia coli when fed to weanling pigs (Knarreborg et al. Citation2002; Guggenbuhl et al. Citation2007). Furthermore, BA can improve protein digestion (Risley et al. Citation1991), nitrogen (N) retention (Kluge et al. Citation2006) and weanling pig performance (Partanen & Mroz Citation1999; Kluge et al. Citation2006; Torrallardona et al. Citation2007). Previous studies indicated that the addition of 1%, 2% and 3% BA reduced NH3 emission (Hansen et al. Citation2007; Murphy et al. Citation2011), but nutrient digestibility was unchanged (Murphy et al. Citation2011). BA has also the possibility to reduce low-density lipoprotein (LDL) cholesterol due to its chemical similarity of niacin, which improves all lipoprotein abnormalities (Kamanna & Kashyap Citation2000).
The aim of this study was to investigate the interactive effect of DF and BA on the growth performance, nutrient digestibility, noxious gas emissions, serum metabolites and meat quality in finisher pigs.
2. Materials and methods
The experimental protocol used in this study was approved by the Animal Care and Use Committee of Dankook University.
2.1. Experimental design, animals and diets
Ninety six finisher pigs ([Landrace × Yorkshire] × Duroc) with an average initial body weight (BW) of 56.67 ± 2.69 kg were selected and were allotted to dietary treatments based on BW in a 2 × 2 factorial experiment. The factors were DF (low vs. high; 13.5% and 16.0% non-starch polysaccharide, respectively) and BA (0% and 0.5% BA, respectively) with six replicate pens consisting of four pigs per pen. Wheat bran and sugar beet pulp were included at 5% and 5%, respectively, as the sources of DF.
Experimental diets were conventional Korean diets mainly based on corn, wheat and soybean meal. This feed was produced at a commercial feed mill and provided as mash. All diets were formulated to contain net energy (NE) 9.80 MJ/kg and 16% crude protein (CP) (). Pigs were housed in an environmentally controlled facility with slatted plastic flooring and a mechanical ventilation system. Each pen was equipped with a single face self-feeder and a drinker nipple to allow pigs ad libitum access to feed and water throughout the experimental period.
Table 1. Compositions of the experimental diets for finishing pigs, as fed basis.
2.2. Sampling and measurements
Individual pig live weights and feed consumption of each pen were measured at the beginning, middle (35 d) and end (70 d) of the experimental period.
During d 28–35 and d 63–70, chromium oxide (Cr2O3) was added to the diets as an indigestible marker at 0.20% of the diet to measure digestibility. Fresh faecal grab samples were obtained from at least two pigs in each pen (one gilt and one barrow; 12 pigs per treatment) at d 34, 35, 69 and 70 to determine the apparent total tract digestibility (ATTD) of dry matter (DM), N and gross energy (E). All faecal and feed samples were stored at −20°C until analysed. Faecal samples were freeze-dried and ground to pass through a 1 mm screen. The feed and faecal samples were analysed for DM, N and E according to AOAC (Citation2000). Chromium was analysed by UV absorption spectrophotometry (Shimadzu UV-1201, Shimadzu, Kyoto, Japan) following the method described by Williams et al. (Citation1962).
On d 35 and 70, the urine and faeces from two pigs per pen were collected separately, four times a day for detecting gas emission. The urine was collected in a bucket via a funnel positioned below the cage. The faeces were collected in a plastic sample bag and sealed. The collected urine and faeces were stored immediately at −20°C and 4°C, respectively. The fresh faeces (300 g) were mixed with 300 mL of fresh urine (1:1, wt/vol) for each respective pig. The stock slurries were stored in 2.6 L plastic boxes in duplicate. Each box had a small hole in the middle of one side wall, which was sealed with adhesive plaster. The samples were allowed to ferment for a period of 24 h at room temperature (25°C). After the fermentation period, a Gastec (model GV-100) gas sampling pump was utilized for gas detection (Gastec Corp., Gastec detector tube No. 3 M and 3 La for NH3, No. 4 LL and 4 LK for H2S, No. 70 and 70 L for R·SH). Prior to measurement, the manure slurries were shaken manually for approximately 30 s in order to disrupt any crust formation on the surface of the slurry sample and to homogenize them. The adhesive plaster was punctured and 100 mL of headspace air was sampled approximately 2.0 cm above the faeces surface. After air sampling, each box was again covered with adhesive plaster. Headspace measurement was repeated at d 1, 3, 5 and 7. Our previous study also confirmed this procedure (Zhao et al. Citation2013).
Two pigs were randomly selected from each pen and bled via jugular venipuncture at d 35 and 70. Blood samples were collected in 5 mL K3EDTA coated tubes (Becton Dickinson Vacutainer Systems, Franklin Lakes, NJ, USA). The blood samples were then centrifuged at 2000 × g at 4°C for 20 min within one hour after collection to separate the serum. The concentrations of total, LDL and high-density lipoprotein (HDL) cholesterol, non-esterified fatty acids (NEFA) and triglyceride (TG) in the serum samples were analysed with an automatic biochemical analyser (RA-1000, Bayer Corp., Tarrytown, NY) using colorimetric methods.
At the end of the experiment, pigs were slaughtered at a local commercial slaughterhouse. After chilling at 2°C for at least 24 h, piece of the right loin sample was removed between the 10th and 11th ribs. Sensory evaluation (colour, marbling and firmness score) was conducted according to the National Pork Producers Council Standards (NPPC Citation2000) at ambient temperature. Immediately after the subjective tests were conducted, the lightness (L*), redness (a*) and yellowness (b*) values were measured at three locations on the surface of each sample using a Model CR-410 Chroma meter (Konica Minolta Sensing, Inc., Osaka, Japan).
At the same time, duplicate pH values of each sample were directly measured using a pH meter (Pittsburgh, PA, USA). The water holding capacity (WHC) was measured in accordance with the methods described by Kauffman et al. (Citation1986). Briefly, a 0.3 g sample was pressed at 3000 psi for 3 min on a 125-mm-diameter piece of filter paper. The areas of the pressed sample and the expressed moisture were delineated and then determined using a digitizing area-line sensor (MT-10S; M.T. Precision Co. Ltd., Tokyo, Japan). The ratio of water:meat area was calculated, giving a measure of WHC (a smaller ratio indicates increased WHC). The longissimus muscle (LM) area was measured by tracing the LM surface at the 10th rib, which was conducted using the aforementioned digitizing area-line sensor. Drip loss was measured using approximately 2 g of meat sample at d 1, 3, 5 and 7 after slaughter according to the plastic bag method described by Honikel et al. (Citation1986). Cook loss was determined as described by Sullivan et al. (Citation2007).
2.3. Statistical analyses
Data were analysed as a completely randomized 2 × 2 factorial design using the General Linear Model procedure of SAS (SAS Institute Inc., Cary, NC, Citation2009). The pen was considered as experimental unit. The final model included the main effects of DF and BA as well as the interaction between DF and BA. Data were reported as means ± standard error and was considered significant when P < 0.05.
3. Results
3.1. Growth performance and nutrient digestibility
The growth performance and apparent nutrient digestibility are shown in and . During 0–5 weeks and 0–10 weeks, pigs fed low fibre (LF) diet grew faster than those fed HF diet (P = 0.007 and P = 0.022, respectively). However, average daily feed intake (ADFI) was not significantly affected by treatment. Therefore, the gain/feed (G/F) of pigs fed HF diet were lower (P = 0.044) than those fed LF diet. There were not any significantly differences in average daily gain (ADG), feed consumption and G/F in BA treatment and interaction between DF and BA.
Table 2. Effects of DF and BA on growth performance in finishing pigs.
Table 3. Effects of DF and BA on the ATTD (%) in finishing pigs.
The ATTD of DM of LF group was higher than HF group (P = 0.010) on d 35. There were interactive (P = 0.048) effect on ATTD of DM between the levels of fibre and BA. In the second half of this test, the interactive effect between different levels of fibre and BA on N and E digestibility was significant (P = 0.0009 and P = 0.022, respectively). And also, N digestibility of pigs fed 0.5% BA was improved (P = 0.011) compared with those fed without BA.
3.2. Noxious gas emission from slurry
Pigs fed with HF diet had lower NH3, R·SH and H2S level (P < 0.05) at d 35 and 70 (). Addition of BA in finishing diet significantly increased R·SH and H2S emission at d 35 and increased NH3, R·SH and H2S emission at d 70 (P < 0.05). However, a significant interaction effect between DF and BA was not observed on the NH3, R·SH and H2S emission.
Table 4. Effect of DF and BA on noxious gas emission (ppm) in the manure of finishing pigs.
3.3. Serum metabolites
The differences were observed on the content of cholesterol, LDL and NEFA by different levels of DF (). At d 35, the cholesterol level of pigs fed with HF diet was lower than that of pigs fed with LF diet (P < 0.05). In similar with cholesterol, HF treatment was lower (P < 0.05) in LDL than LF treatment both at d 35 and 70. NEFA was higher in HF (P < 0.05) than that in LF.
Table 5. Effect of DF and BA on serum metabolites of finishing pigs.
3.4. Meat quality
The effects of dietary treatments on the meat quality were presented in . In the current study, sensory evaluation revealed that marbling score was improved (P < 0.05) in the HF group compared to the LF group. Furthermore, drip loss at d 1 was significantly lower (P < 0.05) in pigs fed with HF diet. Drip loss was lower (P < 0.05) at d 5 in meat of pigs fed diets added with BA. In terms of BA supplementation, meat colour was less (P < 0.05) red in pigs that received diets supplemented with BA. And pH was lower (P < 0.05) in BA supplemented group.
Table 6. Effects of DF and BA on the meat quality of finishing pigs.
4. Discussion
4.1. Growth performance and nutrient digestibility
There has been increasing interest in the use of HF feed diets for pigs from an economic and social perspective. However, previous study reported negative effects of fibre on growth performance of pigs and nutrient digestibility of feed due to the chemical and physical properties of the fibre source (Graham et al. Citation1986). An increase of soluble DF in the diet impinges on total nutrient digestion and absorption (Wilfart et al. Citation2007). Furthermore, the retention time of digesta in the stomach increases in the presence of DF (Wenk Citation2001), causing earlier satiety. A study of the effects of dietary protein and fermentable fibre in grower pigs reported that E and N digestibility was reduced when pigs were fed 15% of soy hull or 20% of sugar beet pulp, growth performance reduced when pigs fed 15% soy hull diet (Zervas & Zijlstra Citation2002). In a cannula study, Anguita et al. (Citation2006) found that the ileal effluent of digesta increased from 19.9% to 46.8% of feed, leading to a reduction in the energy digested at the terminal ileum, from 15 to 11 MJ/kg of feed DM. Similar to previous studies, pigs fed high DF diet in the current study had lower BW gain compare to those fed low DF diet, especially in the first five weeks. As well, DM digestibility of HF group was lower than LF group in the same period. However, the DF level did not affect feed intake of pig in this trial, which might be inferred that feed intake was not influenced, but that digestibility and growth rate were affected, perhaps because we used a relatively low quantity of DF and treated soluble and insoluble DF at the same diet.
Dietary addition of BA resulted in a numerical increase of average daily weight gain and a remarkable and significant improvement of feed conversion (den Brok et al. Citation1999; Yan & Kim Citation2013). However, we found that BA did not affect pig performance and apparent digestibility of nutrient except for N digestibility at d 70, and also did not make an impact on compensating for the reduced growth performance in the HF group. These results might be derived from that we used relatively high-density commercial diets for this test.
4.2. Noxious gas emission from slurry
Surveys have been undertaken with the goal of reducing ammonia emissions in pig husbandry through diet manipulation (Canh et al. Citation1998; Mroz et al. Citation2000; Panetta et al. Citation2006; Botermans et al. Citation2010). One of these approaches involved feeding high fermentable fibre to pigs. DF lowered the pH of the slurry for short-chain fatty acids (SCFAs) production, hence reducing urease activity. Furthermore, DF may influence the reduction of decomposable N content in the urine by N repartitioning. Canh et al. (Citation1998) surveyed male hybrid pigs with a BW of 80–90 kg; the pH of the slurry from pigs fed the sugar beet pulp-based diet was 0.8 unit lower and ammonia emission was 52–53% lower than that of barley–wheat, tapioca and barley–tapioca based diets. When the N repartitioning effect was conducted, urinary N:faecal N ratios in manure of pigs fed diets with tapioca, soybean hulls and beet pulp were 2.09, 1.35 and 1.67, respectively (Mroz et al. Citation2000).
Another approach for reducing ammonia emission is to reduce the pH in the urine by adding BA in the diet. BA is metabolized in the liver and converted into hippuric acid via conjugation with the amino acid glycine. It was reported that the increased excretion of hippuric acid in pig urine resulted in its direct acidification (den Brok et al. Citation1999). Aarnink et al. (Citation2008) reported that the addition of 1% BA into the diet reduced 16% of ammonia emission and dropped pH from 6.50 to 5.29 in the pig manure. In the present work, the ammonia content in the manure from pigs fed a BA-treated diet was higher than those from pigs fed a diet free of BA (19.10 ppm vs. 17.65 ppm). This result was not expected and may reflect differences of N digestibility between those two groups.
4.3. Serum metabolites
The effect of DF on the reduction of cholesterol was reported in animal (Collings et al. Citation1979; Graham et al. Citation1986; Shen et al. Citation1998) as well as human (Kendall et al. Citation2010). Kendall et al. (Citation2010) provided a detailed and comprehensive report on the link between DF and human health. An overall 1% reduction in serum levels of LDL cholesterol corresponded to a 1–2% reductions in occurrence of coronary heart disease events. Graham et al. (Citation1986) observed in animal models that DF such as wheat bran and sugar beet pulp decreased small intestinal lipid absorption. Collings et al. (Citation1979) found that the serum cholesterol level was decreased in male growing pigs when more than 10% of wheat middlings was replaced in corn-soybean diets. DF binds to bile acids in the small intestine, which makes them less likely to enter the body, decreases intestinal lipid absorption and subsequently reduces the level of cholesterol in the blood (Graham et al. Citation1986; Wilfart et al. Citation2007; Anderson et al. Citation2009). DF had an influence on hepatic enzyme activity and lipid receptor sensitivity and reduced blood cholesterol (Shen et al. Citation1998). DF not digested in the small intestine can be fermented by microbes in the large intestine. When DF is fermented, SCFAs including propionic acid, butyric acid and acetic acid are produced. SCFAs suppress cholesterol synthesis by the liver and reduce the blood levels of LDL cholesterol and TG (Wong et al. Citation2006). It increased the capacity of the intestine for oxidative metabolism and induced a repartitioning of body lipid stores via mobilization of NEFA (Weber & Kerr Citation2012). NEFA differed depending on the content of DF. These observations partially agree with the findings of Weber and Kerr (Citation2012). The author divided three groups of pigs into corn-soybean control, sugar beet pulp and wheat bran treatment, and found that sugar beet pulp treatment increased NEFA, while wheat bran treatment did not.
In the present study, a decrease of total and LDL cholesterol and an increase of NEFA were found in the serum of pigs fed HF diet. However, serum TG was not affected by the dietary level of DF. It may be that, even though DF decreased dietary lipid absorption, liver TG can be mobilized into the blood under low lipid absorption, increasing circulating lipids, which provides a substrate for the increase in oxidative metabolism.
In our experiment, BA supplementation did not affect the serum metabolized. However, BA has supposed to reduce the serum cholesterol as BA acts like niacin which has ability to decrease the blood TG levels and eventually reduce LDL cholesterol through increasing hepatic breakdown of Apo-B. Niacin has long been used for the treatment of lipid disorders and cardiovascular disease in human. Niacin rapidly decreases the TG levels in humans by inhibiting the release of fatty acids from adipose tissue as well as hepatic synthesis of fatty acids and TG (Kamanna & Kashyap Citation2000). Reduced TG synthesis is postulated to enhance hepatic degradation very low of Apo-B, the major lipoprotein component of very low-density lipoprotein (VLDL), thereby reducing VLDL production and LDL in the body (Jin et al. Citation1999). The reduction in TG availability also results in production of smaller, TG-poor VLDL particles, with subsequent inhibits the production of small, dense LDL particles. Niacin may elevate HDL-cholesterol levels primarily by suppressing the hepatic removal of Apo A-I, which increases levels of Apo A-I as well as large Apo A-I containing HDL particles (Jin et al. Citation1997). Niacin is excreted in the form of nicotinuric acid conjugated with glycine. BA has a structural and metabolic similarity to niacin. BA is rapidly absorbed (Schanker et al. Citation1958) and is rapidly and completely excreted in the urine by conjugation with glycine (Schachter Citation1957). The maximum urinary excretory rate achieved depends on the dose of BA given and limitations in availability of glycine (Quick Citation1933). The similarity in the structure and excretion mechanism of niacin and BA support the view that, BA may help decrease LDL cholesterol in the blood. However, despite of these similarities, the difference of serum metabolites did not affected by addition of 0.5% BA in the present work. Hence, more researches are needed to evaluate the effect of BA on serum metabolites on finishing pigs.
4.4. Meat quality
Despite the many studies conducted with DF, its influence on pork quality is unclear. DF may reduce objectionable odours such as skatole by preventing N absorption and reducing the occurrence of pale, soft and exudative meat by the reduction of glycogen. Reduced muscle glycogen concentration at slaughter reduces the formation of lactic acid during the post-slaughter conversion of muscle to meat (Gierus & Rocha Citation1997). Reduced lactic acid formation drives the rapid drop in pH. Furthermore, both pale colour and WHC are related to low ultimate pH in the meat (Ledward Citation1992; den hertog-meischke et al. Citation1997). A post-mortem study Rosenvold et al. (Citation2001) reported that, muscle glycogen reserves were reduced in LM by 11–26% at the time of slaughter, with higher L* values evident in pigs fed a HF diet than in pigs fed a barley–soybean control diet. However, no difference in the ultimate pH was evident. DF may also influence the reduction of back fat thickness by preventing lipid absorption in the gut. In the present work, marbling score was improved by 12.3% in the meat from pigs fed a high DF diet. This improvement may be because the HF diet had more fat content. Friend et al. (Citation1988) suggested a similar parallel between the loin fat content and the dietary fat content. This relationship was also confirmed by Fortin et al. (Citation2005); marbling scores increased in the loins from pigs fed high-fat diet. In the present study, increased fibre level did not affect the ultimate pH, meat colour and WHC. DF prevents the digestion and absorption of glucose and impacts the level of glucose and glycogen synthesis. Remained relatively low level of glycogen in the muscle prevents to produce lactic acid from glycogen and holds the sudden pH drop of muscle after slaughter (Gierus & Rocha Citation1997).
The addition of BA had a tendency to improve (P = 0.0659) marbling score in this survey. The reason of this effect was not clear. We expected that the conversional mechanism of BA in the body slightly influenced the lipid metabolism. The addition of BA had a negative effect on reducing pH of pork in the present work. This was caused by the conversion into hippuric acid via conjugation with the amino acid glycine.
5. Conclusion
In summary, the addition of 50 g of sugar beet pulp and 50 g of wheat bran as a source of DF per kg of finisher pig feed slightly affected growth performance, but appreciably reduced noxious gases and serum cholesterol level and improved meat quality. However, the addition of 0.5% BA did not improve any assessed character. Thus, moderate levels of DF would be beneficial in improving pig health and meat quality.
Funding
This work was carried out with the support of Cooperative Research Program for Agriculture Science & Technology Development (Project No. 008494), Rural Development Administration, Republic of Korea.
Additional information
Funding
References
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