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Animal Science Journal (2015) 86, 610–616
doi: 10.1111/asj.12334
ORIGINAL ARTICLE Effects of beet pulp supplementation on growth performance, fecal moisture, serum hormones and litter performance in lactating sows Pinyao ZHAO,1 Zhengfan ZHANG2 and In Ho KIM1 1
Department of Animal Resource and Science, Dankook University, Cheonan, Choongnam, South Korea and College of Life Science and Technology, Southwest University for Nationalities, Chengdu, China
2
ABSTRACT This study was conducted to evaluate effects of beet pulp supplementation on growth performance, fecal moisture, serum hormones and litter performance in lactating sows. Ninety primiparous sows (Landrace × Yorkshire) were randomly allotted to one of three dietary treatments in a 21-day trial starting 3 days before parturition. The three dietary treatments were supplemented with 0, 10 and 20% beet pulp, respectively. Backfat loss and fecal moisture content were increased (P < 0.05), where cortisol and norepinephrine levels were decreased (P < 0.05) in sows fed beet pulp supplementation diets compared with control diet, but there was no difference between 10% and 20% beet pulp supplementation treatments. No effect was observed on bodyweight, average daily intake, weaning to estrus interval, epinephrine level in sows and litter weight, litter size, survivability in piglets among dietary treatments. Taken together, beet pulp supplementation has no significant effect of growth performance of lactating sows and piglets with decreased cortisol and norepinephrine levels in lactating sows, but it can increase fecal moisture content which is beneficial for sow feces excretion.
Key words: beet pulp, fecal moisture, growth performance, lactating sow, serum hormones.
INTRODUCTION Dietary fiber is the indigestible portion of plant foods comprised of soluble and insoluble fiber (Menezes et al. 2004). Soluble fiber is readily fermented in the colon into gases and physiologically active by-products, whereas insoluble fiber is metabolically inert, absorbing water as it moves through the digestive system and easing defecation (Trumbo et al. 2002). Dietary fiber acts by changing the nature of the gastrointestinal tract contents and by changing how other nutrients and chemicals are absorbed (Eastwood & Kritchevsky 2005). Higher fiber diets are commonly fed to gestating sows to improve sow behavior (Matte et al. 1994; Ramonet et al. 1999; Guillemet et al. 2006). Feeding a high-fiber diet during gestation increases voluntary feed intake during lactation (Dourmad et al. 1996; Farmer et al. 1996; Quesnel et al. 2009) and improves sow litter performance (Matte et al. 1994; Ramonet et al. 1999; Danielsen & Vestergaard 2001). Sugar beet pulp is a by-product from sugar beet processing, which is used as fodder for horses and other livestock (Togrul & Arslan 2003; MirzaeiAghsaghali et al. 2011). Despite being a by-product of © 2014 Japanese Society of Animal Science
sugar beet processing, sugar beet pulp is high in energy and fiber (Warren 2007). Sugar beet pulp has great estimated net energy value (13.4 kJ/g) for sows because the non-starch polysaccharides in sugar beet pulp are utilized in the large intestine for energy by sows as efficiently as the energy from digested starch (Rijnen et al. 2001). Most studies reporting the effects of dietary fiber on physical activity have used sugar beet pulp as the fiber source (Brouns et al. 1994; Braud et al. 1998; Ramonet et al. 2000). As we know, it is a big challenge for sows during lactation and they will cope with severe stress. The concentration of cortisol, epinephrine and norepinephrine in serum is a criterion that reflects stress intensity (Webel et al. 1997). However, not enough studies have been conducted to evaluate the use of beet pulp in lactating sows. Additionally, we wondered if beet pulp could reduce stress
Correspondence: In Ho Kim, Department of Animal Resource and Science, Dankook University, Cheonan, Choongnam 330-714, South Korea. (Email: inhokim@ dankook.ac.kr) Received 19 May 2014; accepted for publication 7 August 2014.
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during lactation or improve sow and piglet growth performances. The objective of this study was to evaluate effects of beet pulp supplementation on growth performance, fecal moisture, serum hormones and litter performance in lactating sows.
MATERIALS AND METHODS The experimental protocol used in this study was approved by the Animal Care and Use Committee of Dankook University, which is comparable to those laid down by the Canadian Council on Animal Care.
Experimental design, animals and housing A total of 90 primiparous sows (Landrace × Yorkshire) were used in this experiment. On day 110 of gestation, sows were weighed and moved into the farrowing facility, randomly allotted to one of three dietary treatments, and fed 2.5 kg/ day feed to allow for adjustment to the lactation diets before parturition. Experimental treatments contained three levels of beet pulp: (i) CON, basal diet; (ii) BP1, contain 10% beet pulp; and (iii) BP2, contain 20% beet pulp. The different ingredients in three dietary treatments were adjusted in an attempt to provide isonitrogenous and isoenergetic rations. Dietary nutrients were formulated to meet or exceed the NRC (1998) recommendations (Table 1). The chemical composition of sugar beet pulp is presented in Table 2. Sows were housed in farrowing crates (2.1 m × 0.6 m) which contained an area (2.1 m × 0.6 m) for newborn piglets on each side, and the temperature in the farrowing house was maintained at a minimum of 20°C. Heat lamps were provided for piglets. Piglets were treated according to routine management practices that included teeth clipping, tail docking, ear notching and subcutaneous iron dextran injections (1 mL per pig) within 24 h of birth. After farrowing, daily feed allowance increased gradually and sows had ad libitum access to feed by day 6. Sows were provided with free access to drinking water throughout the experimental period. The piglets received no creep feed.
Sampling and measurements Three experimental diets were analyzed for crude protein (method 990.03), crude fiber (method 962.09), crude ash (method 942.05), acid detergent fiber (method 973.18), calcium and phosphorus (method 985.01) as described by AOAC (2007), and neutral detergent fiber (Holst 1973). The ammonia acid profile of diets was analyzed using a Sykam Amino Acid Analyzer (Sykam-S7130; Tokyo, Japan) and high-performance liquid chromatography (HPLC) after acid hydrolysis for 24 h in 6N HCl. Methionine was analyzed as Met sulfone after cold performic acid oxidation overnight before hydrolysis and tryptophan was determined after NaOH hydrolysis for 22 h at 110°C. Individual sow was weighed and scanned for backfat thickness within a few hours after day of farrowing and on day 21 of lactation to determine weight and backfat loss. The backfat thickness of the sows (6 cm off the midline at the 10th rib) was measured using a real-time ultrasound instrument (Piglot 105; SFK Technology, Herlev, Denmark). During the experimental period, numbers of piglets alive and death per litter were recorded to calculate survival ratio. Individual pig weight was recorded at birth and weaning Animal Science Journal (2015) 86, 610–616
Table 1
Composition of experimental diets (as-fed basis)
Item
CON
BP1
BP2
Ingredient, % Corn 51.28 44.96 35.22 Soybean meal (47% crude protein) 24.47 21.60 21.00 Beet pulp – 10.00 20.00 Wheat bran 4.03 3.73 3.73 Rapeseed meal 2.50 2.50 3.00 Rice bran 5.00 4.58 4.48 Tallow 6.00 6.00 6.00 Molasses 3.50 3.50 3.50 Dicalcium phosphate 1.64 1.58 1.54 Limestone 0.76 0.73 0.71 Salt 0.50 0.50 0.50 Lysine (98%) 0.12 0.12 0.12 Vitamin premix† 0.10 0.10 0.10 Mineral premix‡ 0.10 0.10 0.10 Calculated compositions, % Metabolic energy, MJ/kg 3.41 3.43 3.43 Crude protein 17.10 17.11 17.13 Crude fat 9.10 9.16 9.13 Lysine 1.00 0.99 0.97 Calcium 0.78 0.83 0.85 Phosphorus 0.69 0.70 0.73 Analyzed compositions, % Crude protein 17.12 17.10 17.05 Crude fat 9.13 9.15 9.12 Lysine 1.00 0.99 0.98 Threonine 0.68 0.66 0.65 Isoleucine 0.67 0.66 0.65 Methionine 0.25 0.24 0.24 Calcium 0.81 0.84 0.86 Phosphorus 0.71 0.71 0.72 Neutral detergent fiber 9.75 12.54 14.87 Acid detergent fiber 5.07 9.46 13.82 †Provided per kilogram of complete diet: vitamin A, 10 000 IU; vitamin D3, 2000 IU; vitamin E, 48 IU; vitamin K3, 1.5 mg; riboflavin, 6 mg; niacin, 40 mg; d-pantothenic, 17 mg; biotin, 0.2 mg; folic acid, 2 mg; choline, 166 mg; vitamin B6, 2 mg; and vitamin B12, 28 μg. ‡Provided per kilogram of complete diet: Fe (as FeSO4·7H2O), 90 mg; Cu (as CuSO4·5H2O), 15 mg; Zn (as ZnSO4), 50 mg; Mn (as MnO2), 54 mg; I (as KI), 0.99 mg; and Se (as Na2SeO3·5H2O), 0.25 mg.
Table 2 Chemical composition (% dry matter (DM)) of sugar beet pulp
Item
Unit
Value
DM Crude protein Crude fiber Acid detergent fiber Neutral detergent fiber Lignin Ether extract Ash Starch Total sugars Gross energy
% as fed % DM % DM % DM % DM % DM % DM % DM % DM % DM MJ/kg DM
88.5 9.1 18.7 23.5 47.6 2.2 0.8 7.6 0.9 7.4 17.1
(day 21 of lactation) to determine weight gain. After farrowing, daily feed allowance increased 1 kg/day until day 6 postpartum, and then sows were given ad libitum access to feed and water. During lactation, feed consumption was © 2014 Japanese Society of Animal Science
612 P. ZHAO et al.
recorded for each sow to calculate average daily feed intake. After weaning, weaning to estrus interval was recorded for each sow. Samples of feces were collected (one collection per sow) for the determination of moisture content. Total moisture was determined by air-drying the collection at 60°C, followed by an equilibration and moisture determination at 105°C (Harris 1970). At day 21 of lactation, blood samples were collected from the cervical vein into non-heparinized vacuum tubes (Becton Dickinson Vacutainer Systems, Franklin Lakes, NJ, USA) of each sow at the same time of the day. Blood samples were collected before meals and after removal of piglets. After collection, the serum samples were centrifuged (3000 × g) for 30 min at 4°C and stored at −20°C until being used in cortisol, norepinephrine and epinephrine analysis. Serum concentrations of cortisol were determined with a standardized solid phase radioimmunoassay kit (Diagnostic Products Corporation, Los Angeles, CA, USA). The norepinephrine and epinephrine were assayed using an ionexchange purification procedure followed by liquid chromatography with electrochemical detection, as described previously by Hay and Mormède (1997). In brief, the samples were loaded onto cationic columns and the catecholamines were eluted with boric acid. The eluates were assayed via HPLC with electrochemical detection with an oxidizing potential of +0.65V. The intra- and inter-assay coefficients of variation (CV) were 7.0% and 7.1% for norepinephrine and 6.5% and 11.6% for epinephrine, respectively.
Statistical analyses All experimental data were analyzed using the GLM procedure of SAS (2001) as a randomized complete block design (SAS Inst. Inc., Cary, NC, USA) according to their body weight (BW). The sow or litter of piglets was used as the experimental unit. The analysis of sow backfat thickness and change during lactation used fat depth at farrowing as covariates. Piglet birth weight was used as covariates for weaning weights during lactation. Lactation length was used as a covariate for piglet survivability, sow and piglet weaning weight, sow feed intake, and weaning to estrus interval and backfat thickness depth change. The initial values were used as a covariate for blood profiles. Orthogonal contrasts were used to the effect of treatments: CON versus BP1 + BP2 and
BP1 versus BP2 treatments. Variability in the data was expressed as the pooled standard error (SE) and a P < 0.05 was considered as significant.
RESULTS Growth performance of sows and piglets During lactation, backfat loss was increased (P < 0.05) in sows fed beet pulp supplementation diets compared with sows fed CON diet (Table 3). Sow bodyweight loss, feed intake, and weaning to estrus interval were not affected (P > 0.05) by beet pulp supplementation. In addition, litter weaning weight and the number of pig survivals were not different (P > 0.05) among dietary treatments (Table 4). No difference (P > 0.05) was observed in backfat loss, BW loss, feed intake, weaning to estrus interval of sows, litter weight and survivability of piglets between BP1 and BP2 treatments.
Fecal moisture content and serum hormones of sows Sows fed diets containing beet pulp had higher (P < 0.05) fecal moisture content than those fed CON diet, but there was no difference (P > 0.05) between BP1 and BP2 treatments (Table 3). Sows fed diets containing beet pulp had lower (P < 0.05) cortisol and norepinephrine levels than those fed CON diets (Table 5). However, no effect (P > 0.05) was observed in cortisol and norepinephrine levels between BP1 and BP2 treatments. In addition, there was no differences (P > 0.05) in epinephrine levels among dietary treatments.
DISCUSSION Sow BW losses during lactation were greater in sows fed a high-fiber diet compared with those fed a CON diet (Guillemet et al. 2006). Baudon and Hancock (2003) reported that a better energy balance might be
Table 3 Effect of beet pulp supplementation on performance and fecal moisture content in lactating sows†
Item
Sow bodyweight, kg At parturition At day 21 of lactating Bodyweight loss Backfat thickness, mm At parturition At day 21 of lactating Backfat loss Average daily feed intake, kg Weaning to estrus interval, days Fecal moisture content, %
CON
223.3 213.5 9.8 17.5 15.8 1.7 6.18 6.0 69.44
BP1
221.8 211.7 10.1 20.1 17.7 2.4 5.80 4.0 73.48
BP2
218.5 204.2 14.3 21.5 18.9 2.6 6.09 5.6 74.48
SE‡
P-value CON vs. BP1 + BP2
BP1 vs. BP2
7.45 11.39 2.62
0.21 0.34 0.17
0.28 0.44 0.21
1.19 1.32 0.19 0.31 0.77 0.81
0.09 0.08 0.02 0.12 0.08 0.04
0.41 0.26 0.07 0.14 0.07 0.15
†CON, basal diet; BP1, CON + 10% beet pulp; BP2, CON + 20% beet pulp. ‡Standard error.
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Table 4
Effect of beet pulp supplementation on performance in piglets†
Item
CON
Litter weight, kg Initial Final Weight gain Litter size Initial Final Survivability, %
BP1
BP2
SE‡
P-value CON vs. BP1 + BP2
BP1 vs. BP2
14.42 66.38 51.96
17.05 71.00 53.95
15.66 70.90 55.24
2.08 4.94 2.53
0.13 0.31 0.26
0.21 0.38 0.14
10.42 10.42 100.00
10.95 10.25 93.61
11.24 10.00 89.00
0.69 0.82 5.08
0.14 0.19 0.34
0.18 0.09 0.29
†CON, basal diet; BP1, CON + 10% beet pulp; BP2, CON + 20% beet pulp. ‡Standard error.
Table 5
Effect of beet pulp supplementation on serum hormones in lactating sows†
Item
Cortisol, μg/dL Epinephrine, pg/mL Norepinephrine, pg/mL
CON
3.70 40.64 186.5
BP1
2.78 36.28 171.8
BP2
SE‡
2.92 37.50 173.1
0.24 1.25 6.47
P-value CON vs. BP1 + BP2
BP1 vs. BP2
0.03 0.24 0.02
0.13 0.22 0.42
†CON, basal diet; BP1, CON + 10% beet pulp; BP2, CON + 20% beet pulp. ‡Standard error.
expected to decrease bodyweight loss by sows during the lactation period. However, Hill et al. (2008) reported that sows fed a basal diet with 5% beet pulp or a basal diet with 15% distillers dried grains with solubles had similar bodyweight loss during the lactation period. In our study, no differences were found in BW loss during the lactation period. Che et al. (2011) showed that sows fed a low-fiber diet during parity 1 gained more backfat during gestation but lost more during lactation than sows fed a high-fiber diet. This was different from our results about backfat loss. In our research, sows fed beet pulp diets which were high in fiber lost more backfat than sows fed the basal diet. Similar results as ours were reported by Peet-Schwering et al. (2003), that sows fed a high level of dietary fermentable non-starch polysaccharides during lactation lost more backfat during lactation than sows fed a starch diet. As reported by Maes et al. (2004), sow backfat could reflect nutrient retention and potential reproductive efficiency. The higher inclusion of fiber decreased the digestibility of dry matter, energy and nitrogen (Ramonet et al. 1999; Holt et al. 2006; Renteria-Flores et al. 2008), and feed intake (Brouns et al. 1997; Braud et al. 1998; Ramonet et al. 2000) of a gestating diet. These factors rmean that sows needed to increase metabolic rate of body reserves to maintain health and survival, which led to an increased backfat loss. In addition, it was likely that parity also had effect on backfat loss during the gestation period. Che et al. (2011) reported that sows in parity 1 fed a low-fiber diet lost more backfat during lactation than sows fed a high-fiber diet, while in Animal Science Journal (2015) 86, 610–616
parity 2, sows receiving high-fiber diet did not lose backfat during lactation compared with sows receiving low-fiber diet, but the lower backfat thickness was observed at day 22 of lactation in sows fed high-fiber diet. Serena (2005) performed an extensive characterization of sugar beet pulp, potato pulp, pea hull, seed residue, brewers spent grain and pectin residue by-products. Sugar beet pulp and potato pulp were characterized as high in soluble dietary fiber; pectin residue and pea hull were medium in soluble dietary fiber; brewers spent grain and seed residue were high in insoluble dietary fiber. These differences are expected to affect digestibility in the gastrointestinal tract. By-products characterized with a high concentration of soluble dietary fiber may delay gastric emptying because of high water-binding capacity and viscosity, whereas by-products characterized with a high concentration of insoluble dietary fiber are expected to increase fecal excretion because of relatively decreased microbial degradation in the large intestine (Serena et al. 2008). Hong et al. (2001) reported that pigs fed basal and yucca extract120 diets tended to increase feed intake compared with growing-finishing pigs fed a yucca extract60 diet. Yan et al. (2011) also reported that Taraxacum officinale extract powder (1 g/kg) improved feed intake in finishing pigs compared with that of a control group during 0 to 5 and 0 to 10 weeks. A review by Meunier-Salaün et al. (2001) showed that the low feed consumption rate of diets containing high levels of sugar beet pulp might be due to reduced feeding © 2014 Japanese Society of Animal Science
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motivation level, increased mastication time, or lower palatability due to physical and/or metabolic processes during sugar beet pulp digestion. However, Guillemet et al. (2006) reported that during the entire lactation period, the feed intake was 2.3% greater in high-fiber treated sows (6.33 kg/day) than that in control group sows (6.19 kg/day), which represented 140 g more food per day, but this was not different. PeetSchwering et al. (2003) showed that voluntary intake of a sugar beet pulp diet is significantly lower than that of the other five high fiber diets (2.3 kg/day vs. 7.1 kg/ day). In our study, no differences were found on sow feed intake among dietary treatments. On the other hand, Brouns et al. (1997), Braud et al. (1998) and Ramonet et al. (2000) reported that feed consumption rates of sows fed a control diet are higher than those of sows fed a diet containing a high percentage of sugar beet pulp. The reasons may be a higher water-holding capacity and delayed gastric emptying for diets with sugar beet pulp (Guerin et al. 2001). Sugar beet pulp gives a higher degree of satiety in the gastrointestinal tract than that of other fibrous ingredients (Vestergaard 1997), so voluntary feed intake is reduced. It appeared that there was a saturation point for the fecal material at around 70–73% moisture, and that loose stools were observed above this percentage. Percentage moisture could possibly be used as an index for diarrhea severity (Etheridge et al. 1984). Lewis et al. (1995) reported that fecal water content decreased with increasing grain and decreasing forage in the diet because grain is lower in fiber content. Fiber digestibility is low and fiber binds water. As a result, the more fiber consumed, the more fiber excreted in the feces, which increases both fecal mass and fecal moisture content, both of which increase fecal water excretion. This was consistent with our results that both 10% and 20% beet pulp supplementation increased fecal moisture content. In addition, Klopfenstein (1990) demonstrated that beet fiber particle size and surface area had no effect on fecal weight or waterholding capacity at the 5, 7.5 or 10% level of supplementation. This may be the reason why there was no significant difference between 10% and 20% beet pulp diet on fecal moisture content. Cortisol produced during stress suppresses the immune response (Coe 1997) and higher levels of cortisol in the bloodstream have negative effects, such as lowered immunity (Suzanne & Gregory 2004). Norepinephrine and epinephrine are catecholamines secreted by the adrenals that trigger the ‘fight or flight’ response, providing an energy and strength boost by way of the central nervous system for 2–15 min (Cacioppo 2000). We rely on these hormones to overcome and persevere. Epinephrine provides energy for intense workouts and, in the form of norepinephrine, for the mental demands of problem solving. © 2014 Japanese Society of Animal Science
The imbalance in blood sugar and insulin levels causes the adrenal glands to increase their production of cortisol, which act as an anti-stress hormone. Longterm increased cortisol levels signal the pituitary gland to increase levels of adrenocorticotropic hormone, which signals the adrenal glands to produce more cortisol. Increased epinephrine results in increased adrenocorticotropic hormone and increased cortisol, leading to insulin resistance. Dietary (high fiber with 25% beet pulp and control diet) and developmental environments (indoor or outdoor) do not influence plasma cortisol concentrations in gilts (McGlone & Fullwood 2001). These results indicated that pregnant gilts in any of the four treatments of the experiment mentioned above were not under any more or less stress to the point that their physiology changed. In our study, cortisol and norepinephrine concentration was decreased, which can be interpreted as indicating that beet pulp had beneficial effects on reducing stress in lactation sows. As there are not enough reports about beet pulp reducing stress in sows, and the mechanism is still unclear, more research is required to processed. However, sow performance response to dietary fiber is inconsistent, depending on fiber sources, type and duration of sows receiving a fibrous diet (Johnson et al. 2003; Reese et al. 2008). For example, feeding a fibrous diet of soybean hulls results in fewer pigs born (Holt et al. 2006), whereas sows receiving a diet with ground wheat straw produces more and heavier pigs (Everts 1991; Veum et al. 2009). One of the reasons why there is no difference in performance index might be the diets were formulated to be isonitrogenous and isoenergetic in this study.
Conclusion In conclusion, 10% and 20% beet pulp supplementation did not have a positive effect on growth performance in lactating sows and piglets. However, it can relieve stress during the lactation period and increase fecal moisture content which is good for sow feces excretion.
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digestibility, nitrogen retention, and fiber digestibility of diets fed to gestating sows. Journal of Animal Science 86, 2568–2575. Rijnen MMJA, Verstegen MWA, Heetkamp MJW, Haaksma J, Schrama JW. 2001. Effects of dietary fermentable carbohydrates on energy metabolism in group-housed sows. Journal of Animal Science 79, 148–154. SAS. 2001. SAS User’s Guide. SAS Institute, Inc., Cary, NC. Serena A. 2005. Physiological properties of dietary carbohydrates for sows. PhD thesis. Department of Basic Animal and Veterinary Sciences, Royal Veterinary and Agricultural University. Serena A, Jørgensen H, Bach Knudsen KE. 2008. Digestion of carbohydrates and utilization of energy in sows fed diets with contrasting levels and physicochemical properties of dietary fiber. Journal of Animal Science 86, 2208– 2216. Suzanne CS, Gregory EM. 2004. Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychological Bulletin 130, 601–630. Togrul H, Arslan N. 2003. Production of carboxymethyl cellulose from sugar beet pulp cellulose and rheological behaviour of carboxymethyl cellulose. Carbohydrate Polymers 54, 73–82. Trumbo P, Schlicker S, Yates AA, Poos M. 2002. Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty
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acids, cholesterol, protein, and amino acids. Journal of the American Dietetic Association 102, 1621–1630. Vestergaard EM. 1997. The effect of dietary fiber on welfare and productivity of sows. PhD thesis. The Royal Veterinary and Agricultural University. Veum TL, Crenshaw JD, Cromwell GL, Easter RA, Ewan RC, Nelssen JL, et al., the North Central Region-42 Committee on Swine Nutrition. 2009. The addition of ground wheat straw as a fiber source in the gestation diet of sows and the effect on sow and litter performance for three successive parities. Journal of Animal Science 87, 1003–1012. Warren LK. 2007. Horse feeding myths and misconceptions. PhD thesis. Alberta Agriculture, Food and Rural Development. Webel DM, Finck BN, Baker DH, Johnson RW. 1997. Time course of increased plasma cytokines, cortisol, and urea nitrogen in pigs following intraperitoneal injection of lipopolysaccharide. Journal of Animal Science 75, 1514– 1520. Yan L, Meng QW, Kim IH. 2011. The effects of dietary Houttuynia cordata and Taraxacum officinale extract powder on growth performance, nutrient digestibility, blood characteristics and meat quality in finishing pigs. Livestock Science 141, 188–193.
Animal Science Journal (2015) 86, 610–616
Animal Science Journal (2015) 86, 610–616
doi: 10.1111/asj.12334
ORIGINAL ARTICLE Effects of beet pulp supplementation on growth performance, fecal moisture, serum hormones and litter performance in lactating sows Pinyao ZHAO,1 Zhengfan ZHANG2 and In Ho KIM1 1
Department of Animal Resource and Science, Dankook University, Cheonan, Choongnam, South Korea and College of Life Science and Technology, Southwest University for Nationalities, Chengdu, China
2
ABSTRACT This study was conducted to evaluate effects of beet pulp supplementation on growth performance, fecal moisture, serum hormones and litter performance in lactating sows. Ninety primiparous sows (Landrace × Yorkshire) were randomly allotted to one of three dietary treatments in a 21-day trial starting 3 days before parturition. The three dietary treatments were supplemented with 0, 10 and 20% beet pulp, respectively. Backfat loss and fecal moisture content were increased (P < 0.05), where cortisol and norepinephrine levels were decreased (P < 0.05) in sows fed beet pulp supplementation diets compared with control diet, but there was no difference between 10% and 20% beet pulp supplementation treatments. No effect was observed on bodyweight, average daily intake, weaning to estrus interval, epinephrine level in sows and litter weight, litter size, survivability in piglets among dietary treatments. Taken together, beet pulp supplementation has no significant effect of growth performance of lactating sows and piglets with decreased cortisol and norepinephrine levels in lactating sows, but it can increase fecal moisture content which is beneficial for sow feces excretion.
Key words: beet pulp, fecal moisture, growth performance, lactating sow, serum hormones.
INTRODUCTION Dietary fiber is the indigestible portion of plant foods comprised of soluble and insoluble fiber (Menezes et al. 2004). Soluble fiber is readily fermented in the colon into gases and physiologically active by-products, whereas insoluble fiber is metabolically inert, absorbing water as it moves through the digestive system and easing defecation (Trumbo et al. 2002). Dietary fiber acts by changing the nature of the gastrointestinal tract contents and by changing how other nutrients and chemicals are absorbed (Eastwood & Kritchevsky 2005). Higher fiber diets are commonly fed to gestating sows to improve sow behavior (Matte et al. 1994; Ramonet et al. 1999; Guillemet et al. 2006). Feeding a high-fiber diet during gestation increases voluntary feed intake during lactation (Dourmad et al. 1996; Farmer et al. 1996; Quesnel et al. 2009) and improves sow litter performance (Matte et al. 1994; Ramonet et al. 1999; Danielsen & Vestergaard 2001). Sugar beet pulp is a by-product from sugar beet processing, which is used as fodder for horses and other livestock (Togrul & Arslan 2003; MirzaeiAghsaghali et al. 2011). Despite being a by-product of © 2014 Japanese Society of Animal Science
sugar beet processing, sugar beet pulp is high in energy and fiber (Warren 2007). Sugar beet pulp has great estimated net energy value (13.4 kJ/g) for sows because the non-starch polysaccharides in sugar beet pulp are utilized in the large intestine for energy by sows as efficiently as the energy from digested starch (Rijnen et al. 2001). Most studies reporting the effects of dietary fiber on physical activity have used sugar beet pulp as the fiber source (Brouns et al. 1994; Braud et al. 1998; Ramonet et al. 2000). As we know, it is a big challenge for sows during lactation and they will cope with severe stress. The concentration of cortisol, epinephrine and norepinephrine in serum is a criterion that reflects stress intensity (Webel et al. 1997). However, not enough studies have been conducted to evaluate the use of beet pulp in lactating sows. Additionally, we wondered if beet pulp could reduce stress
Correspondence: In Ho Kim, Department of Animal Resource and Science, Dankook University, Cheonan, Choongnam 330-714, South Korea. (Email: inhokim@ dankook.ac.kr) Received 19 May 2014; accepted for publication 7 August 2014.
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during lactation or improve sow and piglet growth performances. The objective of this study was to evaluate effects of beet pulp supplementation on growth performance, fecal moisture, serum hormones and litter performance in lactating sows.
MATERIALS AND METHODS The experimental protocol used in this study was approved by the Animal Care and Use Committee of Dankook University, which is comparable to those laid down by the Canadian Council on Animal Care.
Experimental design, animals and housing A total of 90 primiparous sows (Landrace × Yorkshire) were used in this experiment. On day 110 of gestation, sows were weighed and moved into the farrowing facility, randomly allotted to one of three dietary treatments, and fed 2.5 kg/ day feed to allow for adjustment to the lactation diets before parturition. Experimental treatments contained three levels of beet pulp: (i) CON, basal diet; (ii) BP1, contain 10% beet pulp; and (iii) BP2, contain 20% beet pulp. The different ingredients in three dietary treatments were adjusted in an attempt to provide isonitrogenous and isoenergetic rations. Dietary nutrients were formulated to meet or exceed the NRC (1998) recommendations (Table 1). The chemical composition of sugar beet pulp is presented in Table 2. Sows were housed in farrowing crates (2.1 m × 0.6 m) which contained an area (2.1 m × 0.6 m) for newborn piglets on each side, and the temperature in the farrowing house was maintained at a minimum of 20°C. Heat lamps were provided for piglets. Piglets were treated according to routine management practices that included teeth clipping, tail docking, ear notching and subcutaneous iron dextran injections (1 mL per pig) within 24 h of birth. After farrowing, daily feed allowance increased gradually and sows had ad libitum access to feed by day 6. Sows were provided with free access to drinking water throughout the experimental period. The piglets received no creep feed.
Sampling and measurements Three experimental diets were analyzed for crude protein (method 990.03), crude fiber (method 962.09), crude ash (method 942.05), acid detergent fiber (method 973.18), calcium and phosphorus (method 985.01) as described by AOAC (2007), and neutral detergent fiber (Holst 1973). The ammonia acid profile of diets was analyzed using a Sykam Amino Acid Analyzer (Sykam-S7130; Tokyo, Japan) and high-performance liquid chromatography (HPLC) after acid hydrolysis for 24 h in 6N HCl. Methionine was analyzed as Met sulfone after cold performic acid oxidation overnight before hydrolysis and tryptophan was determined after NaOH hydrolysis for 22 h at 110°C. Individual sow was weighed and scanned for backfat thickness within a few hours after day of farrowing and on day 21 of lactation to determine weight and backfat loss. The backfat thickness of the sows (6 cm off the midline at the 10th rib) was measured using a real-time ultrasound instrument (Piglot 105; SFK Technology, Herlev, Denmark). During the experimental period, numbers of piglets alive and death per litter were recorded to calculate survival ratio. Individual pig weight was recorded at birth and weaning Animal Science Journal (2015) 86, 610–616
Table 1
Composition of experimental diets (as-fed basis)
Item
CON
BP1
BP2
Ingredient, % Corn 51.28 44.96 35.22 Soybean meal (47% crude protein) 24.47 21.60 21.00 Beet pulp – 10.00 20.00 Wheat bran 4.03 3.73 3.73 Rapeseed meal 2.50 2.50 3.00 Rice bran 5.00 4.58 4.48 Tallow 6.00 6.00 6.00 Molasses 3.50 3.50 3.50 Dicalcium phosphate 1.64 1.58 1.54 Limestone 0.76 0.73 0.71 Salt 0.50 0.50 0.50 Lysine (98%) 0.12 0.12 0.12 Vitamin premix† 0.10 0.10 0.10 Mineral premix‡ 0.10 0.10 0.10 Calculated compositions, % Metabolic energy, MJ/kg 3.41 3.43 3.43 Crude protein 17.10 17.11 17.13 Crude fat 9.10 9.16 9.13 Lysine 1.00 0.99 0.97 Calcium 0.78 0.83 0.85 Phosphorus 0.69 0.70 0.73 Analyzed compositions, % Crude protein 17.12 17.10 17.05 Crude fat 9.13 9.15 9.12 Lysine 1.00 0.99 0.98 Threonine 0.68 0.66 0.65 Isoleucine 0.67 0.66 0.65 Methionine 0.25 0.24 0.24 Calcium 0.81 0.84 0.86 Phosphorus 0.71 0.71 0.72 Neutral detergent fiber 9.75 12.54 14.87 Acid detergent fiber 5.07 9.46 13.82 †Provided per kilogram of complete diet: vitamin A, 10 000 IU; vitamin D3, 2000 IU; vitamin E, 48 IU; vitamin K3, 1.5 mg; riboflavin, 6 mg; niacin, 40 mg; d-pantothenic, 17 mg; biotin, 0.2 mg; folic acid, 2 mg; choline, 166 mg; vitamin B6, 2 mg; and vitamin B12, 28 μg. ‡Provided per kilogram of complete diet: Fe (as FeSO4·7H2O), 90 mg; Cu (as CuSO4·5H2O), 15 mg; Zn (as ZnSO4), 50 mg; Mn (as MnO2), 54 mg; I (as KI), 0.99 mg; and Se (as Na2SeO3·5H2O), 0.25 mg.
Table 2 Chemical composition (% dry matter (DM)) of sugar beet pulp
Item
Unit
Value
DM Crude protein Crude fiber Acid detergent fiber Neutral detergent fiber Lignin Ether extract Ash Starch Total sugars Gross energy
% as fed % DM % DM % DM % DM % DM % DM % DM % DM % DM MJ/kg DM
88.5 9.1 18.7 23.5 47.6 2.2 0.8 7.6 0.9 7.4 17.1
(day 21 of lactation) to determine weight gain. After farrowing, daily feed allowance increased 1 kg/day until day 6 postpartum, and then sows were given ad libitum access to feed and water. During lactation, feed consumption was © 2014 Japanese Society of Animal Science
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recorded for each sow to calculate average daily feed intake. After weaning, weaning to estrus interval was recorded for each sow. Samples of feces were collected (one collection per sow) for the determination of moisture content. Total moisture was determined by air-drying the collection at 60°C, followed by an equilibration and moisture determination at 105°C (Harris 1970). At day 21 of lactation, blood samples were collected from the cervical vein into non-heparinized vacuum tubes (Becton Dickinson Vacutainer Systems, Franklin Lakes, NJ, USA) of each sow at the same time of the day. Blood samples were collected before meals and after removal of piglets. After collection, the serum samples were centrifuged (3000 × g) for 30 min at 4°C and stored at −20°C until being used in cortisol, norepinephrine and epinephrine analysis. Serum concentrations of cortisol were determined with a standardized solid phase radioimmunoassay kit (Diagnostic Products Corporation, Los Angeles, CA, USA). The norepinephrine and epinephrine were assayed using an ionexchange purification procedure followed by liquid chromatography with electrochemical detection, as described previously by Hay and Mormède (1997). In brief, the samples were loaded onto cationic columns and the catecholamines were eluted with boric acid. The eluates were assayed via HPLC with electrochemical detection with an oxidizing potential of +0.65V. The intra- and inter-assay coefficients of variation (CV) were 7.0% and 7.1% for norepinephrine and 6.5% and 11.6% for epinephrine, respectively.
Statistical analyses All experimental data were analyzed using the GLM procedure of SAS (2001) as a randomized complete block design (SAS Inst. Inc., Cary, NC, USA) according to their body weight (BW). The sow or litter of piglets was used as the experimental unit. The analysis of sow backfat thickness and change during lactation used fat depth at farrowing as covariates. Piglet birth weight was used as covariates for weaning weights during lactation. Lactation length was used as a covariate for piglet survivability, sow and piglet weaning weight, sow feed intake, and weaning to estrus interval and backfat thickness depth change. The initial values were used as a covariate for blood profiles. Orthogonal contrasts were used to the effect of treatments: CON versus BP1 + BP2 and
BP1 versus BP2 treatments. Variability in the data was expressed as the pooled standard error (SE) and a P < 0.05 was considered as significant.
RESULTS Growth performance of sows and piglets During lactation, backfat loss was increased (P < 0.05) in sows fed beet pulp supplementation diets compared with sows fed CON diet (Table 3). Sow bodyweight loss, feed intake, and weaning to estrus interval were not affected (P > 0.05) by beet pulp supplementation. In addition, litter weaning weight and the number of pig survivals were not different (P > 0.05) among dietary treatments (Table 4). No difference (P > 0.05) was observed in backfat loss, BW loss, feed intake, weaning to estrus interval of sows, litter weight and survivability of piglets between BP1 and BP2 treatments.
Fecal moisture content and serum hormones of sows Sows fed diets containing beet pulp had higher (P < 0.05) fecal moisture content than those fed CON diet, but there was no difference (P > 0.05) between BP1 and BP2 treatments (Table 3). Sows fed diets containing beet pulp had lower (P < 0.05) cortisol and norepinephrine levels than those fed CON diets (Table 5). However, no effect (P > 0.05) was observed in cortisol and norepinephrine levels between BP1 and BP2 treatments. In addition, there was no differences (P > 0.05) in epinephrine levels among dietary treatments.
DISCUSSION Sow BW losses during lactation were greater in sows fed a high-fiber diet compared with those fed a CON diet (Guillemet et al. 2006). Baudon and Hancock (2003) reported that a better energy balance might be
Table 3 Effect of beet pulp supplementation on performance and fecal moisture content in lactating sows†
Item
Sow bodyweight, kg At parturition At day 21 of lactating Bodyweight loss Backfat thickness, mm At parturition At day 21 of lactating Backfat loss Average daily feed intake, kg Weaning to estrus interval, days Fecal moisture content, %
CON
223.3 213.5 9.8 17.5 15.8 1.7 6.18 6.0 69.44
BP1
221.8 211.7 10.1 20.1 17.7 2.4 5.80 4.0 73.48
BP2
218.5 204.2 14.3 21.5 18.9 2.6 6.09 5.6 74.48
SE‡
P-value CON vs. BP1 + BP2
BP1 vs. BP2
7.45 11.39 2.62
0.21 0.34 0.17
0.28 0.44 0.21
1.19 1.32 0.19 0.31 0.77 0.81
0.09 0.08 0.02 0.12 0.08 0.04
0.41 0.26 0.07 0.14 0.07 0.15
†CON, basal diet; BP1, CON + 10% beet pulp; BP2, CON + 20% beet pulp. ‡Standard error.
© 2014 Japanese Society of Animal Science
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Table 4
Effect of beet pulp supplementation on performance in piglets†
Item
CON
Litter weight, kg Initial Final Weight gain Litter size Initial Final Survivability, %
BP1
BP2
SE‡
P-value CON vs. BP1 + BP2
BP1 vs. BP2
14.42 66.38 51.96
17.05 71.00 53.95
15.66 70.90 55.24
2.08 4.94 2.53
0.13 0.31 0.26
0.21 0.38 0.14
10.42 10.42 100.00
10.95 10.25 93.61
11.24 10.00 89.00
0.69 0.82 5.08
0.14 0.19 0.34
0.18 0.09 0.29
†CON, basal diet; BP1, CON + 10% beet pulp; BP2, CON + 20% beet pulp. ‡Standard error.
Table 5
Effect of beet pulp supplementation on serum hormones in lactating sows†
Item
Cortisol, μg/dL Epinephrine, pg/mL Norepinephrine, pg/mL
CON
3.70 40.64 186.5
BP1
2.78 36.28 171.8
BP2
SE‡
2.92 37.50 173.1
0.24 1.25 6.47
P-value CON vs. BP1 + BP2
BP1 vs. BP2
0.03 0.24 0.02
0.13 0.22 0.42
†CON, basal diet; BP1, CON + 10% beet pulp; BP2, CON + 20% beet pulp. ‡Standard error.
expected to decrease bodyweight loss by sows during the lactation period. However, Hill et al. (2008) reported that sows fed a basal diet with 5% beet pulp or a basal diet with 15% distillers dried grains with solubles had similar bodyweight loss during the lactation period. In our study, no differences were found in BW loss during the lactation period. Che et al. (2011) showed that sows fed a low-fiber diet during parity 1 gained more backfat during gestation but lost more during lactation than sows fed a high-fiber diet. This was different from our results about backfat loss. In our research, sows fed beet pulp diets which were high in fiber lost more backfat than sows fed the basal diet. Similar results as ours were reported by Peet-Schwering et al. (2003), that sows fed a high level of dietary fermentable non-starch polysaccharides during lactation lost more backfat during lactation than sows fed a starch diet. As reported by Maes et al. (2004), sow backfat could reflect nutrient retention and potential reproductive efficiency. The higher inclusion of fiber decreased the digestibility of dry matter, energy and nitrogen (Ramonet et al. 1999; Holt et al. 2006; Renteria-Flores et al. 2008), and feed intake (Brouns et al. 1997; Braud et al. 1998; Ramonet et al. 2000) of a gestating diet. These factors rmean that sows needed to increase metabolic rate of body reserves to maintain health and survival, which led to an increased backfat loss. In addition, it was likely that parity also had effect on backfat loss during the gestation period. Che et al. (2011) reported that sows in parity 1 fed a low-fiber diet lost more backfat during lactation than sows fed a high-fiber diet, while in Animal Science Journal (2015) 86, 610–616
parity 2, sows receiving high-fiber diet did not lose backfat during lactation compared with sows receiving low-fiber diet, but the lower backfat thickness was observed at day 22 of lactation in sows fed high-fiber diet. Serena (2005) performed an extensive characterization of sugar beet pulp, potato pulp, pea hull, seed residue, brewers spent grain and pectin residue by-products. Sugar beet pulp and potato pulp were characterized as high in soluble dietary fiber; pectin residue and pea hull were medium in soluble dietary fiber; brewers spent grain and seed residue were high in insoluble dietary fiber. These differences are expected to affect digestibility in the gastrointestinal tract. By-products characterized with a high concentration of soluble dietary fiber may delay gastric emptying because of high water-binding capacity and viscosity, whereas by-products characterized with a high concentration of insoluble dietary fiber are expected to increase fecal excretion because of relatively decreased microbial degradation in the large intestine (Serena et al. 2008). Hong et al. (2001) reported that pigs fed basal and yucca extract120 diets tended to increase feed intake compared with growing-finishing pigs fed a yucca extract60 diet. Yan et al. (2011) also reported that Taraxacum officinale extract powder (1 g/kg) improved feed intake in finishing pigs compared with that of a control group during 0 to 5 and 0 to 10 weeks. A review by Meunier-Salaün et al. (2001) showed that the low feed consumption rate of diets containing high levels of sugar beet pulp might be due to reduced feeding © 2014 Japanese Society of Animal Science
614 P. ZHAO et al.
motivation level, increased mastication time, or lower palatability due to physical and/or metabolic processes during sugar beet pulp digestion. However, Guillemet et al. (2006) reported that during the entire lactation period, the feed intake was 2.3% greater in high-fiber treated sows (6.33 kg/day) than that in control group sows (6.19 kg/day), which represented 140 g more food per day, but this was not different. PeetSchwering et al. (2003) showed that voluntary intake of a sugar beet pulp diet is significantly lower than that of the other five high fiber diets (2.3 kg/day vs. 7.1 kg/ day). In our study, no differences were found on sow feed intake among dietary treatments. On the other hand, Brouns et al. (1997), Braud et al. (1998) and Ramonet et al. (2000) reported that feed consumption rates of sows fed a control diet are higher than those of sows fed a diet containing a high percentage of sugar beet pulp. The reasons may be a higher water-holding capacity and delayed gastric emptying for diets with sugar beet pulp (Guerin et al. 2001). Sugar beet pulp gives a higher degree of satiety in the gastrointestinal tract than that of other fibrous ingredients (Vestergaard 1997), so voluntary feed intake is reduced. It appeared that there was a saturation point for the fecal material at around 70–73% moisture, and that loose stools were observed above this percentage. Percentage moisture could possibly be used as an index for diarrhea severity (Etheridge et al. 1984). Lewis et al. (1995) reported that fecal water content decreased with increasing grain and decreasing forage in the diet because grain is lower in fiber content. Fiber digestibility is low and fiber binds water. As a result, the more fiber consumed, the more fiber excreted in the feces, which increases both fecal mass and fecal moisture content, both of which increase fecal water excretion. This was consistent with our results that both 10% and 20% beet pulp supplementation increased fecal moisture content. In addition, Klopfenstein (1990) demonstrated that beet fiber particle size and surface area had no effect on fecal weight or waterholding capacity at the 5, 7.5 or 10% level of supplementation. This may be the reason why there was no significant difference between 10% and 20% beet pulp diet on fecal moisture content. Cortisol produced during stress suppresses the immune response (Coe 1997) and higher levels of cortisol in the bloodstream have negative effects, such as lowered immunity (Suzanne & Gregory 2004). Norepinephrine and epinephrine are catecholamines secreted by the adrenals that trigger the ‘fight or flight’ response, providing an energy and strength boost by way of the central nervous system for 2–15 min (Cacioppo 2000). We rely on these hormones to overcome and persevere. Epinephrine provides energy for intense workouts and, in the form of norepinephrine, for the mental demands of problem solving. © 2014 Japanese Society of Animal Science
The imbalance in blood sugar and insulin levels causes the adrenal glands to increase their production of cortisol, which act as an anti-stress hormone. Longterm increased cortisol levels signal the pituitary gland to increase levels of adrenocorticotropic hormone, which signals the adrenal glands to produce more cortisol. Increased epinephrine results in increased adrenocorticotropic hormone and increased cortisol, leading to insulin resistance. Dietary (high fiber with 25% beet pulp and control diet) and developmental environments (indoor or outdoor) do not influence plasma cortisol concentrations in gilts (McGlone & Fullwood 2001). These results indicated that pregnant gilts in any of the four treatments of the experiment mentioned above were not under any more or less stress to the point that their physiology changed. In our study, cortisol and norepinephrine concentration was decreased, which can be interpreted as indicating that beet pulp had beneficial effects on reducing stress in lactation sows. As there are not enough reports about beet pulp reducing stress in sows, and the mechanism is still unclear, more research is required to processed. However, sow performance response to dietary fiber is inconsistent, depending on fiber sources, type and duration of sows receiving a fibrous diet (Johnson et al. 2003; Reese et al. 2008). For example, feeding a fibrous diet of soybean hulls results in fewer pigs born (Holt et al. 2006), whereas sows receiving a diet with ground wheat straw produces more and heavier pigs (Everts 1991; Veum et al. 2009). One of the reasons why there is no difference in performance index might be the diets were formulated to be isonitrogenous and isoenergetic in this study.
Conclusion In conclusion, 10% and 20% beet pulp supplementation did not have a positive effect on growth performance in lactating sows and piglets. However, it can relieve stress during the lactation period and increase fecal moisture content which is good for sow feces excretion.
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