Abstract
The effects of formulating broiler diets that contain sources of either rapidly or slowly digestible protein and 2 different dietary fiber sources on growth performance were studied in broilers chickens from 0 to 36 d of age. A total of 1,920 one-day-old, male Ross 708 broiler chickens were randomly allocated and housed in 48 floor pens (40 birds/pen) to one of 4 dietary treatments. Birds were allotted according to a completely randomized block design using a factorial arrangement of treatments with 2 protein digestion rates (rapidly or slowly) and 2 dietary fiber sources [3% oat hulls (OH) or 3% sugar beet pulp (SBP)] from 0 to 36 d of age. All diets were formulated to be isocaloric and isonitrogenous. The pen was the experimental unit for all variables studied (12 replicates/treatment). Data were analyzed using the MIXED procedure of SAS, and the model included the main effects of the protein digestion rate, dietary fiber source, and their interaction. There were 3 experimental feeding phases; starter (from day 0–14), grower (from day 14–28), and finisher (from day 28–36). Results indicated that broilers fed diets containing sources that supplied more rapidly digestible protein had 4% greater (P < 0.01) ADG and improved (P < 0.01) the feed conversion ratio (FCR) by 5% throughout the experiment, most notably after the starter phase. Diets containing 3% OH increased (P < 0.05) the ADFI and ADG (P < 0.05) in the starter phase compared with broilers fed diets containing 3% SBP, without affecting the FCR. The ADG and FCR of broilers fed diets containing sources of slowly digestible protein were improved (P < 0.05) to the level of broilers fed rapidly digestible protein containing diets with the addition of 3% OH. It is concluded that broiler diets should be formulated to contain a high concentration of ingredients that supply rapidly digestible protein, but if this is cost-prohibitive, then 3% OH could be used to increase the ADFI and ADG and potentially protein digestion rates to reduce the FCR.
Key words: dietary fiber, growth performance, oat hull, protein digestion kinetics, sugar beet pulp
Introduction
Broiler diets are normally formulated using apparent, standardized or true digestibility coefficients of amino acids (AA), and these coefficients are typically measured at the terminal ileum. However, this approach ignores the fact that AA and protein may have different rates and sites of digestion and absorption. The rate and site of protein digestion along the digestive tract have been investigated in different species including ruminant and humans (Ørskov and McDonald, 1979; Boirie et al., 1997). In broilers, there is growing evidence indicating that the site and rate of digestion of protein and absorption of AA influence broiler performance (Liu et al., 2017; Truong et al., 2017; Moss et al., 2018). In this respect, Liu et al. (2013) showed that 70% of the methionine present in sorghum-soybean meal-canola meal-based diets was digested in the proximal jejunum in broilers. In addition, Liu et al. (2015) determined apparent digestibility coefficients of protein at 4 sites of the small intestine and reported that 79% of protein was digested in the jejunum. The variation in digestion pattern across different sections of the small intestine was also reported for crude protein digestion in broilers by Gutiérrez del Álamo et al. (2009). Therefore, AA are digested to varying degrees across each section of the small intestine, although almost all investigations focus on ileal digestibility, and no attention is paid to jejunal digestibility coefficients. These data indicate that the kinetics of protein digestion may also need to be considered along with the static ileal digestibility coefficients, and that protein digestion rates may be used to further enhance broiler performance. It must be considered, however, that AA composition in portal circulation is a result of first-pass postabsorptive metabolism, while further metabolism and regulation alters the composition of AA in the liver and muscles.
In contrast, degradation characteristics of raw materials used in poultry diets are scarce, although this type of research is often studied in human nutrition (Dangin et al., 2001; Koopman et al., 2009). To characterize protein sources according to digestion kinetics, in vitro and in vivo protein digestibility assays have been developed to predict different ingredient protein fractions, as well as their rate and extent of digestion (Bryan et al., 2018, 2019a,b).
The type of dietary fiber in the diet affects the gastrointestinal tract (GIT) development and growth performance of broilers (Jiménez-Moreno et al., 2009). This is due to a number of physicochemical properties of fibrous ingredients including solubility, water-holding capacity (WHC), viscosity, bulk, fermentability, and ability to bind bile acids (Jiménez-Moreno et al., 2013a). In this respect, soluble dietary fiber (SDF) sources can increase viscosity and bulk of the digesta, which results in delayed gizzard emptying. Sugar beet pulp (SBP) is a source of the SDF high in pectin, a nonstarch polysaccharide with the ability to increase the viscosity of digesta within the GIT, reducing the rate of diffusion of digestive enzymes into the digesta, and consequently, reducing nutrient absorption (Jiménez-Moreno et al., 2009). On the other hand, insoluble dietary fiber (IDF) sources, such as oat hulls (OH), are known for their positive effects on the gizzard function and mucosal structure of the small intestine (González-Alvarado et al., 2008; Sacranie et al., 2012), which might improve nutrient digestibility (Hetland et al., 2004). Studies have shown that a well-developed gizzard is linked to strong muscular contractions that allow thorough grinding of the feed, helping to control the flow of the digesta from the gizzard to the small intestine, facilitating the mixing of chyme and gastric juices (Jiménez-Moreno et al., 2019). Therefore, the objective of this trial was to test the hypothesis that broilers fed diets formulated to contain ingredients which supply rapidly digestible protein (which are quickly digested and absorbed in the digestive tract) would have greater performance than those fed a diet containing sources that supply slowly digestible protein. Furthermore, the addition of OH was hypothesized to ameliorate the reduced performance of broilers fed diets containing slowly digestible protein sources.
Materials and methods
The present study was approved by the Trouw Nutrition animal care committee and followed recommendations of the Canadian Council of Animal Care guidelines on the care and use of farm animals in research, teaching, and testing (CCAC, 2009).
Bird Husbandry and Fiber Sources
In total, 1,920 one-day-old, male Ross 708 broiler chickens were obtained from a local hatchery and housed in the experimental facilities of Trouw Nutrition Agresearch (Burford, Ontario, Canada). After arrival, birds were weighed and randomly allocated to one of 48 floor pens (49 sq. ft./pen) with an individual feeder and nipple drinker line (4 nipples/pen). All pens had a similar average BW (39.34 ± 1.15 g) at placement. The birds were kept on a 24 h/d light program the first 3 d and 18 h/d light program from 3 to 36 d of age. The birds had ad libitum access to feed and water throughout the experiment. The environmental conditions of the barn were controlled automatically according to the age of the birds. The room temperature was maintained at 33°C ± 1.5°C for the first week of the experiment and then it was reduced 2°C per week until reaching 23°C. The SBP was received as 10-mm pellets, and OH were received as mash. The dietary fiber sources were ground with a hammer mill and sieved with a 2.5-mm screen before being included in their respective experimental diets. The calculated and analyzed composition and the physicochemical properties of the dietary fiber sources are shown in Table 1.
Table 1.
Calculated and analyzed chemical composition (%, as-fed basis, unless otherwise indicated) and the physicochemical properties of the dietary fiber sources.
| Item (%, as fed basis, unless otherwise indicated) | Oats hulls | Sugar beet pulp |
|---|---|---|
| Calculated composition | ||
| Dry matter | 90.7 | 93.4 |
| Total ash | 4.3 | 4.8 |
| Crude protein | 5.1 | 9.2 |
| Starch | 18.1 | - |
| Ether extract | 1.4 | 0.8 |
| Crude fiber | 25.9 | 19.9 |
| Neutral detergent fiber | 57.9 | 46.8 |
| Acid detergent fiber | 29.3 | 24.0 |
| Analyzed composition1 | ||
| Dry matter | 92.6 | 91.1 |
| Gross energy (Kcal/kg) | 979.2 | 926.7 |
| Total ash | 4.0 | 5.8 |
| Crude protein | 3.9 | 9.6 |
| Starch | 9.2 | 1.0 |
| Crude fiber | 23.2 | 17.5 |
| Neutral detergent fiber | 61.9 | 48.5 |
| Acid detergent fiber | 32.4 | 21.3 |
| Acid detergent lignin | 5.4 | 3.0 |
| Total dietary fiber | 71.3 | 59.0 |
| Insoluble dietary fiber | 70.6 | 47.4 |
| Soluble dietary fiber | 0.7 | 11.6 |
| Physicochemical properties | ||
| GMD2±GSD3 | 760 ± 1.9 | 630 ± 2.1 |
| WHC4±SD | 4.6 ± 0.75 | 9.8 ± 0.21 |
| SWC5±SD | 2.4 ± 0.40 | 5.3 ± 0.78 |
Analyzed in duplicate.
GMD = geometric mean diameter (μm).
GSD = log normal geometric SD.
WHC = water-holding capacity (mL/g DM).
SWC = swelling water capacity (mL/g DM).
Experimental Design, Experimental Diets, and Measurements
Four dietary treatments were arranged in a randomized complete block design using a 2 × 2 factorial arrangement with 2 protein digestion rates (rapidly or slowly) and 2 sources of dietary fiber (3% OH or SBP) from day 0 to 36 of age. There were 12 blocks in the house, and these were distributed throughout the house to ensure equal treatment spacing from the exhaust fans on the southside of the house and the air inlet vent on the north side of the house. Five blocks were closest to the air inlet vent, 3 blocks were in the middle, 3 blocks were closest to the exhaust fans, and 1 block was equally split between the middle and closest to the exhaust fans. The experimental unit was the pen with 40 birds per pen, and each experimental treatment was replicated 12 times. There were 3 experimental feeding phases: starter (from day 0–14), grower (from day 14–28), and finisher (from day 28–36). Starter diets were fed as a crumble, whereas grower and finisher diets were fed as pellets (3 mm). According to the literature (Truong et al., 2017; Bryan et al., 2019a; Jaworski et al., 2019), soybean meal and wheat were considered as rapidly digestible protein sources, whereas soy protein concentrate, rapeseed meal, corn gluten meal, and corn were considered as slowly digestible protein sources. The SDF source was SBP, whereas the IDF source was OH. All diets were formulated to be isocaloric and isonitrogenous and were formulated to meet or exceed requirements for digestible AA and phosphorus, vitamins, and minerals (CVB Feed Table, 2016). Exogenous phytase and xylanase were added to all experimental diets.
Birds were weighed by pen, and feed intake was measured by pen on days 0, 8, 14, 22, 28, and 36 d of the experiment. Mortalities were recorded daily. The ADG, ADFI, and feed conversion ratio (FCR) were calculated from these data by week and cumulatively. Mortality was not included in the calculation of the FCR.
Laboratory Analyses
Representative samples of the dietary fiber sources and experimental diets were ground in a laboratory mill (Retsch model Z-I; Retsch GmbH, Stuttgart, Germany) equipped with a 1-mm screen. Samples were analyzed for moisture by oven-drying (method 930.15), total ash by muffle furnace (method 942.05), and nitrogen by Dumas (method 968.06) using a Leco analyzer (model FP-528; Leco Corp., St. Joseph, MI) as indicated by the AOAC International (2000). Ether extract in raw materials and in experimental diets was determined (method 920.39) according to AOAC International (2005). Acid detergent fiber and neutral detergent fiber were determined using Ankom Technology methods 12 and 13, respectively (Ankom2000 Fiber Analyzer, Ankom Technology, Macedon, NY), and acid detergent lignin was analyzed as the acid detergent fiber residue remaining after a 72-h soak in 72% H2SO4. Insoluble dietary fiber and SDF were analyzed in all samples according to method 991.43 (AOAC International, 2007) using the AnkomTDF Dietary Fiber Analyzer (Ankom Technology). The total dietary fiber (TDF) was determined as the sum of the analyzed IDF and SDF. The geometric mean diameter and geometric SD of the fiber sources were determined in 100-g samples using a shaker (Retsch GmbH) provided with 8 sieves ranging in mesh from 5,000 to 40 μm, as described by the ASAE (1995). The in vitro WHC was measured as indicated by González-Alvarado et al. (2008). Briefly, 2 subsamples (1.0 g DM) of each dietary fiber source were left to soak for 20 h in an excess of distilled water (100 mL). Samples were filtered on a fritted glass crucible (porosity 2). The wet sample was weighed after letting the water drain for 10 min, and the WHC, expressed as milliliters per gram DM, was calculated as the amount of water retained. In addition, the swelling water capacity (SWC) was determined as indicated by Jiménez-Moreno et al. (2009a). Briefly, 2 subsamples (2.0 g of DM) of the dietary fiber source were hydrated in 10 mL of distilled water in a calibrated cylinder (25 mL) at room temperature. Samples were dispersed by gentle stirring for 5 min and left undisturbed at room temperature for 22 to 24 h. After equilibration, the bed volume was recorded and expressed as milliliters per gram DM of the original sample.
Statistical Analyses
Normality of residuals were determined using the UNIVARIATE procedure of SAS (SAS Inst. Inc., Cary, NC). Outliers were determined using the BOXPLOT procedure of SAS (SAS Inst. Inc., Cary, NC) and the influence statement in conjunction with Cook's D. Three outliers were from 1 pen of birds fed the diet containing rapidly digestible protein and OH (ADG day 15 to 22 = 75.5 g/d; FCR day 15 to 22 = 1.163 g/g; FCR day 22 to 28 = 1.702 g/g), 2 outliers were from 1 pen of birds fed the same diet (ADFI day 8 to 15 = 46.0 g/d; FCR day 8 to 15 = 1.320 g/d), 2 outliers were from 1 pen of birds fed the diet containing rapidly digestible protein and SBP (ADFI day 8 to 15 = 42.0 g/d; FCR day 8 to 15 = 1.163 g/g), and 1 outlier was from 1 pen of birds fed the diet containing slowly digestible protein and SBP (FCR day 8 to 15 = 1.501 g/g). Growth performance was analyzed as a 2 × 2 factorial arrangement of treatments, and the model included the main effects of protein digestion rate (rapidly vs. slowly), dietary fiber source (3% OH or SBP), and their interaction using an ANOVA in the MIXED procedure of SAS (SAS Inst. Inc., Cary, NC). The block was considered a random effect. The pen was the experimental unit. For all outcomes, a P-value ≤ 0.05 was used to determine significance among dietary treatments, and a P-value > 0.05, but <0.10, was considered a trend.
Results
The analyzed chemical composition and physical characteristics of the dietary fiber sources are shown in Table 1. Oat hulls contained 71.3, 70.6, and 0.7% TDF, IDF, and SDF, respectively, whereas SBP contained 59.0, 47.4, and 11.6% of TDF, IDF, and SDF, respectively. The geometric mean diameter was greater for OH than for SBP (760 vs. 630 μm, respectively). The WHC and SWC of SBP were twice as high compared with those of OH. The calculated and determined analysis of the experimental diets are shown in Tables 2 and 3. The analyzed CP in the rapidly digestible protein plus OH diet was 25.4%, and this was greater compared with the 21.5% CP that was calculated. We suspect this to be an analytical error because the NIR result was 20.5% CP. Nonetheless, this could have impacted the observed performance results during the starter phase. Overall mortality was low (2.4%) and not affected by treatment (P > 0.05; data not shown).
Table 2.
Experimental diets (%, as-fed basis, unless otherwise indicated) during the 3 feeding phases (day 0–36 of age).
| Starter (Day 0–14 of age) | Grower (Day 14–28 of age) | Finisher (Day 28–36 of age) | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Protein digestion rate |
Rapidly |
Slowly |
Rapidly |
Slowly |
Rapidly |
Slowly |
||||||
| Dietary fiber source | OH1 | SBP2 | OH | SBP | OH | SBP | OH | SBP | OH | SBP | OH | SBP |
| Ingredient, % | ||||||||||||
| Corn | 20.55 | 32.93 | 44.15 | 39.29 | 24.78 | 12.37 | 27.61 | 30.43 | 19.79 | 22.19 | 50.79 | 51.24 |
| Wheat | 31.45 | 20.00 | 10.00 | 16.03 | 31.85 | 45.36 | 30.61 | 27.91 | 40.81 | 38.56 | 10.00 | 10.00 |
| Soybean meal, dehulled 48% CP | 34.09 | 36.49 | 20.74 | 19.12 | 32.65 | 29.68 | 17.46 | 17.61 | 29.21 | 29.26 | 18.41 | 18.00 |
| Rapeseed meal | 2.30 | 7.50 | 7.50 | 7.50 | 7.50 | 7.50 | 7.50 | |||||
| Soy protein concentrate | 5.00 | 5.00 | 5.00 | 5.00 | 4.17 | 4.28 | ||||||
| Corn gluten meal | 0.23 | 2.88 | 3.42 | 1.86 | 1.45 | 1.39 | ||||||
| Oats hulls | 3.00 | 3.00 | 3.00 | 3.00 | 3.00 | 3.00 | ||||||
| Sugar beet pulp | 3.00 | 3.00 | 3.00 | 3.00 | 3.00 | 3.00 | ||||||
| Soybean oil | 5.00 | 4.21 | 3.35 | 3.25 | 4.99 | 5.00 | 4.66 | 4.52 | 4.90 | 4.76 | 3.92 | 3.81 |
| Dicalcium phosphate | 1.05 | 1.08 | 1.04 | 1.04 | 0.47 | 0.46 | 0.41 | 0.42 | 0.20 | 0.20 | 0.18 | 0.18 |
| Calcium carbonate | 1.00 | 0.97 | 0.98 | 0.94 | 1.02 | 0.99 | 0.98 | 0.93 | 0.88 | 0.84 | 0.81 | 0.77 |
| Sodium bicarbonate | 0.24 | 0.22 | 0.30 | 0.30 | 0.19 | 0.20 | 0.25 | 0.24 | 0.19 | 0.18 | 0.23 | 0.22 |
| Salt | 0.18 | 0.18 | 0.14 | 0.13 | 0.19 | 0.17 | 0.15 | 0.15 | 0.19 | 0.19 | 0.17 | 0.16 |
| DL-methionine 99% | 0.27 | 0.28 | 0.22 | 0.22 | 0.24 | 0.22 | 0.21 | 0.21 | 0.22 | 0.22 | 0.20 | 0.20 |
| L-Lysine HCl 98% | 0.20 | 0.17 | 0.27 | 0.31 | 0.17 | 0.23 | 0.25 | 0.25 | 0.16 | 0.16 | 0.19 | 0.19 |
| L-Threonine min. 98% | 0.05 | 0.04 | 0.03 | 0.04 | 0.05 | 0.05 | 0.05 | 0.05 | 0.04 | 0.04 | 0.03 | 0.03 |
| Nonstarch polysaccharide enzyme3 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 | 0.05 |
| Phytase | 0.01 | 0.01 | 0.01 | 0.01 | 0.01 | 0.01 | 0.01 | 0.01 | 0.01 | 0.01 | 0.01 | 0.01 |
| Vitamin and mineral premix4 | 0.35 | 0.35 | 0.35 | 0.35 | 0.35 | 0.35 | 0.35 | 0.35 | 0.35 | 0.35 | 0.35 | 0.35 |
Oat hulls.
Sugar beet pulp.
Commercially available enzyme that provided 500 units of endo-1,4-beta-xylanase.
Provided the following (per kilogram of diet): 10,000-IU vitamin A (trans-retinyl acetate), 2,500-IU vitamin D3 (cholecalciferol), 50-IU vitamin E (all-rac-tocopherol-acetate), 2.0-mg vitamin B1 (thiamine-mononitrate), 6-mg vitamin B2 (riboflavin), 40-mg niacin, 490-mg vitamin B4 choline cl 70%, 4.0-mg vitamin B6 (pyridoxine HCl), 25-mcg vitamin B12 (cyanocobalamin), 2.0-mg vitamin K3 (bisulfate menadione complex), 10-mg pantothenic acid (d-Ca pantothenate), 1.0-mg folic acid, 150-mcg d-biotin, 0.25 mg Se (Na2SeO3),1.0-mg I, 15-mg Cu (CuSO4·5H2O), 67.7-mg Fe (FeSO4·7H2O), 90-mg Mn (MnSO4·H2O), 80-mg Zn (ZnO), (supplied by Trouw Nutrition, St. Mary's Ontario Canada), 500-mg Salinomycin sodium 12%.
Table 3.
Calculated and analyzed (%, as-fed basis, unless otherwise indicated) nutrient and energy concentration of experimental diets during the 3 feeding phases (day 0–36 of age).
| Starter (Day 0–14 of age) | Grower (Day 14–28 of age) | Finisher (Day 28–36 of age) | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Protein digestion rate |
Rapidly |
Slowly |
Rapidly |
Slowly |
Rapidly |
Slowly |
||||||
| Dietary fiber source | OH1 | SBP2 | OH | SBP | OH | SBP | OH | SBP | OH | SBP | OH | SBP |
| Calculated analysis | ||||||||||||
| Dry matter | 87.65 | 87.32 | 87.32 | 87.29 | 87.42 | 87.53 | 87.48 | 87.35 | 87.34 | 87.23 | 86.95 | 86.86 |
| Total ash | 5.63 | 5.80 | 5.37 | 5.49 | 4.84 | 4.91 | 4.61 | 4.76 | 4.30 | 4.46 | 4.16 | 4.31 |
| Crude protein | 21.50 | 21.50 | 21.50 | 21.50 | 20.12 | 20.50 | 19.90 | 20.00 | 19.00 | 19.11 | 18.50 | 18.55 |
| Ether extract | 6.62 | 6.03 | 5.42 | 5.24 | 6.66 | 6.47 | 6.43 | 6.33 | 6.48 | 6.38 | 6.07 | 5.96 |
| Starch | 30.54 | 31.12 | 33.31 | 33.71 | 33.20 | 33.52 | 34.91 | 34.86 | 35.35 | 35.32 | 36.94 | 37.02 |
| AMEn (kcal/kg) | 2,700 | 2,700 | 2,700 | 2,700 | 2,775 | 2,775 | 2,775 | 2,775 | 2,800 | 2,800 | 2,800 | 2,800 |
| Crude fiber | 3.42 | 2.57 | 3.74 | 3.19 | 3.17 | 2.65 | 3.85 | 3.26 | 3.19 | 2.61 | 3.69 | 3.12 |
| Total dietary fiber | 18.85 | 17.58 | 18.68 | 17.93 | 18.26 | 17.50 | 18.95 | 18.17 | 18.24 | 17.47 | 18.61 | 17.86 |
| Determined analysis | ||||||||||||
| Dry matter | 87.40 | 87.30 | 87.30 | 88.30 | 87.70 | 88.40 | 88.60 | 88.00 | 87.80 | 88.00 | 87.70 | 87.90 |
| Total ash | 4.72 | 4.76 | 4.95 | 4.65 | 4.80 | 4.90 | 5.10 | 5.20 | 3.90 | 4.22 | 4.28 | 4.13 |
| Crude protein | 25.40 | 21.60 | 22.20 | 20.60 | 20.90 | 21.20 | 20.20 | 19.80 | 18.60 | 20.10 | 19.80 | 19.50 |
| Crude Fat | 6.65 | 5.71 | 2.67 | 4.82 | 6.20 | 6.90 | 6.80 | 6.70 | 5.77 | 6.54 | 6.16 | 6.15 |
| Starch | 30.70 | 32.20 | 35.50 | 35.20 | 35.50 | 32.50 | 36.50 | 35.60 | 37.10 | 34.20 | 34.50 | 35.00 |
| Crude fiber | 3.12 | 2.81 | 3.09 | 3.19 | 3.30 | 3.30 | 3.80 | 3.70 | 3.70 | 3.14 | 3.94 | 3.51 |
| Total dietary fiber | 17.70 | 16.90 | 16.10 | 17.01 | 15.62 | 15.83 | 16.40 | 15.33 | 15.54 | 16.95 | 18.90 | 18.40 |
| Soluble dietary fiber | 1.90 | 1.90 | 1.90 | 1.90 | 1.40 | 1.80 | 1.30 | 1.70 | 1.60 | 1.60 | 1.60 | 1.90 |
| Insoluble dietary | 15.80 | 15.10 | 15.10 | 14.22 | 14.43 | 13.84 | 15.05 | 13.60 | 15.30 | 13.80 | 17.43 | 16.64 |
Oat hulls.
Sugar beet pulp.
During the starter phase (day 0 to 14 of age), broilers fed diets that contained slowly digestible protein sources had a greater ADFI (36.7 vs. 34.8 g/d; P < 0.05) and an inferior FCR (1.34 vs. 1.30 g/g; P < 0.05) than birds fed diets that contained rapidly digestible protein sources (especially from day 8 to 14 of age), however, the ADG was not different (Table 4). In addition, from day 0 to 14 of age, broilers fed OH resulted in a greater ADFI (36.6 vs. 34.9 g/d; P < 0.05) and ADG (27.5 vs. 26.5 g/d; P < 0.05), but the positive effect of 3% OH inclusion was not reflected in the FCR. There was an interaction between the protein digestion rate and dietary fiber source indicating that the ADFI and ADG were improved (P < 0.05) when broilers were fed 3% OH in the diet that contained slowly digestible protein sources (Table 4). During the grower phase (day 14 to 28 of age), the ADFI was not affected by either the protein digestion rate or dietary fiber source. However, broilers fed diets that contained rapidly digestible protein sources had a greater ADG (77.5 vs. 74.0 g/d; P < 0.05) and an improved FCR (1.42 vs. 1.48 g/g; P < 0.05) than broilers fed diets that contained slowly digestible protein sources (Table 5). In the finisher phase (from day 28–36 of age), a similar pattern as in the grower phase was observed. Broilers fed diets that contained rapidly digestible protein sources had a greater ADG (84.0 vs. 80.3 g/d; P < 0.05) and an improved FCR (1.79 vs. 1.87 g/g; P < 0.05) relative to broilers fed diets that contained slowly digestible protein sources (Table 6). There was an interaction between the protein digestion rate and dietary fiber source, which indicated that the ADG was less and FCR was inferior (P < 0.05) when broilers were fed 3% SBP in the diet that contained slowly digestible protein sources. Overall (day 0–36), broilers fed diets that contained rapidly digestible protein sources had a greater ADG (57.6 vs. 55.5 g/d; P < 0.05) and improved FCR (1.51 vs. 1.58 g/g; P < 0.05) compared with broilers fed diets that contained slowly digestible protein sources (Table 6). In addition, there was an interaction between the protein digestion rate and dietary fiber source, which indicated that broiler ADG was less (P < 0.05) when broilers were fed diets that contained slowly digestible protein sources supplemented with 3% SBP (Table 6).
Table 4.
Influence of protein digestion rates and dietary fiber sources on growth performance of broilers from day 0 to 14 of age.
| Item | Rapidly digested protein |
Slowly digested protein |
SEM3 |
P-values |
||||
|---|---|---|---|---|---|---|---|---|
| SBP1 | OH2 | SBP1 | OH2 | Protein | Dietary fiber | Protein × dietary fiber | ||
| Initial BW4 | 39.2 | 39.6 | 39.3 | 39.3 | 0.341 | 0.546 | 0.189 | 0.281 |
| Day 0 to 8 | ||||||||
| BW day 8 | 171.0b | 172.0b | 168.0b | 180.0a | 2.33 | 0.302 | 0.003 | 0.011 |
| ADFI5 | 20.6 | 21.4 | 20.9 | 22.3 | 0.406 | 0.132 | 0.007 | 0.395 |
| ADG6 | 16.4b | 16.5b | 16.1b | 17.4a | 0.281 | 0.240 | 0.005 | 0.018 |
| FCR7 | 1.26 | 1.30 | 1.30 | 1.28 | 0.016 | 0.426 | 0.580 | 0.081 |
| Day 8 to 14 | ||||||||
| BW day 14 | 443.0b | 448.0b | 438.0b | 467.0a | 5.01 | 0.065 | 0.006 | 0.009 |
| ADFI | 51.2b | 52.0b | 52.1b | 56.5a | 0.570 | <0.001 | <0.001 | 0.001 |
| ADG | 38.7b | 39.3b | 38.3b | 40.8a | 0.514 | 0.099 | <0.001 | 0.005 |
| FCR | 1.32b | 1.32b | 1.36b | 1.38a | 0.008 | <0.001 | 0.014 | 0.008 |
| Day 0 to 14 | ||||||||
| ADFI | 34.5b | 35.2b | 35.4b | 38.0a | 0.460 | 0.001 | 0.003 | 0.082 |
| ADG | 26.7b | 26.8b | 26.4b | 28.2a | 0.414 | 0.113 | 0.007 | 0.010 |
| FCR | 1.29b | 1.31b | 1.34a | 1.35a | 0.070 | 0.001 | 0.356 | 0.662 |
a,bMeans not sharing the same superscript letter across each row differ at P ≤ 0.05 based on the interactive effect.
Sugar beet pulp.
Oat hull.
SEM (n = 12).
BW, g.
ADFI, g/d.
ADG, g/d.
Feed conversion ratio, g/g.
Table 5.
Influence of protein digestion rates and dietary fiber sources on growth performance of broilers from day 14 to 28 of age.
| Item | Rapidly digested protein |
Slowly digested protein |
SEM3 |
P-values |
||||
|---|---|---|---|---|---|---|---|---|
| SBP1 | OH2 | SBP | OH | Protein | Dietary fiber | Protein × dietary fiber | ||
| Day 14 to 22 | ||||||||
| BW4 day 22 | 897a,b | 913a | 862b | 902a,b | 8.91 | 0.001 | 0.001 | 0.072 |
| ADFI5 | 88.4 | 90.1 | 88.6 | 91.5 | 0.839 | 0.243 | 0.002 | 0.317 |
| ADG6 | 64.5 | 65.3 | 60.2 | 61.2 | 0.868 | 0.001 | 0.196 | 0.834 |
| FCR7 | 1.37 | 1.39 | 1.47 | 1.50 | 0.010 | 0.001 | 0.063 | 0.711 |
| Day 22 to 28 | ||||||||
| BW day 28 | 1,464a | 1,454a,b | 1,406b | 1,448a,b | 14.82 | 0.017 | 0.214 | 0.052 |
| ADFI | 135b | 134b | 135b | 140a | 1.52 | 0.118 | 0.156 | 0.037 |
| ADG | 93.0a | 91.9a | 88.1b | 91.0b | 1.40 | 0.045 | 0.520 | 0.152 |
| FCR | 1.46b | 1.45b | 1.53a | 1.54a | 0.014 | 0.001 | 0.834 | 0.499 |
| Day 14 to 28 | ||||||||
| ADFI | 149 | 151 | 147 | 153 | 1.48 | 0.130 | 0.256 | 0.127 |
| ADG | 77.8a | 77.3a | 73.8b | 74.3b | 1.38 | 0.003 | 0.946 | 0.535 |
| FCR | 1.42b | 1.42b | 1.45a | 1.52a | 0.025 | 0.001 | 0.164 | 0.360 |
a,bMeans not sharing the same superscript letter across each row differ at P ≤ 0.05 based on the interactive effect.
Sugar beet pulp.
Oat hull.
SEM (n = 12).
BW, g.
ADFI, g/d.
ADG, g/d.
Feed conversion ratio, g/g.
Table 6.
Influence of protein digestion rates and dietary fiber sources on growth performance of broilers from day 28 to 36 of age.
| Item | Rapidly digested protein |
Slowly digested protein |
SEM3 |
P-values |
||||
|---|---|---|---|---|---|---|---|---|
| SBP1 | OH2 | SBP1 | OH2 | Protein | Dietary fiber | Protein × dietary fiber | ||
| Day 28 to 36 | ||||||||
| BW4 day 36 | 2,142a | 2,145a | 2,026b | 2,133a | 18.49 | 0.005 | 0.038 | 0.001 |
| ADFI5 | 149 | 151 | 147 | 153 | 1.48 | 0.797 | 0.079 | 0.330 |
| ADG6 | 85.0a | 83.0a | 77.5b | 83.1a,b | 1.38 | 0.006 | 0.228 | 0.041 |
| FCR7 | 1.76b | 1.83b | 1.91a | 1.84a,b | 0.025 | <0.001 | 0.568 | 0.002 |
| Overall, day 0–36 | ||||||||
| ADFI | 86.7 | 87.7 | 86.3 | 89.8 | 0.889 | 0.147 | 0.068 | 0.153 |
| ADG | 57.8a | 57.4a | 54.2b | 56.8a,b | 0.625 | 0.002 | 0.226 | 0.032 |
| FCR | 1.50b | 1.52b | 1.59a | 1.58a | 0.008 | <0.001 | 0.388 | 0.235 |
a,bMeans not sharing the same superscript letter across each row differ at P ≤ 0.05 based on the interactive effect.
Sugar beet pulp.
Oat hull.
SEM (n = 12).
BW, g.
ADFI, g/d.
ADG, g/d.
Feed conversion ratio, g/g.
Discussion
Effect of Using Rapidly or Slowly Digestible Protein Sources in Broiler Diets
Results indicated that formulating diets to contain rapidly digestible protein sources increased the broiler ADG and improved FCR. However, economics of using rapidly digestible protein sources in diets must be considered as these ingredients can typically be more costly.
Therefore, we hypothesized that the addition of OH to diets containing less-expensive slowly digestible protein sources could ameliorate the loss in performance that results from including slowly digestible protein sources in broiler diets. Indeed, in grower and finisher phases, there was an interaction between the protein digestion rate and dietary fiber source indicating that the ADFI and ADG was improved when broilers were fed with 3% OH in the diets that contained slowly digestible protein sources. These results confirm the hypothesis that the addition of OH to diets containing slowly digestible protein sources would ameliorate the reduced performance. The supplementation of 3% OH to diets that contained slowly digestible protein sources potentially increased the passage rate and improved the GIT development and, thereby, improved protein digestion rates to similar levels as the diets which contained rapidly digestible protein sources. In this respect, Hetland and Svihus (2001) reported an increased passage rate of digesta with inclusion of OH and hypothesized that a rapid feed passage would decrease time for microbial fermentation in the small intestine and, thus, less protein will be fermented resulting in improved GIT development and health. The positive results of including rapidly digestible protein sources in broiler diets are in agreement with most data published. In this respect, Jaworski et al. (2019) studied the influence of 3 different levels of protein digestion rate (low, medium, and high) and reported that broilers fed diets with high concentrations of rapidly digested protein had 12% heavier BW than broilers fed diets containing a low level of rapidly digestible protein. In addition, Liu et al. (2017) reported that the feed conversion efficiency might be improved by inclusion of rapidly digestible protein sources. Furthermore, Truong et al. (2017) offered broiler chickens 2 diets containing different rates of protein digestion (rapidly vs. slowly) and reported that the rapidly digestible protein diet had significantly higher apparent digestibility coefficients of AA in the distal jejunum and distal ileum. The beneficial effect observed in birds fed diets containing rapidly digestible protein may also be due to these sources being rapidly absorbed in the proximal small intestine, suggesting that there was less undigested protein in the ileal digesta. In this respect, Goldberg and Guggenheim (1962) compared the digestion of AA and their appearance in portal circulation in rats offered either casein, as a rapidly digestible protein source, or soy flour, as a slowly digestible protein source. The authors reported that a greater proportion of lysine was absorbed and entered the portal circulation from casein, the more rapidly digested protein source.
Effect of Type of Dietary Fiber in the Diet
From day 0 to 14 of age, broilers fed diets containing 3% SBP had a reduced ADFI compared with broilers fed diets containing 3% OH. In addition, in finisher and the overall period, broilers fed diets containing 3% SBP tended to have reduced ADFI. These results are in disagreement with the data of Jimenez-Moreno et al. (2013b) and Rogel et al. (1987). In the studies of Jimenez-Moreno et al. (2013b), broilers were fed with increased levels of OH (2.5, 5.0, and 7.5%), and the authors did not find any improvement on the ADFI. In addition, Rogel et al. (1987) reported similar ADFI in broilers fed 40 or 60 g OH/kg diet to broilers fed the control diet. The discrepancy between our study and previous reports is most likely because we compared 2 different sources of dietary fiber at similar concentrations of the TDF, whereas others compared the same source of dietary fiber, but at increased inclusion rates (i.e., increased concentrations of TDF). The increased addition of OH (or any other fiber source) would typically limit the ADFI because the TDF would be increased in the diets, whereas in our study, the TDF was similar among experimental treatments. Therefore, it actually appears that an increased SDF from SBP reduced broiler ADFI, rather than OH improving the ADFI.
In contrast, Gonzalez-Alvarado et al. (2010) reported improvements in the ADFI from day 1 to 42 of age in broilers fed with 3% OH compared with broilers fed with 3% SBP, in agreement of the results obtained in the current experiment. In addition, Hetland and Svihus (2001) determined that broilers fed with 40 g OH/kg diet increased the ADFI from day 7 to 21 of age. In this respect, Montagne et al. (2003) reported that an increase in IDF increased the rate of passage of digesta through the distal part of the GIT that in turn might result in a greater feed intake. On the other hand, the reduction of the ADFI in broilers fed 3% SBP was expected. The pectin content in SBP is characterized by its high WHC and SWC (Serena and Bach Knudsen, 2007; Gonzalez-Alvarado et al., 2010), and in this study, it was twice as much as OH. A wetter and bulkier digesta caused by inclusion of SBP in the diet could result in an increase in gut fill, and delayed emptying of the GIT, reducing feed intake. On the other hand, in the current experiment, from day 0 to 14 of age, broilers fed with 3% OH had improved ADG compared with broilers fed with 3% SBP. In this respect, Gonzalez-Alvarado et al. (2010) also reported improvements in ADG when broilers were fed with 3% OH compared with broilers fed a diet containing 3% SBP or a control diet from day 25 to 42 of age and for the entire experimental period. The increase of ADG detected in broilers fed with OH might account for the differences in the ADFI observed between broilers fed OH and SBP. Finally, broilers fed with 3% OH improved energy efficiency (g BW gain/Kcal AMEn ingested) compared with broilers fed with 3% SBP. The difference in energy efficiency between diets could be attributed to differences in their physicochemical characteristics that might affect gut motility, microbiota growth, and voluntary feed intake of the birds. In addition, the ether extract and oil content in the diets of the current experiments were higher in OH diets than SBP diets. In this respect, Hetland et al. (2003) reported that the inclusion of 100 g OH/kg diet increased bile acids' concentration in the chime, which in turn, could improve lipid digestibility in young broilers. Further research would be required to validate the relative interaction effects on nutrient digestibility throughout the digestive tract to confirm these hypotheses.
In conclusion, broilers fed diets containing rapidly digestible protein sources had an increased ADG and improved FCR throughout the experiment, but most notably after the starter phase. Inclusion of IDF such as OH improved the ADFI and ADG in the starter phase compared with SBP, an SDF source. However, this was not reflected in an improvement on the FCR. The ADG and FCR of broilers fed diets that contained slowly digestible protein sources could be improved to the level of broilers fed diets containing rapidly digestible protein sources by adding 3% OH. These results confirm the hypothesis that the addition of OH to diets that contain slowly digestible protein sources would ameliorate the reduced performance of broilers fed slowly digestible protein diets. It is concluded that broiler diets should be formulated to contain a high concentration of rapidly digestible protein sources, but if this is cost-prohibitive, then 3% OH or potentially other IDF sources can be used to increase the ADFI and ADG and potentially protein digestion rates to reduce the FCR.
Acknowledgments
The authors would like to acknowledge the staff at Trouw Nutrition Agresearch (Burford, Ontario, Canada), especially Lan You, for study design considerations, conducting the study, and data collection.
Conflict of Interest Statement: There are no conflicts of interest in this manuscript.
References
- AOAC International . 17th ed. AOAC Int.; Gaithersburg, MD: 2000. Official Methods of Analysis of AOAC International. [Google Scholar]
- AOAC International . AOAC International; Gaithersburg, MD: 2005. Official Method of Analysis of AOAC International Method 920.39, Fat (Crude) or Ether Extract in Animal Feed. [Google Scholar]
- AOAC International . AOAC International; Gaithersburg, MD: 2007. Official Methods of Analysis of AOAC International. 18th ed. Methods 925.10, 985.29, 991.42, 991.43, 993.19, 994.13, 996.01, 2001.03, 2002.01, 2002.02, 2009.01, and 2011.25. [Google Scholar]
- ASAE . ASAE; St. Joseph, MO: 1995. ASAE Standard S319.2. Method of Determining and Expressing Fineness of Feed Materials by Sieving. ASAE, Ed. Agricultural Engineers Yearbook of Standards. [Google Scholar]
- Boirie Y., Dangin M., Gachon P., Vasson M.P., Maubois J.L., Beaufrère B. Slow and fast dietary proteins differently modulate postprandial protein. Proc. Natl. Acad. Sci. U S A. 1997;94:14930–14935. doi: 10.1073/pnas.94.26.14930. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bryan D.D.S.L., Abbott D.A., Classen H.L. Development of an in vitro protein digestibility assay mimicking the chicken digestive tract. Anim. Nutr. 2018;4:401–409. doi: 10.1016/j.aninu.2018.04.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bryan D.D.S.L., Abbott D.A., Classen H.L. Digestion kinetics of protein sources determined using an in vitro chicken model. Anim. Feed Sci. Technol. 2019;248:106–113. [Google Scholar]
- Bryan D.D.S.L., Van Kessel A.G., Classen H.L. In vivo digestion characteristics of protein sources fed to broilers. Poult. Sci. 2019;98:3313–3325. doi: 10.3382/ps/pez067. [DOI] [PubMed] [Google Scholar]
- CCAC (Canadian Council of Animal Care) Guidelines on: the care and use of farm animals in research, teaching, and testing. 2009. http://www.ccac.ca/en/CCAC_Main. htm
- CVB Feed Table . Central Bureau for Livestock Feeding (CVB); Lelystad, the Netherlands: 2016. Chemical Composition and Nutritional Values of Feedstuffs. [Google Scholar]
- Dangin M., Boirie Y., Garcia-Rodenas C., Gachon P., Fauquant J., Callier P., Ballevre O., Beaufrere B. The digestion rate of protein is an independent regulating factor of postprandial protein retention. Am. J. Physiol. Endocrinol. Metab. 2001;280:340–348. doi: 10.1152/ajpendo.2001.280.2.E340. [DOI] [PubMed] [Google Scholar]
- Goldberg A., Guggenheim K. Digestive release of amino acids and their concentrations in portal plasma of rats after protein feeding. Biochem. J. 1962;83:129–135. doi: 10.1042/bj0830129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- González-Alvarado J.M., Jiménez-Moreno E., Valencia D.G., Lázaro R., Mateos G.G. Effects of fiber source and heat processing of the cereal on the development and pH of the gastrointestinal tract of broilers fed diets based on corn or rice. Poult. Sci. 2008;87:1779–1795. doi: 10.3382/ps.2008-00070. [DOI] [PubMed] [Google Scholar]
- González-Alvarado J.M., Jiménez-Moreno E., González-Sánchez D., Lázaro R., Mateos G.G. Effect of inclusion of oat hulls and sugar beet pulp in the diet on productive performance and digestive traits of broilers from 1 to 42 days of age. Anim. Feed Sci. Technol. 2010;162:37–46. [Google Scholar]
- Gutiérrez del Álamo A., Verstegen M.W.A., Den Hartog L.A., de Ayala P.P., Villamide M.J. Wheat starch digestion rate affects broiler performance. Poult. Sci. 2009;88:1666–1675. doi: 10.3382/ps.2008-00502. [DOI] [PubMed] [Google Scholar]
- Hetland H., Choct M., Svihus B. Role of insoluble nonstarch polysaccharides in poultry nutrition. Worlds Poult. Sci. J. 2004;60:415–422. [Google Scholar]
- Hetland H., Svihus B. Effect of oat hulls on performance, gut capacity and feed passage time in broiler chickens. Br. Poult. Sci. 2001;42:354–361. doi: 10.1080/00071660120055331. [DOI] [PubMed] [Google Scholar]
- Hetland H., Svihus B., Krögdahl Å. Effects of oat hulls and wood shavings on digestion in broilers and layers fed diets based on whole or ground wheat. Br. Poult. Sci. 2003;44:275–282. doi: 10.1080/0007166031000124595. [DOI] [PubMed] [Google Scholar]
- Jaworski N.W., Boerboom G., Jacobs M., Alfonso C., Geerse K., Dijkslag A., Ramaekers P., Smits C.H.M. Effects of different levels of fast digestible starch, protein, and fiber on broiler growth performance. Aust. Poult. Sci. Symp. 2019;30:11–14. [Google Scholar]
- Jimenez-Moreno E., Frikha M., de Coca-Sinova A., Garcıa J., Mateos G.G. Oat hulls and sugar beet pulp in diets for broilers 1. Effects on growth performance and nutrient digestibility. Anim. Feed Sci. Technol. 2013;182:33–43. [Google Scholar]
- Jimenez-Moreno E., Frikha M., de Coca-Sinova A., Lázaro R.P., Mateos G.G. Oat hulls and sugar beet pulp in diets for broilers. 2. Effects on the development of the gastrointestinal tract and on the structure of the jejunal mucosa. Anim. Feed Sci. Technol. 2013;182:44–52. [Google Scholar]
- Jiménez-Moreno E., González-Alvarado J.M., de Coca-Sinova A., Lázaro R.P., Cámara L., Mateos G.G. Insoluble fiber sources in mash or pellets diets for young broilers. 2. Effects on gastrointestinal tract development and nutrient digestibility. Poult. Sci. 2019;98:2531–2547. doi: 10.3382/ps/pey599. [DOI] [PubMed] [Google Scholar]
- Jimenez-Moreno E., González-Alvarado J.M., de Coca-Sinova A., Lázaro R., Mateos G.G. Effects of source of fiber on the development and pH of the gastrointestinal tract of broilers. Anim. Feed Sci. Technol. 2009;154:93–101. [Google Scholar]
- Koopman R., Crombach N., Gijsen A.P., Walrand S., Fauquant J., Kies A.K., Lemosquet S., Saris W.H.M., Boirie Y., van Loon L.J.C. Ingestion of a protein hydrolysate is accompanied by an accelerated in vivo digestion and absorption rate when compared with its intact protein. Am. J. Clin. Nutr. 2009;90:106–115. doi: 10.3945/ajcn.2009.27474. [DOI] [PubMed] [Google Scholar]
- Liu S.Y., Cadogan D.J., Peron A., Truong H.H., Selle P.H. A combination of xylanase, amylase and protease influences growth performance, nutrient utilisation, starch and protein digestive dynamics in broiler chickens offered maize-, sorghum- and wheat-based diets. Anim. Prod. Sci. 2015;55:1255–1263. [Google Scholar]
- Liu S.Y., Selle P.H., Cowieson A.J. Influence of white- and red-sorghum varieties and hydrothermal component of steam-pelleting on digestibility coefficients of amino acids and kinetics of amino acids, nitrogen and starch digestion in diets for broiler chickens. Anim. Feed Sci. Technol. 2013;186:53–63. [Google Scholar]
- Liu S.Y., Selle P.H., Raubenheimer D., Cadogan D.J., Simpson S.J., Cowieson A.J. An assessment of the influence of macronutrients on growth performance and nutrient utilisation in broiler chickens by nutritional geometry. Br. J. Nutr. 2017;116:2129–2138. doi: 10.1017/S0007114516004190. [DOI] [PubMed] [Google Scholar]
- Montagne L., Pluske J.R., Hampson D.J. A review of interactions between dietary fiber and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Anim. Feed Sci. Technol. 2003;108:95–117. [Google Scholar]
- Moss A.F., Sydenhama C.J., Khoddamia A., Naranjo V.D., Liu S.Y., Selle P.H. Dietary starch influences growth performance, nutrient utilisation and digestive dynamics of protein and amino acids in broiler chickens offered low-protein diets. Anim. Feed Sci. Technol. 2018;237:55–67. [Google Scholar]
- Ørskov E.R., Mc Donald I. The estimation of protein degradability in the rumen from incubation measurements weighted according to rate of passage. J. Agric. Sci. 1979;92:499–503. [Google Scholar]
- Rogel A.M., Balnave D., Bryden W.L., Annison E.F. Improvement of raw potato starch digestion in chickens by feeding oat hulls and other fibrous feedstuffs. Aust. J. Agric. Res. 1987;38:629–637. [Google Scholar]
- Sacranie A., Svihus B., Denstadli V., Moen B., Iji P.A., Choct M. The effect of insoluble fiber and intermittent feeding on gizzard development, gut motility, and performance of broiler chickens. Poult. Sci. 2012;91:693–700. doi: 10.3382/ps.2011-01790. [DOI] [PubMed] [Google Scholar]
- Serena A., Bach Knudsen K.E. Chemical and physicochemical characterisation of co-products from the vegetable food and agro industries. Anim. Feed Sci. Technol. 2007;139:109–124. [Google Scholar]
- Truong H.H., Chrystal P.V., Moss A.F., Selle P.H., Liu S.Y. Rapid protein disappearance rates along the small intestine advantage poultry performance and influence the post-enteral availability of amino acids. Br. J. Nutr. 2017;118:1031–1042. doi: 10.1017/S0007114517003257. [DOI] [PubMed] [Google Scholar]