Abstract
This study was to evaluate the effects of rapeseed (Brassica napus L.) from China with different content of glucosinolate (Gls) and erucic acid (EA) on laying hens. A total of 600 laying hens at 33 wk of age were randomly divided into 5 treatments containing a control diet and 4 diets with 11.5% rapeseed. The 11.5% rapeseed diets varied in Gls and EA levels: 1) Deyou no. 6 (DY6) with Gls at 22.67 μmol/g and EA at 0.7%, 2) Mianbangyou no. 1 (MB1) with Gls at 43.23 μmol/g and EA at 3.5%, 3) Deyou no. 5 (DY5) with Gls at 74.66 μmol/g and EA at 16.20%, 4) Xiheyou no. 3 (XH3) with Gls at 132.83 μmol/g and EA at 44.60%. Each group had eight replicates and each replicate had 15 hens. The trial lasted for 12 wk with 4 wk withdrawal. From 1 to 8 wk of the trial, 11.5% rapeseed reduced average daily feed intake (ADFI) compared to the control group (P = 0.002), and egg-laying rate of XH3 rapeseed was lower than that of DY6 rapeseed (P = 0.006), and egg weight of MB1, DY5, and XH3 rapeseed were lower than that of the control group (P = 0.007). Egg mass was reduced by 11.5% rapeseed and egg mass of XH3 and DY5 rapeseed were lower than that of DY6 rapeseed (P = 0.004). Feed conversion ratio (FCR) of 11.5% rapeseed was higher than that the control group and FCR was higher in XH3 rapeseed than in DY6 rapeseed from 1 to 8 wk (P = 0.008). At wk 8, the lightness value of eggshell color of XH3 rapeseed was significantly lower than that of the control and DY5 rapeseed (P = 0.012). Xiheyou no. 3 rapeseed had a higher redness value of eggshell color than the control and MB1 and DY5 rapeseed (P = 0.008). Albumen height of DY5 rapeseed was lower than that of the control group at wk 8 (P = 0.012). Mianbangyou no. 1 and DY5 rapeseed decreased Haugh unit at wk 4 and 8, respectively (P = 0.011, P = 0.024). Serum estradiol (E2) content was decreased by 11.5% rapeseed (P = 0.003). Thyroid index increased as the Gls and EA content increased (P = 0.008). The smallest hierarchical follicle numbers of XH3 and MB1 rapeseed were lower than that of the control group (P = 0.009). After 4 wk withdrawal, the egg weight, egg mass, and FCR did not recover (P = 0.011, P = 0.033, P = 0.024, respectively). In conclusion, 11.5% rapeseed decreased egg production performance which might be caused by decreasing hormone levels, and high Gls and EA rapeseed had a lower performance than low Gls and EA rapeseed.
Keywords: Brassica napus rapeseed variety, Laying hens, Egg production performance, Hormone level, Follicle number, Organ index
1. Introduction
Rapeseed or canola is an oil crop that is widely grown around the world. Full-fat rapeseed contains approximately 40% oil and 21% to 23% protein and is therefore a valuable source of energy and protein in poultry diets (Ajuyah et al., 1993). Rapeseed protein has a physiologically suitable amino acid composition, including a high content of essential amino acids like lysine, threonine, tryptophan and sulphur-containing amino acids (Chmielewska et al., 2021). Moreover, rapeseed has also been known to be a good source of α-linolenic acid (ALA, C18:3n-3), which can be readily converted to n-3 LC-PUFA in poultry (Li et al., 2017). However, rapeseed contains nutritionally unfavorable substances such as glucosinolates, sinapine, tannins, and phytates which may negatively influence many physiological processes and adversely impact health status (Chmielewska et al., 2021). There are relatively few reports in the literature on the nutritive value of unextracted rapeseed for laying birds. Olomu et al. (1975) observed that 15% rapeseed had no adverse effects on egg production performance and internal egg quality. Lichovnikova and Zeman (2004) also observed that 13.5% rapeseed had no effect on egg performance or internal egg quality. Canola was originally derived from rapeseed varieties; its components have been altered through genetic selection which has markedly reduced its detrimental components, erucic acid and the glucosinolates, to a negligible level and to less than 20 μg/g which is low enough to be of little or no harm to poultry (Najib and Al-Khateeb, 2004). Research has shown that 5% to 10% canola seed in hens’ diets improved egg production, and 20% canola seed reduced egg performance including egg production, egg weight, and feed conversion (Najib and Al-Khateeb, 2004 had no effect on feed intake. Leslie and Summers (1972) showed that 5% rapeseed significantly reduced egg weight, 10% rapeseed had no effect on egg performance except egg weight, and for egg quality, 15% rapeseed could be used in laying hens' diets (Leslie and Summers, 1972). There are some inconsistencies in the results of the current study, and more data is needed to determine its dosage in layer diets.
China is not only the world's second largest producer of rapeseeds (FAO, 2019), but also breeds many rapeseed varieties with high or low glucosinolates (Gls) and erucic acid (EA) content. Given that rapeseed may affect the performance and egg quality in laying hens, and there are no studies to compare the difference between different rapeseed varieties used in feed, we conducted the following experiment. We chose 4 kinds of Brassica napus rapeseed with different Gls and EA content: Deyou no. 5 (DY5), Deyou no. 6 (DY6), Mianbangyou no. 1 (MB1), and Xiheyou no. 3 (XH3) (Gls and EA content: DY6 < MB1 < DY5 < XH3), which were produced from different geographic regions in Sichuan province of China (DY5 and DY6 rapeseed from Deyang City, MB1 and XH3 rapeseed from Mianyang City) to evaluate the effects of different kinds of raw unbroken rapeseed on production performance, egg quality, and organ index. At the same time, we also examined the production performance after the 4-wk rapeseed withdrawal period to provide some theoretical data for the use of rapeseed in industrial production.
2. Material and methods
2.1. Animal ethics statement
Animal procedures were performed according to the Guidelines for Care and Use of Laboratory Animals of Sichuan Agricultural University and approved by the Animal Care Advisory Committee of Sichuan Agricultural University (approval no. YYS160915).
2.2. Hens, diets, and management
At 33 wk of age, a total of 600 laying hens (Lohmann white, Sun Daily Inc., Chengdu, Sichuan, China) were randomly assigned to 5 dietary treatments with 8 replicates per group and 15 hens per replicate (3 hens/cage, cage size: 38.2 cm × 50.1 cm × 40.0 cm) including a control group (corn-soybean diet) and 4 groups with 11.5% raw unbroken rapeseed (DY5, DY6, MB1, and XH3). The experiment lasted for 12 wk, which comprised of an 8-wk experimental deposition period and a 4-wk withdrawal period. Hens were housed individually in stainless steel cages and the room environment was controlled at 22 °C by a daily lighting schedule of 16 h light and 8 h dark. Hens were allowed ad libitum access to experimental diets and water. The hens were fed diets in mash form (Table 1) during the experiment, which were formulated to meet or exceed energy and nutrient requirements of hens according to NRC (1994) and a published management guide (Lohmann Tierzucht GmbH, Cuxhaven, Lower Saxony, Germany). The nutrient composition of feeds (Table 2) in this study referred to the China Feed Database (2014).
Table 1.
Ingredients of experimental diets (%, as-fed basis).
| Item | Control | 11.5% Rapeseed |
|---|---|---|
| Corn | 61.04 | 49.63 |
| Soybean meal (43% CP) | 26.77 | 21.69 |
| Wheat bran | 0.94 | 6.00 |
| Full-fat rapeseed | 0.00 | 11.50 |
| Corn gluten meal | 0.02 | 0.01 |
| Soybean oil | 0.98 | 0.00 |
| Calcium carbonate | 3.65 | 3.57 |
| Calcium carbonate | 4.26 | 4.26 |
| Calcium hydrophosphate | 1.17 | 1.11 |
| NaCl | 0.40 | 0.40 |
| Mineral premix 1 | 0.50 | 0.50 |
| Vitamin premix2 | 0.03 | 0.03 |
| L-Lys·HCl | 0.00 | 0.14 |
| DL-Met | 0.14 | 0.14 |
| Thr | 0.00 | 0.02 |
| Trp | 0.00 | 0.02 |
| Chloride choline | 0.10 | 0.10 |
| Rice bran and hull | 0.00 | 0.88 |
| Total | 100.00 | 100.00 |
CP= crude protein.
Provided per kilogram of diet: 60 mg Fe (FeSO4·7H2O), 8 mg Cu (CuSO4·5H2O), 60 mg Mn (MnSO4·H2O), 80 mg Zn (ZnSO4·7H2O), 0.3 mg Se (NaSeO3), and 0.35 mg I (KI).
Provided per kilogram of diet: 8000 IU, vitamin A, 1600 IU, vitamin D3, 5 IU, vitamin E, 0.8 mg vitamin B1, 2.5 mg vitamin B2, 1.5 mg vitamin B6, 0.004 mg vitamin B12, 2.2 mg D-pantothenic acid, 0.25 mg folic acid, 20 mg nicotinic acid, and 0.1 mg biotin.
Table 2.
Nutrient composition of experimental diets (%, as-fed basis).
| Item | Control | DY6 | MB1 | DY5 | XH3 |
|---|---|---|---|---|---|
| Gross energy, Cal/g | 3641.42 | 3654.93 | 3556.17 | 3557.62 | 3612.31 |
| Dry matter | 89.22 | 89.28 | 89.54 | 89.10 | 89.89 |
| CP | 16.43 | 16.85 | 16.68 | 16.87 | 17.00 |
| EE | 4.21 | 6.63 | 6.14 | 5.71 | 6.57 |
| CF | 2.99 | 10.50 | 10.47 | 9.37 | 11.12 |
CP= crude protein; EE= ether extract; CF= crude fiber; DY5 = Deyou no. 5 rapeseed; DY6 = Deyou no. 6 rapeseed; MB1 = Mianbangyou no. 1 rapeseed; XH3 = Xiheyou no. 3 rapeseed.
2.3. Productive performance
Feed intake (FI) and feed conversion ratio (FCR) were recorded every week, and egg production, egg weight, and mortality rate were monitored daily to evaluate the performance outcomes. The average weight of the eggs was calculated weekly. The egg production rate was determined by dividing the number of daily eggs by the number of hens present on the same day. To determine the egg mass, the weight was multiplied by the rate of egg production. The FCR was also calculated by dividing the average FI by the egg mass.
2.4. Sampling procedure
A daily record of egg production (2 wk) and a weekly record of feed consumption were maintained. Egg-laying rates were expressed as an average hen-day production. Every 2 wk, 3 eggs were chosen from each replicate for egg-quality measurement. At wk 8, one hen was chosen from each replicate randomly and blood samples were collected from wing veins for serum biochemical analysis, and then sacrificed by cervical dislocation. Organs including liver, thyroid, and kidneys were extracted and weighed. After the blood was collected, the tubes containing blood were centrifuged at 3000 × g at 4 °C for 10 min, and then serum was collected in new tubes and stored at −20 °C until further analysis. The organ index was calculated using the following equation: organ index (%) = (organ weight/body weight) × 100. Ovaries were removed and the hierarchical follicles were identified by size and counted. The follicles were classified by size, including small white follicles (SWF; 1 to 2 mm), large white follicles (LWF; 3 to 5 mm), small yellow follicles (SYF; 6 to 8 mm), and the smallest hierarchical follicle (F6; >8 mm).
2.5. Nutritional and antinutritional factor determination
For rapeseed, fatty acid composition was determined according to GB/T 21514-2008 (China National Standard, 2008). Glucosinolates were detected according to NY/T 1582-2007 (Ministry of Agriculture of the People’s Republic of China, 2007). Isothiocyanates were detected according to NY/T 1596-2008 (Ministry of Agriculture of the People’s Republic of China, 2008). Oxazolidinethione was detected according to NY/T 1799-2009 (Ministry of Agriculture of the People’s Republic of China, 2009). Sinapine was detected as the following steps. A sample (1 g) was accurately weighed and placed in a 100-mL triangular bottle with 50 mL methanol for ultrasonic extraction for 20 min, then filtered, and a small amount of methanol washing filter was used and the lotion was incorporated into the filtrate. The residue was extracted twice, and then the extracted liquid was combined and evaporated to dry. The residue was dissolved with 0.08 mol/L potassium dihydrogen phosphate solution in a 50-mL volumetric flask and filtered with a microporous filter membrane (0.45 μm) for HPLC analysis. Dry matter, gross energy, ether extract, crude protein, and crude fiber content of diets were detected according to the methods of GB/T 6435-2018 (China National Standard, 2018), ISO 9831:1998 (ISO, 1998), GB/T 6433-2006 (China National Standard, 2006), GB/T 24318-2009 (China National Standard, 2009), and GB/T 6434-2022 (China National Standard, 2022), respectively.
2.6. Determination of egg quality
At the end of feeding experiment, 24 eggs (3 eggs per replicate) were chosen from each group for egg quality analysis. Eggshell color (lightness: L∗, redness: a∗, and yellowness: b∗) was measured by a color meter (Minolta CR410 chroma meter, Konica Minolta Sensing Inc., Osaka, Japan). Eggshell strength was evaluated using an eggshell force gauge model II (Robotmation Co., Ltd., Tokyo, Japan). Eggshell thickness was measured on the large end, equatorial region, and small end, respectively, using an eggshell thickness gauge (Robotmation Co., Ltd., Tokyo, Japan). The egg weight, egg yolk color, and Haugh unit were evaluated using an egg multi tester (EMT-7300, Robotmation Co., Ltd., Tokyo, Japan).
2.7. Serum biochemical analysis
The level of alanine aminotransferase (ALT), aspartate aminotransferase (AST), triiodothyronine (T3), tetraiodothyronine (T4), urea, creatinine (CREA), estradiol (E2), and progesterone (P4) in serum were measured using an automatic serum biochemical analyzer (HITACH 7020, Japan).
2.8. Statistical analysis
The data are presented as the mean and SEM. One-way ANOVA and post hoc multiple mean comparison (Tukey's HSD test) were performed in order to determine differences between the samples with a confidence interval of 95%. P < 0.05 was used to indicate a significant difference. The statistical method model is as follows:
| Yijkl = μ + Ti + Pj + Sk + C(k)l + T × Sik + eijkl |
where Yijkl refers to the dependent variable; μ, the overall mean; Ti, the ith fixed treatment effect; Pj, the jth random period effect; Sk, the kth random square effect; C(k)l, the random effect of the lth steer within the kth square; T × Sik, the interaction between the ith treatment and the kth square; and eijkl, the error residual.
3. Results
3.1. Antinutritional factor content of rapeseed
Antinutritional factor content is shown in Table 3. Total Gls and oxazolidinethione content increased along a gradient (DY6 < MB1 < DY5 < XH3). In rapeseed, about 25% to 50% Gls was 2-OH-3-butenyl and Gls 3-Butenyl Gls. DY5 rapeseed had the highest sinapine content. The erucic acid content increased along a gradient (DY6 < MB1 < DY5 < XH3). Sinapine content of DY5 rapeseed was higher than that of other three rapeseeds.
Table 3.
Antinutritional factor content of four varieties rapeseed (as fed basis).
| Item | DY6 | MB1 | DY5 | XH3 |
|---|---|---|---|---|
| Total Gls1, μmol/g rapeseed cake | 22.67 | 43.23 | 74.66 | 132.83 |
| 2-OH-3-butenyl Gls, μmol/g | 4.04 | 8.93 | 17.68 | 42.96 |
| 3-Butenyl Gls, μmol/g | 1.76 | 5.54 | 10.70 | 23.44 |
| 4-OH-3-indolylmethyl Gls, μmol/g | 1.78 | 1.87 | 2.96 | 2.75 |
| Phenethyl Gls, μmol/g | 1.76 | 1.46 | 2.32 | 1.26 |
| Isothiocyanate, mg/g | 0.13 | 1.35 | 0.82 | 5.20 |
| Oxazolidinethione, mg/g | 0.06 | 0.60 | 0.82 | 2.24 |
| Sinapine, g/kg | 5.60 | 4.43 | 7.21 | 6.43 |
| Erucic acid (relative to total fatty acids), % | 0.50 | 8.50 | 22.90 | 54.00 |
Gls = glucosinolates; DY5 = Deyou no. 5 rapeseed; DY6 = Deyou no. 6 rapeseed; MB1 = Mianbangyou no. 1 rapeseed; XH3 = Xiheyou no. 3 rapeseed.
Total Gls only contains Gls with a relatively large proportion of content.
3.2. Egg production performance
The effects of rapeseed on egg production performance are shown in Tables 4 and 5. Compared to the control group, four kinds of 11.5% rapeseeds reduced ADFI from wk 1 to 4, wk 5 to 8, and wk 1 to 8 (P = 0.003, P = 0.001, P = 0.002). From wk 1 to 4, XH3 rapeseed had a significantly lower ADFI than DY6 rapeseed (P = 0.003). Egg production was reduced by 11.5% rapeseed from wk 1 to 4, wk 5 to 8, and wk 1 to 8 (P = 0.0004, P = 0.003, P = 0.006). From wk 1 to 4, there was no difference in egg-laying rate between the DY6 rapeseed and control group; as the time increased, the egg-laying rate of DY6 rapeseed was significantly lower than the control group (P = 0.003). Egg-laying rate of XH3 rapeseed was significantly lower than that of DY6 rapeseed from wk 1 to 4, wk 5 to 8, and wk 1 to 8. DY5 rapeseed had a lower egg weight than the control group from wk 1 to 4 (P = 0.030). Mianbangyou no. 1, DY5, and XH3 rapeseed had a lower egg weight than the control group from wk 5 to 8 (P = 0.008). For the wk 1 to 8 period, egg weight of MB1, DY5, and XH3 rapeseed were significantly lower than the control group (P = 0.007). For egg mass, MB1, DY5, and XH3 rapeseed were significantly lower than the control group from wk 1 to 4 (P = 0.005). From wk 5 to 8, four kinds of rapeseed had a lower egg mass than the control group (P = 0.006), and egg mass of XH3 rapeseed was lower than that of DY6 rapeseed. For the wk 1 to 8 period, 11.5% rapeseed reduced the egg mass, and egg mass in XH3 and DY5 rapeseed were lower than that in DY6 rapeseed (P = 0.004). From wk 1 to 4, there was no difference in FCR between each group (P = 0.100). From wk 5 to 8 and wk 1 to 8, 11.5% rapeseed had a higher FCR than the control group (P = 0.009), and FCR in XH3 rapeseed was higher than that in DY6 rapeseed (P = 0.008).
Table 4.
Effects of different rapeseed varieties on egg production in laying hens.1
| Item | Treatment |
SEM | P-value | ||||
|---|---|---|---|---|---|---|---|
| Control | DY6 | MB1 | DY5 | XH3 | |||
| ADFI, g/d per bird | |||||||
| 1–4 wk | 110.50a | 105.76b | 105.97b | 103.34bc | 101.99c | 0.721 | 0.003 |
| 5–8 wk | 105.30a | 99.83b | 99.07b | 99.07b | 99.79b | 0.571 | 0.001 |
| 1–8 wk | 107.90a | 102.79b | 102.52b | 101.20b | 100.88b | 0.483 | 0.002 |
| Egg-laying rate, % | |||||||
| 1–4 wk | 91.67a | 88.21ab | 86.31bc | 83.57bc | 83.24c | 1.195 | 0.004 |
| 5–8 wk | 88.48a | 78.09b | 74.06bc | 75.43bc | 70.77c | 1.642 | 0.003 |
| 1–8 wk | 90.07a | 83.15b | 80.19bc | 79.50bc | 77.01c | 1.074 | 0.006 |
| Egg weight, g/d per bird | |||||||
| 1–4 wk | 60.10a | 59.05ab | 58.82ab | 58.63b | 58.91ab | 0.337 | 0.030 |
| 5–8 wk | 60.94a | 59.73ab | 58.67b | 58.47b | 58.98b | 0.431 | 0.008 |
| 1–8 wk | 60.52a | 59.39ab | 58.74b | 58.55b | 58.94b | 0.358 | 0.007 |
| Egg mass, g/d per bird | |||||||
| 1–4 wk | 55.11a | 52.10ab | 50.79b | 49.03b | 49.08b | 0.783 | 0.005 |
| 5–8 wk | 53.94a | 46.63b | 43.47bc | 44.08bc | 41.74c | 0.910 | 0.006 |
| 1–8 wk | 54.52a | 49.37b | 47.13bc | 46.55c | 45.41c | 0.639 | 0.004 |
| FCR | |||||||
| 1–4 wk | 2.01 | 2.04 | 2.09 | 2.12 | 2.09 | 0.032 | 0.100 |
| 5–8 wk | 1.96c | 2.15b | 2.31ab | 2.26ab | 2.41a | 0.051 | 0.009 |
| 1–8 wk | 1.99c | 2.09bc | 2.20ab | 2.19ab | 2.25a | 0.033 | 0.008 |
ADFI = average daily feed intake; FCR = feed conversion ratio; DY5 = Deyou no. 5 rapeseed; DY6 = Deyou no. 6 rapeseed; MB1 = Mianbangyou no. 1 rapeseed; XH3 = Xiheyou no. 3 rapeseed.
Means with different superscripts in the same row differ significantly (P < 0.05).
Data are expressed as mean and SEM.
Table 5.
Effects of different rapeseed varieties on egg production during elimination phase (9–12 wk of the trial).1
| Item | Treatment |
SEM | P-value | ||||
|---|---|---|---|---|---|---|---|
| Control | DY6 | MB1 | DY5 | XH3 | |||
| ADFI, g/d per bird | 103.72 | 101.04 | 101.47 | 101.38 | 101.99 | 0.800 | 0.191 |
| Egg-laying rate, % | 87.37 | 82.63 | 82.57 | 86.07 | 82.15 | 1.661 | 0.152 |
| Egg weight, g/d per bird | 62.07a | 61.44ab | 59.81b | 59.75b | 60.62ab | 0.465 | 0.011 |
| Egg mass, g/d per bird | 54.21a | 50.74ab | 49.38b | 51.43ab | 49.78b | 0.963 | 0.033 |
| FCR | 1.91b | 1.99ab | 2.07a | 1.98ab | 2.06a | 0.032 | 0.024 |
ADFI = average daily feed intake; FCR = feed conversion ratio; DY5 = Deyou no. 5 rapeseed; DY6 = Deyou no. 6 rapeseed; MB1 = Mianbangyou no. 1 rapeseed; XH3 = Xiheyou no. 3 rapeseed.
Means with different superscripts in the same row differ significantly (P < 0.05).
Data are expressed as mean and SEM.
After 4 weeks withdrawal of rapeseed, the ADFI and egg-laying rate had recovered in the rapeseed groups, and there was no difference between each group (P = 0.191, P = 0.152, respectively). But the egg weight, egg mass, and FCR did not recover. DY5 and MB1 rapeseed had a lower egg weight than the control group (P = 0.011). XH3 and MB1 rapeseed had a lower egg mass than the control group (P = 0.033). XH3 and MB1 rapeseed had a higher FCR than the control group (P = 0.024).
3.3. Egg quality
The effects of rapeseed on eggshell and egg internal quality are shown in Table 6, Table 7, Table 8. DY5 rapeseed had a lower L∗ than MB1 rapeseed at wk 2 (P = 0.009). At wk 4, The value of L∗ significantly decreased with the increase of antinutritional factors in rapeseed, and L∗ of DY6 rapeseed was significantly higher than that of XH3 rapeseed (P = 0.023). At wk 8, L∗ of XH3 rapeseed was significantly lower than the control and DY5 rapeseed (P = 0.012). XH3 rapeseed had a higher a∗ value than the control and MB1 and DY5 rapeseed (P = 0.008). There was no difference in b∗ between each group at wk 2, 4, 6, and 8 (P = 0.524, P = 0.714, P = 0.592, P = 0.642). For the eggshell strength, MB1 rapeseed tended to be higher than DY6 rapeseed at wk 8 (P = 0.053), at the same time, eggshell thickness of DY6 rapeseed was lower than other groups (P = 0.009). Albumen height of XH3 rapeseed was lower than the control group at wk 2 (P = 0.022). MB1, DY5, and XH3 rapeseed had a lower albumen height than the control group at wk 4 (P = 0.009). Albumen height of DY5 rapeseed was lower than the control group at wk 8 (P = 0.012). Yolk color was increased by 11.5% rapeseed before wk 6 (P = 0.005, P = 0.003, P = 0.004), and XH3 had a higher yolk color than other rapeseed groups. But there was no difference in yolk color between each treatment at wk 8 (P = 0.122). Mianbangyou no. 1 and DY5 rapeseed decreased Haugh unit at wk 4 and 8 (P = 0.011, P = 0.024).
Table 6.
Effects of different varieties of rapeseed on eggshell color of laying hens.1
| Item | Treatment |
SEM | P-value | ||||
|---|---|---|---|---|---|---|---|
| Control | DY6 | MB1 | DY5 | XH3 | |||
| L∗ | |||||||
| 2 wk | 72.55ab | 72.55ab | 75.19a | 71.86b | 74.25ab | 0.721 | 0.009 |
| 4 wk | 76.58a | 76.20ab | 74.62bc | 74.61bc | 74.42c | 0.593 | 0.023 |
| 6 wk | 73.9 | 75.04 | 74.08 | 73.9 | 74.24 | 0.572 | 0.601 |
| 8 wk | 74.95a | 74.75ab | 74.55ab | 75.12a | 72.92b | 0.474 | 0.012 |
| a∗ | |||||||
| 2 wk | 4.93 | 5.04 | 4.98 | 5.49 | 5.12 | 0.200 | 0.271 |
| 4 wk | 4.56 | 4.96 | 5.34 | 5.1 | 5.41 | 0.261 | 0.153 |
| 6 wk | 5.28 | 4.68 | 4.93 | 5.03 | 5.23 | 0.252 | 0.441 |
| 8 wk | 4.67b | 5.05ab | 4.88b | 4.68b | 5.80a | 0.221 | 0.008 |
| b∗ | |||||||
| 2 wk | 15.44 | 15.53 | 15.28 | 15.93 | 15.24 | 0.302 | 0.524 |
| 4 wk | 15.68 | 15.78 | 16.31 | 15.94 | 15.86 | 0.334 | 0.714 |
| 6 wk | 15.95 | 15.57 | 15.24 | 15.61 | 15.86 | 0.331 | 0.592 |
| 8 wk | 15.19 | 14.86 | 15.10 | 14.74 | 15.53 | 0.391 | 0.642 |
L∗ = lightness; a∗ = redness; b∗ = yellowness; DY5 = Deyou no. 5 rapeseed; DY6 = Deyou no. 6 rapeseed; MB1 = Mianbangyou no. 1 rapeseed; XH3 = Xiheyou no. 3 rapeseed.
Means with different superscripts in the same row differ significantly (P < 0.05).
Data are expressed as mean and SEM.
Table 7.
Effects of different varieties of rapeseed on eggshell quality of laying hens.1
| Item | Treatment |
SEM | P-value | ||||
|---|---|---|---|---|---|---|---|
| Control | DY6 | MB1 | DY5 | XH3 | |||
| Eggshell strength, kg/cm2 | |||||||
| 2 wk | 3.59 | 3.34 | 3.36 | 3.59 | 3.61 | 0.112 | 0.230 |
| 4 wk | 5.44 | 5.19 | 5.12 | 5.58 | 5.41 | 0.214 | 0.501 |
| 6 wk | 5.26 | 5.14 | 5.35 | 5.47 | 5.05 | 0.221 | 0.682 |
| 8 wk | 4.84 | 4.54 | 5.36 | 5.11 | 5.15 | 0.203 | 0.053 |
| Eggshell thickness, mm | |||||||
| 2 wk | 0.39 | 0.38 | 0.38 | 0.39 | 0.38 | 0.006 | 0.414 |
| 4 wk | 0.35 | 0.35 | 0.33 | 0.35 | 0.35 | 0.006 | 0.192 |
| 6 wk | 0.35 | 0.33 | 0.34 | 0.34 | 0.34 | 0.006 | 0.231 |
| 8 wk | 0.34a | 0.32b | 0.34a | 0.34a | 0.34a | 0.004 | 0.009 |
DY5 = Deyou no. 5 rapeseed; DY6 = Deyou no. 6 rapeseed; MB1 = Mianbangyou no. 1 rapeseed; XH3 = Xiheyou no. 3 rapeseed.
Means with different superscripts in the same row differ significantly (P < 0.05).
Data are expressed as mean and SEM.
Table 8.
Effects of different varieties of rapeseed on egg internal quality of laying hens.1
| Item | Treatment |
SEM | P-value | ||||
|---|---|---|---|---|---|---|---|
| Control | DY6 | MB1 | DY5 | XH3 | |||
| Albumen height, mm | |||||||
| 2 wk | 8.63a | 8.17ab | 8.22ab | 8.27ab | 7.92b | 0.142 | 0.022 |
| 4 wk | 9.11a | 8.46ab | 8.12b | 8.26b | 8.32b | 0.171 | 0.009 |
| 6 wk | 8.40ab | 8.76a | 8.09ab | 8.43ab | 7.84b | 0.193 | 0.011 |
| 8 wk | 8.39a | 8.11ab | 8.09ab | 7.51b | 7.87ab | 0.186 | 0.012 |
| Yolk color | |||||||
| 2 wk | 7.61b | 8.65a | 8.77a | 8.83a | 8.93a | 0.201 | 0.005 |
| 4 wk | 7.65b | 8.50a | 8.68a | 8.93a | 8.69a | 0.142 | 0.003 |
| 6 wk | 7.53b | 7.68b | 7.72b | 7.68b | 8.38a | 0.144 | 0.004 |
| 8 wk | 7.30 | 7.19 | 7.45 | 7.40 | 7.79 | 0.163 | 0.122 |
| Haugh unit | |||||||
| 2 wk | 91.58 | 90.24 | 90.01 | 90.49 | 89.26 | 0.791 | 0.343 |
| 4 wk | 95.02a | 91.93ab | 90.40b | 91.35ab | 91.65ab | 0.962 | 0.011 |
| 6 wk | 91.69ab | 93.51a | 90.98ab | 91.95ab | 88.46b | 1.076 | 0.023 |
| 8 wk | 90.74a | 89.40ab | 90.23a | 86.30b | 89.43ab | 0.997 | 0.024 |
DY5 = Deyou no. 5 rapeseed; DY6 = Deyou no. 6 rapeseed; MB1 = Mianbangyou no. 1 rapeseed; XH3 = Xiheyou no. 3 rapeseed.
Means with different superscripts in the same row differ significantly (P < 0.05).
Data are expressed as mean and SEM.
3.4. Serum biochemical indices
The effects of different varieties on serum organ function parameters of laying hens are shown in Table 9. There was no significant difference in serum ALT, CREA, UREA, T3, T4, and T3/T4 (P > 0.05), but XH3 rapeseed tended to increase serum AST content (P = 0.091). Adding 11.5% rapeseed to diets significantly decreased serum E2 content (P = 0.003), and there was no difference between rapeseed variety (P > 0.05). Adding 11.5% rapeseed to diets tended to decrease serum P4 content (P = 0.062).
Table 9.
Effects of different varieties of rapeseed on serum organ function parameters of laying hens (wk 8 of the trial).1
| Item | Treatment |
SEM | P-value | ||||
|---|---|---|---|---|---|---|---|
| Control | DY6 | MB1 | DY5 | XH3 | |||
| ALT, U/L | 5.96 | 5.83 | 5.87 | 3.93 | 5.19 | 0.633 | 0.141 |
| AST, U/L | 161.87 | 165.47 | 161.03 | 169.68 | 196.91 | 10.061 | 0.091 |
| CREA, μmol/L | 48.17 | 62.06 | 57.62 | 70.72 | 73.20 | 9.423 | 0.352 |
| Urea, μmol/L | 0.46 | 0.57 | 0.51 | 0.48 | 0.48 | 0.043 | 0.253 |
| T3, ng/dL | 52.85 | 61.12 | 70.93 | 64.64 | 68.58 | 6.182 | 0.284 |
| T4, ng/L | 1013.72 | 810.66 | 1196.71 | 774.63 | 939.60 | 133.671 | 0.192 |
| T3/T4 | 0.062 | 0.088 | 0.069 | 0.093 | 0.081 | 0.0144 | 0.301 |
| E2, ng/L | 61.15a | 30.59b | 34.00b | 31.34b | 17.84b | 4.286 | 0.003 |
| P4, μg/L | 1685.25 | 1145.11 | 1728.8 | 1416.58 | 1827.75 | 171.336 | 0.062 |
ALT = alanine aminotransferase; AST = aspartate aminotransferase; CREA = creatinine; T3 = triiodothyronine; T4 = tetraiodothyronine; E2 = estradiol; P4 = progesterone; DY5 = Deyou no. 5 rapeseed; DY6 = Deyou no. 6 rapeseed; MB1 = Mianbangyou no. 1 rapeseed; XH3 = Xiheyou no. 3 rapeseed.
Means with different superscripts in the same row differ significantly (P < 0.05).
Data are expressed as mean and SEM.
3.5. Organ index and follicle number
The effects of different variety on organ index and follicle number of laying hens are shown in Table 10. Thyroid index increased as the Gls and EA content increased, and DY5 and XH3 rapeseed had a higher thyroid index than the control group, and there were differences between rapeseed varieties (XH3 > DY6/MB1, P = 0.008). There was no difference in liver index between each group (P = 0.412). DY5 rapeseed had a higher kidney index than DY6 rapeseed (P = 0.034). Adding 11.5% rapeseed in diets decreased follicle number, although there was no difference in SYF, LWT, SWF, and total follicles (P > 0.05), but total follicle number of the XH3 rapeseed group was 6% lower than that of the control group, meanwhile, the number of F6 that could develop into egg yolk of XH3 and MB1 rapeseed was lower than that of the control group (P = 0.009).
Table 10.
Effects of different varieties of rapeseed on organ index and follicle number of laying hens (wk 8 of the trial).1
| Item | Treatment |
SEM | P-value | ||||
|---|---|---|---|---|---|---|---|
| Control | DY6 | MB1 | DY5 | XH3 | |||
| Thyroid index, × 10−5 | 12.50c | 13.00bc | 15.00bc | 19.90ab | 23.30a | 1.703 | 0.008 |
| Liver index, % | 2.04 | 1.93 | 1.83 | 2.00 | 1.86 | 0.094 | 0.412 |
| Kidney index, % | 0.77ab | 0.72b | 0.75ab | 0.86a | 0.83ab | 0.032 | 0.034 |
| F6 | 5a | 4ab | 3b | 4ab | 3b | 0.4 | 0.009 |
| SYF | 5 | 5 | 3 | 4 | 2 | 1.2 | 0.343 |
| LWF | 15 | 11 | 14 | 15 | 11 | 2.2 | 0.612 |
| SWF | 25 | 30 | 29 | 31 | 29 | 3.1 | 0.543 |
| Total follicles | 50 | 50 | 52 | 54 | 47 | 4.2 | 0.812 |
F6 = the smallest hierarchical follicle; SYF = small white follicles; LWF = large white follicles; SWF = small yellow follicles; DY5 = Deyou no. 5 rapeseed; DY6 = Deyou no. 6 rapeseed; MB1 = Mianbangyou no. 1 rapeseed; XH3 = Xiheyou no. 3 rapeseed.
Means with different superscripts in the same row differ significantly (P < 0.05).
Data are expressed as mean and SEM.
4. Discussion
The nutrient profile of rapeseed makes it an ideal ingredient for high nutrient density diets, and it is also a good source of unsaturated fatty acids for poultry products (Drażbo et al., 2019; Du et al., 2017). Research on the use of rapeseed in poultry was mostly published in the 1970s, and very little research has been done in laying hens and the results are inconsistent. Egg production, particularly at the highest level of inclusion of 15% rapeseed was adversely affected as reported by Leslie and Summers (1972), but according to Olomu et al. (1975), 15% span rapeseed did not affect production performance in hens. In our present study, 11.5% rapeseed significantly decreased feed intake, egg mass, feed conversion efficiency, and F6 follicle number, and rapeseed with high Gls and EA content had a lower production performance than rapeseed with low Gls and EA content. As all we know, antinutritional factors such as Gls, sinapine, and their derivatives, tannins, phytic acid, and crude fiber have an adverse effect on animals (Yadav et al., 2022). Because the egg production performance was different between different kinds of rapeseed in this study, we postulated that the inconsistencies between the various studies might be due to the different antinutritional factor content in rapeseed varieties.
In the current study, during the last 4 wk (9–12 wk) for recovery, there was no difference in ADFI and egg laying-rate, but egg weight, egg mass, and feed conversion efficiency of rapeseed were still lower than that of the control group. Some studies have found that the level of antinutritional factors in the blood return to normal following withdrawal of rapeseed supplementation, facilitating a recovery in production performance (Mena et al., 2004; Zeng et al., 2014). Our previous study also showed that the egg production performance, some serum parameters, and organ weight recovered after 4 wk withdrawal of 29.4% rapeseed meal (Zhu et al., 2018). In this study, 4 wk withdrawal of 11.5% rapeseed did not help to recover egg weight and FCR. This might indicate that the organs of laying hens in this study were irreversibly damaged and need additional nutrients to for repair, or that it will take a longer time for egg performance to recover.
Egg quality ss a crucial factor affecting the economic benefits of the poultry industry. Eggshell color affects consumer preference (Samiullah et al., 2015), and research shows that preferences for eggshell color and yolk color vary by geographic region, with darker colors preferred in Northeast China (Chen et al., 2023). In present study, the 11.5% rapeseed diet increased a∗ value of eggshell and decreased L∗ value. This result showed that the eggshell color was darker and redder after feeding rapeseed. Research has indicated that feed source affects eggshell color (Mori et al., 2020) and that the pigmentation derived from rapeseed might induce darker and redder eggshell color for eggs. Although the eggshell thickness of DY6 was a little lower than the control and other rapeseed variety groups, there was no difference in eggshell strength. Interestingly, all rapeseed groups had a higher yolk color before six weeks, but there was no difference in wk 8 among groups. The darker color of egg yolk might be caused by pigments in rapeseed itself, but as the experimental time increased, the digestion and absorption of nutrients might have been affected by high EA content in the diet, so the egg yolk color decreased. This was in line with a previous study, in which Yuan et al. (2019) indicated that high EA rapeseed oil decreased yolk color. The lower albumen height and Haugh unit in the rapeseed groups might be caused by the reduced dry matter digestibility induced by the high content of Gls, EA, or crude fiber in rapeseed (Zhu et al., 2019).
Blood biochemical indices are often used to reflect changes in metabolism and organ function (Zhang et al., 2021). Thyroid hormone regulates metabolic processes essential for normal growth and development (Mullur et al., 2014). It is well established that thyroid hormone status correlates with growth and energy expenditure (Mullur et al., 2014). Gls metabolites impair the thyroid uptake of iodide, its oxidation, iodine binding to thyroglobulin, synthesis, and the release of hormones, which then cause thyroid hyperplasia and goiter (Schöne et al., 1993). In this study, T4 content in serum of high Gls and EA rapeseed was a little lower than the control group, and the thyroid index increased gradually with the increase in Gls content. This was in line with a previous study in which Gls linearly increased thyroid index (Zhu et al., 2018). The rapeseed diets decreased serum E2 content, and this was in line with previous research (Mandiki et al., 2002). Gls metabolites have been proven to act as antiestrogens, blocking estradiol-induced cell proliferation (Ju et al., 2000). This might affect ovarian function, which in turn affects hormone production. Because estrogen regulates follicle development (Fortune 1994), this was the reason why the F6 number and egg laying rate decreased.
5. Conclusion
In summary, regardless of the level of Gls and EA content in rapeseed in the present study, Gls and EA were found to have an adverse effect on egg production performance. There was a difference in egg production performance between rapeseed varieties, and egg laying rate and feed conversion efficiency of high Gls and EA content rapeseed were lower than that of low Gls and EA content rapeseed. Although a rapeseed diet resulted in darker eggshell color, it could decrease internal egg quality as indicated by albumen height and Haugh unit. The negative effects of rapeseed in the diet might be due to its impact on hormone levels, follicle development, and thyroid function. A 4-wk withdrawal period of 11.5% rapeseed was not effective in recovering the egg weight and FCR. It is therefore recommended that when raw and whole rapeseed is used as a feed material for laying hens, the addition amount should not be too high, and rapeseed with a low content of antinutritional factors should be used.
CRediT authorship contribution statement
Liping Zhu: Conceptualization, Investigation, Methodology, Formal analysis, Writing – original draft. Jianping Wang: Conceptualization, Formal analysis, Writing – original draft. Xuemei Ding: Conceptualization, Data curation, Methodology. Shiping Bai: Conceptualization, Data curation, Methodology. Qiufeng Zeng: Conceptualization, Data curation. Yue Xuan: Investigation. Keying Zhang: Conceptualization, Data curation, Investigation, Formal analysis, Resources, Project administration, Writing – review & editing.
Declaration of competing interest
We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, and there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the content of this paper.
Acknowledgments
This project was supported by National Science and Technology Project (2014BAD13B04), the earmarked fund for Modern Agro-Industry Technology Research System and Sichuan Provincial Science and Technology Project (2014NZ0043, 2014NZ0002).
Footnotes
Peer review under the responsibility of Chinese Association of Animal Science and Veterinary Medicine.
References
- Ajuyah A.O., Hardin R.T., Sim J.S. Studies on canola seed in Turkey grower diet: effects on ω-3 fatty acid composition of breast meat, breast skin and selected organs. Can J Anim Sci. 1993;73(1):177–181. [Google Scholar]
- China Feed Database . 2014. Tables of feed composition and nutritive values in China.https://www.chinafeeddata.org.cn/admin/Login/slcfb (in Chinese) [Google Scholar]
- China National Standard . Standards Press of China; Beijing, China: 2006. Determination of crude fat in feeds (GB/T 6433-2006) [Google Scholar]
- China National Standard . Standards Press of China; Beijing, China: 2018. Determination of moisture in feedstuffs (GB/T 6435-2018) [Google Scholar]
- China National Standard . Standards Press of China; Beijing, China: 2008. Determination of the content of fatty acids in feeds (GB/T 21514-2008) [Google Scholar]
- China National Standard . Standards Press of China; Beijing, China: 2009. Determination of total nitrogen content in animal feeding stuffs by combustion according to the Dumas principle and calculation of the crude protein content (GB/T 24318-2009) [Google Scholar]
- China National Standard . Standards Press of China; Beijing, China: 2022. Feeding stuffs-Determination of crude fiber content (GB/T 6434-2022) [Google Scholar]
- Chen R., Jiang C., Li X., Shi X., Zhuang L., Zhou W., et al. Research on Chinese consumers' shell egg consumption preferences and the egg quality of functional eggs. Poultry Sci. 2023;102(10) doi: 10.1016/j.psj.2023.103007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chmielewska A., Kozowska M., Rachwa D., Wnukowski P., Rosicka-Kaczmarek J. Canola/rapeseed protein–nutritional value, functionality and food application: a review. Crit Rev Food Sci. 2021;61(22):3836–3856. doi: 10.1080/10408398.2020.1809342. [DOI] [PubMed] [Google Scholar]
- Drażbo A., Kozłowski K., Ognik K., Zaworska A., Jankowski J. The effect of raw and fermented rapeseed cake on growth performance, carcass traits, and breast meat quality in Turkey. Poultry Sci. 2019;98(11):6161–6169. doi: 10.3382/ps/pez322. [DOI] [PubMed] [Google Scholar]
- Du X., Liu Y., Lu L., Wang W., Zeng T., Tian Y., et al. Effects of dietary fats on egg quality and lipid parameters in serum and yolks of Shan Partridge Duck. Poultry Sci. 2017;96(5):1184–1190. doi: 10.3382/ps/pew348. [DOI] [PubMed] [Google Scholar]
- FAO (Food and Agriculture Organization) FAOSTAT data: rape or colza seed. https://www.fao.org/faostat/zh/#data/QCL
- Fortune J. Ovarian follicular growth and development in mammals. Biol Reprod. 1994;50(2):225–232. doi: 10.1095/biolreprod50.2.225. [DOI] [PubMed] [Google Scholar]
- ISO (International Organization for Standardization) International Organization for Standardization; Geneva, Switzerland: 1998. Animal feeding stuffs, animal products, and Faeces or urine-determination of gross calorific value: bomb calorimeter method, standard 9831. [Google Scholar]
- Ju Y.H., Carlson K.E., Sun J., Pathak D., Katzenellenbogen B.S., Katzenellenbogen J.A., et al. Estrogenic effects of extracts from cabbage, fermented cabbage, and acidified brussels sprouts on growth and gene expression of estrogen-dependent human breast cancer (MCF-7) cells. J Agric Food Chem. 2000;48(10):4628–4634. doi: 10.1021/jf000164z. [DOI] [PubMed] [Google Scholar]
- Leslie A.J., Summers J.D. Therapy. Feeding value of rapeseed for laying hens. Pharmacotherapy. 1972;52(3):563–566. [Google Scholar]
- Li S., Vestergren A.S., Wall H., Trattner S., Pickova J., Ivarsson E. Feeding steam-pelleted rapeseed affects expression of genes involved in hepatic lipid metabolism and fatty acid composition of chicken meat. Poultry Sci. 2017;96(8):2965–2974. doi: 10.3382/ps/pex047. [DOI] [PubMed] [Google Scholar]
- Lichovnikova M., Zeman L. The effects of a higher amount of iodine supplement on the efficiency of laying hens fed extruded rapeseed and on eggshell quality. Czech J Anim Sci. 2004;49(5):199–203. [Google Scholar]
- Mandiki S.N.M., Derycke G., Bister J.A., Mabon N., Wathelet J.P., Marlier M., et al. Chemical changes and influences of rapeseed antinutritional factors on gestating and lactating ewes: 1. Animal performances and plasma hormones and glucose. Anim Feed Sci Technol. 2002;98(1–2):25–35. [Google Scholar]
- Mena H., Santos J.E.P., Huber J.T., Tarazon M., Calhoun M.C. The effects of varying gossypol intake from whole cottonseed and cottonseed meal on lactation and blood parameters in lactating dairy cows. J Dairy Sci. 2004;87(8):2506–2518. doi: 10.3168/jds.S0022-0302(04)73375-5. [DOI] [PubMed] [Google Scholar]
- Ministry of Agriculture of the People’s Republic of China . China Agriculture Press; Beijing, China: 2007. Rapeseed. Determination of glucosinolates content. Method using high-performance liquid chromatography (NY/T 1582-2007) [Google Scholar]
- Ministry of Agriculture of the People’s Republic of China . Thiourea colorimetry method (NY/T 1596-2008) China Agriculture Press; Beijing, China: 2008. Determination of isothiocyanates in rapeseed meal. [Google Scholar]
- Ministry of Agriculture of the People’s Republic of China . China Agriculture Press; Beijing, China: 2009. Determination of oxazolidinethione in rapeseed meal and feed Spectrometric method (NY/T 1799-2009) [Google Scholar]
- Mori H., Takaya M., Nishimura K., Goto T. Breed and feed affect amino acid contents of egg yolk and eggshell color in chickens. Poultry Sci. 2020;99(1):172–178. doi: 10.3382/ps/pez557. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mullur R., Liu Y.Y., Brent G.A. Thyroid hormone regulation of metabolism. Physiol Rev. 2014;2 doi: 10.1152/physrev.00030.2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Najib H., Al-Khateeb S.A. The effect of incorporating different levels of locally produced canola seeds (Brassica napus, L.) in the diet of laying hen. Int J Poultry Sci. 2004;3(7):490–496. [Google Scholar]
- NRC . 9th ed. National Academy Press; Washington (DC): 1994. Nutrition requirements of poultry. [Google Scholar]
- Olomu J.M., Robblee A.R., Clandinin D.R., Hardin R.T. Evaluation of full-fat Span rapeseed as an energy and protein source for laying hens. Can J Anim Sci. 1975;55(2):219–222. [Google Scholar]
- Samiullah S., Roberts J.R., Chousalkar K. Eggshell color in brown-egg laying hens-a review. Poultry Sci. 2015;94(10):2566–2575. doi: 10.3382/ps/pev202. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schöne F., Jahreis G., Richter G., Lange R. Evaluation of rapeseed meals in broiler chicks: effect of iodine supply and glucosinolate degradation by myrosinase or copper. J Sci Food Agric. 1993;61(2):245–252. [Google Scholar]
- Yadav S., Teng P.Y., Choi J., Singh A.K., Vaddu S., Thippareddi H., et al. Influence of rapeseed, canola meal and glucosinolate metabolite (AITC) as potential antimicrobials: effects on growth performance, and gut health in Salmonella Typhimurium challenged broiler chickens. Poultry Sci. 2022;101(1) doi: 10.1016/j.psj.2021.101551. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yuan N., Wang J.P., Ding X.M., Bai S.P., Zeng Q.F., Su Z.W., et al. Effects of supplementation with different rapeseed oil sources and levels on production performance, egg quality, and serum parameters in laying hens. Poultry Sci. 2019;98(4):1697–1705. doi: 10.3382/ps/pey494. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zeng Q.F., Yang G.L., Liu G.N., Wang J.P., Bai S.P., Ding X.M., et al. Effects of dietary gossypol concentration on growth performance, blood profiles, and hepatic histopathology in meat ducks. Poultry Sci. 2014;93(8):2000–2009. doi: 10.3382/ps.2013-03841. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang Q., Zhang S., Cong G., Zhang Y., Madsen M.H., Tan B., et al. Effects of soy protein concentrate in starter phase diet on growth performance, blood biochemical indices, carcass traits, immune organ indices and meat quality of broilers. Animals. 2021;11(2):281. doi: 10.3390/ani11020281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu L.P., Wang J.P., Ding X.M., Bai S.P., Zeng Q.F., Su Z.W., et al. The effects of varieties and levels of rapeseed expeller cake on egg production performance, egg quality, nutrient digestibility, and duodenum morphology in laying hens. Poultry Sci. 2019;98(10):4942–4953. doi: 10.3382/ps/pez254. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu L.P., Wang J.P., Ding X.M., Bai S.P., Zeng Q.F., Su Z.W., et al. The deposition and elimination of glucosinolate metabolites derived from rapeseed meal in eggs of laying hens. J Agric Food Chem. 2018;66(6):1560–1568. doi: 10.1021/acs.jafc.7b05782. [DOI] [PubMed] [Google Scholar]