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. 2021 Feb 23;7(4):1347–1358. doi: 10.1002/vms3.450

Effects of supplementing sow diets during late gestation with Pennisetum purpureum on antioxidant indices, immune parameters and faecal microbiota

Peng‐Fei Huang 1,✉, Qi Mou 1, Ying Yang 1, Jia‐Ming Li 1, Ming‐Lang Xu 1, Jing Huang 1, Jian‐Zhong Li 1, Huan‐Sheng Yang 1,✉, Xiao‐Xiao Liang 2, Yu‐Long Yin 1,2
PMCID: PMC8294372  PMID: 33620158

Abstract

The purpose of this study was to investigate the effects of adding Pennisetum purpureum (P. purpureum, also known as Napier grass or elephant grass) to the diets of late gestation on the antioxidant indexes, immune indexes and faecal microbiota of sows. At the 90 days of gestation, 300 healthy sows were randomly divided into three groups, and they received the basic commercial diet or added 5% P. purpureum and 10% P. purpureum, respectively. The experiment started from 90 days of gestation to parturition. The results showed that the total antioxidant capacity, immunoglobulins and serum equol concentrations of sows on 100 days of gestation and at parturition increased linearly (p < .05) with the increase of the content of P. purpureum in the gestation diet. The 5% P. purpureum increased the relative abundance of Bacteroidetes (p = .027) and Actinobacteria (p < .001) at phylum level, Coriobacteriaceae (p < .001) at family level and Prevotellaceae_UCG_001 (p = .004) at genus level, and decreased the relative abundance of Escherichia_Shigella (p < .001) at genus level. In summary, this study shows that the additive of P. purpureum can increase the concentration of serum equol, improve the antioxidant capacity and immune function of sow in late gestation. In addition, the additive of 5% P. purpureum in the diet might change the composition of intestinal microbiota of sows, particularly the relative abundance of Coriobacteriaceae (p < .001) increased.

Keywords: antioxidant capacity, fiber, gestation diet, immune function, Napier grass

At the 90 days of gestation, 300 healthy sows were randomly divided into three groups, and they received the basic commercial diet or added 5% P. purpureum and 10% P. purpureum respectively. This study shows that the addition of P. purpureum can increase the concentration of serum equol and improve the antioxidant capacity and immune function of sow in late gestation. In addition, the addition of 5% P. purpureum in the diet can change the composition of intestinal microbiota of sows, particularly the relative abundance of Coriobacteriaceae increased.

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1. INTRODUCTION

Pregnant sows suffer from a variety of physiological stress conditions (Li et al., 2019; Merlot et al., 2019), which can adversely effect on the sow (Hu et al., 2019; Verdon et al., 2016; Wang, Ji, et al., 2018). Recent studies reported that the metabolites of intestinal microbiota can reduce the oxidative stress experienced by sows during pregnancy (Tan et al., 2016; Wang, Hu, et al., 2019; Zhou, Xiong, et al., 2019). Many studies have shown that forage grasses application can affect sows gut microbiota composition and improve sows health (Castagnino et al., 2016; Liu et al., 2016; Martin et al., 2016).

Forage grasses are high‐quality feeds for herbivorous livestock, and they are common supplemental raw materials for proteins and vitamins in various livestock and poultry compound feeds. Adding forage grasses to the diets of livestock and poultry helps to improve the antioxidant capacity, immune function and intestinal microbial balance (Al‐Sagheer et al., 2019; He et al., 2017; Huang et al., 2018; Jiang et al., 2014). Fibre has a positive role in maintaining the intestinal microbiota of pigs (Jha et al., 2010; Knudsen, 2001). Forage grasses is rich in fibre, and adding high fibre forage grasses to the feed can affect the composition of pig intestinal microbiota (Chen et al., 2013; Varel, 1987). Such as alfalfa, many studies have reported that alfalfa is beneficial for the growth of essential bacteria and promote the production of metabolites, and inhibit the proliferation of harmful bacteria (Liu, Wang, et al., 2018; Liu, Yuan, et al., 2018; Mattioli et al., 2019; Zheng et al., 2019). There have been many studies on the effects of adding alfalfa to diets during gestation on sows (Aube et al., 2019; Calvert et al., 1985; Holzgraefe et al., 1985, 1986; Krogh et al., 2017). P. purpureum is fertilizer‐resistant, moisture‐resistant and palatable. Its composition is similar to alfalfa. The planting area is wide, the cost is low, and it has a broad development prospects in feed. However, there are few reports on the effect of adding P. purpureum to diets during pregnancy on sows.

Therefore, we hypothesized for the first time that the appropriate additive of P. purpureum in the diet of sows in late gestation can improve the antioxidant capacity and immune function, as well as alter the composition of the intestinal microbiota. The purpose of this study was to investigate the effects of P. purpureum on the antioxidant index, immune parameters and faecal microbiota of the sows during gestation.

2. MATERIALS AND METHODS

The experimental animals were raised in pig farms in Hubei Province, China. Animal management and sampling procedures have been approved by the Animal Care and Use Committee of the Hunan Normal University (1907017).

2.1. Experimental design and animals

This experiment selected 300 Landrace × Yorkshire mixed sows (parity 2.37 ± 1.22; back fat 14.57 ± 1.46 mm, mean ± SD). At 90 days of gestation, sows were randomly divided into three groups based on back fat and parity, with 100 in each group. Dietary treatment included basic commercial pregnancy diet (control group, 0% P. purpureum; Table 1) or a diet that was supplemented with 5% P. purpureum and 10% P. purpureum from 90 days of gestation to parturition, respectively. The P. purpureum was provided by Changsha Haishang Environmental Technology Co. Ltd. All the sows were restrictively fed with diets from 90 days of gestation to delivery. At 90 to 95 days of gestation, the feed intake was controlled at 2.5 kg; at 95 to 112 days of gestation, feeding to 3.5 kg; 2 days before delivery, the feed was reduced to 2.0 kg. The design of the experiment is presented in Figure 1.

TABLE 1.

Ingredient and nutrient composition of basal commercial and experimental gestation diets

Items C a 5% b 10% c
Ingredient (%)
Corn 59.18 61.44 63.72
Rice bran 10.00 10.00 10.00
Wheat bran 18.02 11.05 4.04
Soybean meal 6.83 6.71 6.61
Pennisetum purpureum — 5.00 10.00
Dicalcium phosphate 1.20 1.22 1.28
Zeolite powder 2.00 2.00 2.00
Calcium carbonate 1.43 1.24 1.02
Salt 0.29 0.29 0.29
Lysine hydrochloride 0.05 0.05 0.04
Premix c 1.00 1.00 1.00
Calculated composition d
GE (Mcal/kg) 2.25 2.21 2.26
SID Lys (%) 0.51 0.52 0.55
SID Met (%) 0.22 0.21 0.22
SID Thr (%) 0.41 0.41 0.41
SID Trp (%) 0.09 0.10 0.09
Ca (%) 0.81 0.83 0.81
STTD phosphorus (%) 0.38 0.38 0.38
Analysed composition
CP (%) 12.50 12.50 12.5
EE (%) 4.55 4.47 4.40
NDF (%) 15.96 16.46 16.93
ADF (%) 5.64 7.12 8.61
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Abbreviations: CF, Crude fiber; CP, Crude protein; EE, ether extract; GE, gross energy;SID, standardized ileal digestible; STTD, standardized total tract digestible.

a

C = control diet group; 5% = 5% P. purpureum diet group; 10% = 10% P. purpureum diet group; NDF = neutral detergent fibre; ADF = acid detergent fiber.

b

P. purpureum contains 19.17% crude protein, 2.37% crude fat and 22.77% crude fiber, and GE = 1.66 Mcal/kg.

c

Provided per kilogram of diet: Cu, 10.0 mg; Fe 100 mg; Mn 30 mg; Zn 60 mg; I 0.6 mg; Se 0.3 mg; Vitamin A 7,500 IU; Vitamin D3 1,500 IU; Vitamin E 30 mg; Vitamin K 2 mg; 2 mg thiamin; 2 mg riboflavin; 2 mg pyridoxine; 0.02 mg cobalamin.

d

Calculated chemical concentrations using values for feed ingredients from National Research Council (NRC 2012).

FIGURE 1.

FIGURE 1

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Experimental design

2.2. Sample collection

2.2.1. Blood samples

At 90 and 100 days of gestation and parturition, fasting blood samples (10 ml) were collected from the veins of the ear marginal veins. All blood samples were collected into vacuum tubes. Samples were immediately placed on ice, then centrifuged at 3,000g for 10 min at room temperature and the serum was stored at −20°C.

2.2.2. Faeces samples

Faecal samples of 10 healthy sows in each treatment group with no disease and diarrhoea were collected in sterile test tubes at 90, 100 and 110 days of gestation and at parturition, the samples were collected for 12 hr from 8:00 to 12:00 for three consecutive days each time. Then immediately stored in liquid nitrogen until it is transferred to the refrigerator at −80°C.

2.3. Sample analysis

2.3.1. Apparent total tract digestibility

The apparent total tract digestibility (ATTD) including gross energy (GE), contents of dry matter (DM), crude protein (CP), ether extract (EE), crude ash (Ash), Ca and total P from the 90 to 96 days of gestation was determined by adding 0.3% chromium oxide to sow feed. On 94 to 96 days of gestation, the uncontaminated faeces were collected continuously from 08:00 to 20:00 in each sow for 12 hr.

2.3.2. Oxidant and antioxidant content

Specific detection kits (Nanjing Institute of Jiancheng Biological Engineering, Nanjing, China) were used to determine the contents of Catalase (CAT), superoxide dismutase (SOD), glutathione peroxidase (GSH‐PX), malondialdehyde (MDA) and total antioxidant capacity (T‐AOC) in the serum of sows (Barbato et al., 2019; Gabai et al., 2019).

2.3.3. Immunogloblins and cytokines

The concentrations of IgA, IgG and IgM in serum were measured by ELISA kit (Beyotime Biotechnology Company, Shanghai, China). For the analytical method, refer to the kit instructions. All samples were tested in triplicates.

2.3.4. Equol content

The equol concentration in serum was measured by an ELISA kit (Nanjing Institute of Jiancheng Biological Engineering, Nanjing, China). For the analytical method, refer to the kit instructions. All samples were tested in triplicates.

2.3.5. Short‐chain fatty acid

Short‐Chain Fatty Acid (SCFAs) including acetic acid, propionic acid and butyric acid in faeces samples were analysed by 7890B gas chromatography (Agilent, Inc.) as described previously (Cao et al., 2019).

2.3.6. Microbial analyses

Using the Qubit dsDNA Assay Kit (Cat. No. Q328520, Life Technologies) based on the manufacturer's protocols, total bacterial DNA was extracted from faeces of sows in the control group (n = 10) and the group with 5% P. purpureum (n = 10) were collected for three consecutive days from the 110 days of gestation, this analysis was conducted using faeces from one period of time. To perform amplicon pyrosequencing on the Illumina MiSeq PE300 platform, DNA samples were sent to OE Biotech Company (Shanghai, China) and amplified using 515F and 806R primers to obtain the V3–V4 hypervariable region of the 16S rRNA gene (Bolger et al., 2014). The splicing sequences were called paired end data (total). Further denoising on the paired end data was performed to obtain the clean tags (Bolger et al., 2014; Reyon et al., 2012). Then chimeric filtering to get high‐quality effective labels (Figure 2a; Caporaso et al., 2010). Using Vsearch software (v2.4.2) for analysis, valid tags with sequence similarity of 97% are classified as operating classification units (OUT; Edgar, 2013; Edgar et al., 2011). The sequence with the most grace in each OUT was screened as a representative sequence. The Silva database (v123) was used to compare the representative sequences to obtain a phylogenetic tree and OTU classification table, which ultimately performed downstream alpha and beta diversity analysis (Qiong et al., 2007).

FIGURE 2.

FIGURE 2

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Tags number, OTUs number and Venn diagrams. (a) Total tags are equivalent to clean tags. Taxon tags refer to the number of tags used to build OTUs. OTUs, operational taxonomic units. (b) CONG, the control group at gestation; PPG, the 5% Pennisetum purpureum group at gestation

2.4. Statistical analysis

Excel 2016 was used to sort out the experimental data, ANOVA software was used to further analyse the data, and GLM program of SPSS 20.0 software was used to design the random block. The results are represented by the mean value, and its standard error or the standard error of the mean value.

when p < .05, it means that there is a significant difference between the data; when .05 ≤ p < .10, it means that there is a trend of difference.

3. RESULTS

3.1. Apparent total tract digestibility

The results in Table 2 showed that the 5% P. purpureum inclusion had no effects on the ATTD of sows during late gestation. However, the 10% P. purpureum treatment significantly reduced (p < .05) the GE, EE, Ca and total P digestibility compared with sows fed the control diet, but DM, CP and ash had no effect.

TABLE 2.

Effect of inclusion of Pennisetum purpureum in gestation diet on ATTD of energy and nutrients of sows*

Item C1 5% 10% SEM p value
GE 81.72a 81.31a 80.45b 0.25 .014
DM 82.23 81.79 81.72 0.31 .191
CP 83.66 83.14 83.77 0.44 .837
EE 56.61a 55.05a 50.99b 1.56 .004
Ash 36.33 36.93 33.74 1.96 .152
Ca 41.26a 41.01a 40.75b 0.17 .001
Total P 35.77a 34.20a 37.62b 1.52 .018
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Different letters in the same line indicate significant statistical differences (p < .05).

C = control diet group; 5% = 5% P. purpureum diet group; 10% = 10% P. purpureum diet group. Values were considered statistically significant when p < .05 and as a trend to significance when .05 ≤ p < .10.

*

Values are standard error of the mean (SEM).

3.2. Serum immunoglobulins concentrations

The serum IgA and IgM concentrations of sows increased linearly (p < .05) with the increase of P. purpureum at 100 days of gestation and at parturition. The serum IgG concentrations of sows increased linearly (p < .05) with the increase of P. purpureum at 100 days of gestation (Table 3).

TABLE 3.

Effect of Pennisetum purpureum additive in late gestation on serum immunoglobulin concentrations of sows*

Item P. purpureum, % of diet p value
0 5 10 Con versus P. purpureum Linear Quadratic
90 days, μg/ml
IgA 65.34 ± 4.78 65.99 ± 6.63 70.34 ± 7.54 .186 .093 .463
IgG 419.93 ± 31.62 414.43 ± 20.87 411.39 ± 20.39 .740 .449 .899
IgM 80.79 ± 9.21 75.15 ± 5.46 76.59 ± 6.20 .206 .200 .213
100 days, μg/ml
IgA 101.18 ± 8.26 111.61 ± 12.90 112.95 ± 9.77 .036 .018 .272
IgG 461.29 ± 25.59 478.30 ± 36.80 502.78 ± 22.41 .012 .003 .741
IgM 146.79 ± 8.91 156.97 ± 8.75 161.69 ± 14.34 .016 .005 .526
At parturition, μg/ml
IgA 136.10 ± 15.40 142.34 ± 13.33 149.38 ± 11.99 .113 .039 .939
IgG 809.47 ± 30.89 803.28 ± 38.22 820.47 ± 41.33 .583 .513 .423
IgM 175.99 ± 19.26 179.71 ± 8.53 188.47 ± 11.88 .141 .056 .645
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Values were considered statistically significant when p < .05 and as a trend to significance when .05 ≤ p < .10.

*

Values are means ± SE, n = 10 per treatment.

3.3. Oxidative and antioxidative indicators in the serum

The serum MDA concentrations of sows decreased linearly and quadratically (p < .05) with the increase of P. purpureum at 100 days of gestation and at parturition (Table 4). The serum T‐AOC concentrations of sows increased linearly (p < .05) with the increase of P. purpureum at 100 days of gestation and at parturition. The serum total superoxide dismutase (T‐SOD) and CAT concentrations of sows increased linearly (p < .05) with the increase of P. purpureum at 100 days of gestation and at parturition, The serum GSH‐PX concentration of sows has no effect with the increase of P. purpureum at 100 days of gestation and at parturition (Table 5).

TABLE 4.

Effect of Pennisetum purpureum additive in late gestation on serum MDA concentrations of sows*

Item P. purpureum, % of diet p value
0 5 10 Con versus P. purpureum Linear Quadratic
90 days, nmol/ml 2.75 ± 0.21 2.82 ± 0.23 2.60 ± 0.29 .122 .223 .094
100 days, nmol/ml 5.53 ± 0.67 2.60 ± 0.26 1.62 ± 0.17 <.001 <.001 <.001
At parturition, nmol/ml 7.48 ± 0.67 6.50 ± 0.55 4.23 ± 0.32 <.001 <.001 .013
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Values were considered statistically significant when p < .05 and as a trend to significance when .05 ≤ p < .10.

*

Values are means ± SE, n = 10 per treatment.

TABLE 5.

Effect of Pennisetum purpureum additive in late gestation on serum antioxidative indicators of sows*

Item P. purpureum, % of diet p value
0 5 10 Con versus P. purpureum Linear Quadratic
90 days, U/ml
T‐AOC 10.52 ± 1.47 11.04 ± 1.39 10.79 ± 1.08 .518 .259 .893
T‐SOD 41.67 ± 1.32 42.36 ± 2.09 40.12 ± 1.92 .080 .105 .109
CAT 1.76 ± 0.19 1.58 ± 0.17 1.94 ± 0.33 .248 .174 .329
GSH‐Px 850.6 ± 62.1 859.4 ± 30.4 862.5 ± 60.1 .149 .349 .086
100 days, U/ml
T‐AOC 12.58 ± 1.64 14.41 ± 2.19 15.66 ± 2.16 .012 .008 .135
T‐SOD 65.26 ± 3.75 65.87 ± 2.72 69.22 ± 4.10 .039 .014 .044
CAT 1.95 ± 0.21 2.46 ± 0.15 2.62 ± 0.43 <.001 <.001 .302
GSH‐Px 970.5 ± 43.5 955.8 ± 60.2 991.6 ± 51.2 .512 .707 .278
At parturition, U/ml
T‐AOC 8.25 ± 1.42 10.16 ± 1.61 11.12 ± 1.07 <.001 <.001 .299
T‐SOD 68.41 ± 6.89 70.27 ± 6.52 72.14 ± 7.59 <.001 <.001 .552
CAT 2.15 ± 0.23 2.55 ± 0.42 2.69 ± 0.37 .001 <.001 .720
GSH‐Px 807.4 ± 48.9 799.3 ± 33.7 815.7 ± 45.2 .088 .029 .957
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Values were considered statistically significant when p < .05 and as a trend to significance when .05 ≤ p < .10.

*

Values are means ± SE, n = 10 per treatment.

3.4. The equol concentration in the serum and feces

The serum equol concentration of sows increased linearly and quadratically (p < .05) with the increase of P. purpureum at 100 days of gestation and at parturition (Table 6).

TABLE 6.

Effect of Pennisetum purpureum additive in late gestation on serum equol of sows*

Item P. purpureum, % of diet p value
0 5 10 Con versus P. purpureum Linear Quadratic
90 days, U/ml 86.27 ± 6.89 89.92 ± 6.11 83.56 ± 8.42 .247 .156 .374
100 days, U/ml 97.55 ± 5.41 327.51 ± 27.92 350.13 ± 29.42 <.001 <.001 <.001
At parturition, U/ml 90.22 ± 7.31 412.21 ± 36.14 444.12 ± 42.14 <.001 <.001 <.001
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Values were considered statistically significant when p < .05 and as a trend to significance when .05 ≤ p < .10.

*

Values are means ± SE, n = 10 per treatment.

3.5. The SCFAs concentration in faeces samples

The butyric acid concentration of sows faeces increased linearly (p < .05) with the increase of P. purpureum at 100 days of gestation and at parturition, The acetic acid and propionic acid concentration of sows has no effect with the increase of P. purpureum at 100 days of gestation and at parturition (Table 7).

TABLE 7.

Effect of Pennisetum purpureum additive in gestation on SCFAs concentration in faeces of sows*

Item P. purpureum, % of diet p value
0 5 10 Con versus P. purpureum Linear Quadratic
90 days, μmol/g
Acetic acid 48.39 ± 5.52 47.64 ± 6.12 49.25 ± 5.26 .052 .018 .576
Propionic acid 20.65 ± 2.17 22.14 ± 2.58 20.18 ± 2.72 .058 .071 .107
Butyric acid 10.87 ± 1.44 11.24 ± 1.35 10.52 ± 1.07 .673 .609 .470
100 days, μmol/g
Acetic acid 49.13 ± 4.31 48.45 ± 4.24 50.16 ± 5.04 .423 .889 .196
Propionic acid 22.95 ± 2.56 23.14 ± 2.79 21.22 ± 2.76 .338 .158 .700
Butyric acid 11.29 ± 1.45 14.37 ± 1.72 16.42 ± 1.88 <.001 <.001 .301
At parturition, μmol/g
Acetic acid 46.41 ± 6.28 44.52 ± 5.29 45.24 ± 5.31 .229 .145 .361
Propionic acid 20.42 ± 3.24 21.74 ± 2.98 21.85 ± 2.49 .632 .343 .964
Butyric acid 11.80 ± 2.01 16.52 ± 2.35 18.64 ± 2.75 <.001 <.001 .063
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Values were considered statistically significant when p < .05 and as a trend to significance when .05 ≤ p < .10.

*

Values are means ± SE, n = 10 per treatment.

3.6. Faecal microbiota

A total of 745,198 tags were obtained from the faeces samples range of 33,405 to 41,868, and a total of 14,289 OTUs from 97% of the same level were available for downstream analysis (Figure 2a). The Venn diagram was used to analyse the distribution of OTUs between the two groups. The results showed that there were a total of 559 identical OTUs in the two groups, and the OTUs in the 5% P. purpureum were significantly fewer compared to the control group (5,883 vs. 8,406; Figure 2b). The richness and diversity of microbial community can be reflected by α diversity and β diversity. α diversity is calculated by the observed species index (Figure 3a), and β diversity by principal component analysis (PCA; Figure 3b). Compared with the control group, the species index of sow faeces fed with 5% P. purpureum was significantly higher (p < .05). In the PCA diagram, the faeces microbiota of the control group and the 5% P. purpureum group were divided into two different clusters. In addition, the change of faeces microbiota composition of the 5% P. purpureum group were lighter than that in the control group. The results showed that 5% P. purpureum had an important effect on the diversity of intestinal flora. The significance analysis was performed according to the top seven phyla (relative abundance >0.1% in at least one sample) and the Firmicutes/Bacteroidetes ratio (Figure 4a). The results showed that the relative abundances of Bacteroidetes (p = .027), Fibrobacteres (p = .048) and Actinobacteria (p < .001) were increased, and the relative abundances of Firmicutes (p < .001) and Firmicutes/Bacteroidetes ratio (p = .021) were decreased by 5% of P. purpureum. Thirty‐two families with relative abundance >0.1% in at least one sample were selected for significance analysis. There were eight families with significant difference (Figure 4b). The results showed that the additive of 5% P. purpureum increased the relative abundance of Ruminococcaceae (p = .037), Lachnospiraceae (p = .043) and Coriobacteriaceae (p < .001), and decreased the relative abundance of Prevotellaceae (p = .041), Rikenellaceae (p = .045), Spirochaetaceae (p = .045), Porphyromonadaceae (p = .009) and Enterobacteriaceae (p = .009). Fifty‐five genera with relative abundance >0.1% in at least one sample were selected for significance analysis. There were 14 genera with significant difference (Figure 4c). The results showed that the additive of 5% P. purpureum increased the relative abundance of Oscillibacter (p < .001), Streptococcus (p < .001), Oscillospira (p = .001), Prevotellaceae_UCG_001 (p = .004), and Lachnospiraceae_UCG_005 (p = .036), and decreased the relative abundance of Romboutsia (p < .001), Lachnospiraceae_AC2044_group (p < .001), Erysipelotrichaceae_UCG_004 (p = .007), Desulfovibrio (p = .008), Turicibacter (p = .015), Terrisporobacter (p = .023), Escherichia_Shigella (p < .001), Succinivibrio (p = .043) and Fibrobacter (p = .048).

FIGURE 3.

FIGURE 3

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Alpha diversity and beta diversity analyses of microbial community structure. (a) The observed species index analyses, p < .001; (b) principal component analysis; ANOSIM analyses show the difference of microbial community structure. R value is >0, indicating significant differences between groups. The reliability of statistical analysis is expressed by p value

FIGURE 4.

FIGURE 4

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Relative abundances of faecal microbiota composition at the phylum level (a), family level (b), and the genus level (c). (a) The relative abundances of top seven phyla of faecal microbiota composition. (b) The relative abundances of eight family (%, >0.1% in at least one sample) with significant difference. (c) The relative abundances of 14 genera (%, >0.1% in at least one sample) with significant difference. Data were expressed as means ± SE, n = 10 for each treatment. CONG, the control group; PPG, the 5% Pennisetum purpureum group

4. DISCUSSION

In this study, we investigated the effects of adding P. purpureum to sow diets on antioxidant indices, immune parameters and faecal microbiota of sows during late gestation. The results showed that the additive of P. purpureum improved the antioxidant ability and immune function, enhanced the serum equol content and changed the composition of the intestinal microbiota of sows. In addition, in consideration of nutrient digestibility, the additive of 5% P. purpureum shows the best effect.

In this study, we provided equal amounts of net energy and standard ileal digestible amino acids to the diets of different treatment groups. Through composition analysis, it was found that the contents of NDF and ADF in different treatment groups differed greatly. We infer that the effects of P. purpureum on antioxidant ability, immune function and intestinal microbiota of sows in late pregnancy may be due to the fibre content of different treatment groups.

Studies have shown that the metabolic burden of sows will increase the oxidation of lipids and proteins in late pregnancy, leading to increased oxidative stress (Berchieri‐Ronchi et al., 2011). MDA, T‐AOC, GSH‐Px, CAT and SOD can be used to determine the redox state of sow serum. MDA is a sign of oxidative stress, and its increased level indicates that the animal is in a strong oxidative stress state (Cao et al., 2019). SOD can catalyse the degradation of superoxide radicals into oxygen and hydrogen peroxide, which are then degraded by CAT. T‐AOC is an important comprehensive index reflecting the total antioxidant capacity of animals. GSH PX can act as a reducing agent to prevent the production of lipid peroxide (Berchieri‐Ronchi et al., 2011; Mou et al., 2020; Xie et al., 2016). It is well known that due to the special physiological metabolism during late gestation, a large amount of free radicals are produced (Alanazi et al., 2018; Gitto et al., 2002; Peter Stein et al., 2008; Zimmer & Spencer, 2015). Oxidative stress occurs if excess free radicals are not removed in time, which leads to metabolic disorders and impaired the health of sows (Kim et al., 2013; Zhao et al., 2013; Zhou, Xu, et al., 2019). Oxidative stress might be an important reasons leading to lower reproduction performance of sows (Cools et al., 2011; Gaykwad et al., 2019; Meng et al., 2018; Su et al., 2017; Tan et al., 2015; Wang et al., 2016). In this study, with the increase of P. purpureum, the ability of scavenging free radicals was improved, the content of MDA in serum of sows in late gestation was reduced, and the content of T‐AOC, T‐SOD and CAT was increased, which indicated that the antioxidant capacity of sows was improved. The study of Shah et al. showed that betaine supplementation can improve the digestibility of NDF and ADF, and improve the antioxidant capacity of dairy cows (Shah et al., 2020). The study of Pillai et al. also showed that dietary fiber can control the level of free radicals and prevent oxidative stress (Pillai et al., 1999). In addition, we found that the abundance of IgG and IgM in the serum of the P. purpureum inclusion diet sows were significantly increased, which were involved in humoral immunity and enhances immune function (Kielland et al., 2015; Osterlundh et al., 1998). This is consistent with previous studies (Jiang et al., 2014; Xie et al., 2019). Adding P. purpureum can enhance the immune function of sows, which may be because P. purpureum rich in fibre can regulate the intestinal microbiota interacting with the immune system (Chen et al., 2013; Wang, Qin, et al., 2018), and the colonization of intestinal microbiota is closely related to the animal immune function (Cerf‐Bensussan & Gaboriau‐Routhiau, 2010).

Our results also show that adding P. purpureum can increase the amount of equol in serum. The daidzein is metabolized by the intestinal microbiota to equol in the gastrointestinal tract (Setchell & Clerici, 2010). Equol has anti‐inflammatory effect and is more antioxidant than its precursor, daidzein (Atkinson et al., 2005; Danciu et al., 2018). Moreover in human serum, equol has higher effective free fraction and lower plasma clearance than daidzein (Lampe, 2003). However, intestinal microbiota are key determinants of the formation of metabolites and variable between individuals (Levy et al., 2016; Ma et al., 2017). In order to improve the beneficial effect of soybeans, it has been tested that the intestinal microbiota can regulate the production of equol (Clavel et al., 2005; Hazim et al., 2016; Lambert et al., 2017; Tousen et al., 2013).

Therefore, we hypothesis that the additive of P. purpureum in the diet may change the composition of intestinal microbiota to produce equol, and then enter the circulatory system by absorption. To validate the correlation between equol content and intestinal microbiota, we analysed the faecal microbiota in sows with 5% P. purpureum inclusion (n = 10) and controls (n = 10). Faecal samples were collected from 110 days of gestation for three consecutive days, and the diversity analysis of 16srrna was performed. In this 16srrna analysis, we have some limitations in the sampling of faecal. Considering that the concentration of equol in serum of sows increased linearly with the increase of P. purpureum at 100 days of gestation and at parturition, we only selected faecal samples from the last three consecutive days of late gestation, and did not analyse faecal microbiota in different periods. There are similar sampling analysis before (Hasan et al., 2018). Therefore, our study can provide some research basis for the influence of P. purpureum in diets on the faecal microbiota of sows in late gestation, but further research is needed. The results showed that the relative abundance of Bacteroidetes, Fibrobacteres and Actinobacteria could be increased and the relative abundance of Firmicutes and Firmicutes/Bacteroidetes ratio could be reduced by adding 5% P. purpureum. At family level, the 5% P. purpureum mainly increased the relative abundance of Ruminococcaceae, Lachnospiraceae and Coriobacteriaceae; and decreased the relative abundance of Prevotellaceae, Rikenellaceae, Spirochaetaceae, Porphyromonadaceae and Enterobacteriaceae. At genus level, the 5% P. purpureum mainly increased the relative abundance of Oscillibacter, Streptococcus, Oscillospira, Prevotellaceae_UCG_001 and Lachnospiraceae_UCG_005; and decreased the relative abundance of Romboutsia, Lachnospiraceae_AC2044_group, Erysipelotrichaceae_UCG_004, Desulfovibrio, Turicibacter, Terrisporobacter, Escherichia_Shigella, Succinivibrio and Fibrobacter. We infer that the additive of P. purpureum to the feed causes differences in the gut microbiota, which may be due to the different fibre content. Fibre digestion is a process of microbial fermentation, most of which occurs in the cecum and large intestine of pigs (Farrell & Johnson, 1972; Imoto & Namioka, 1978; Kass et al., 1980). Fibre can affect the diversity of intestinal microbial community and play a positive role in maintaining intestinal health (Jha et al., 2010; Knudsen, 2001). Feeding high fibre diet to growing pigs can increase the activity of bacteria related to fibre degradation in large intestine (Chen et al., 2013; Wang, Ji, et al., 2018), and fiber degrading bacteria are beneficial to intestinal health (Williams et al., 2002). SCFAs concentration can be used as an important index to evaluate the fermentation intensity of hindgut (Serena et al., 2008). Research shows that bacteria of Bacteroidetes phylum, particularly Prevotellaceae_UCG_001, are effective in fermenting fibers into SCFAs (Qi et al., 2019; Wang, Martin, et al., 2019). SCFAs play an important role in the fermentation of equol, especially butyrate (Decroos et al., 2005; Dey, 2019). In addition, SCFA can effectively restrain the reproduction of harmful bacteria (for example Escherichia_Shigella) and promote the reproduction of beneficial bacteria. It is known that many bacteria capable of fermenting daidzein and its metabolites into equol are mainly concentrated in the Actinobacteria phylum, especially in the Coriobacteriaceae (Abiru et al., 2013; Guadamuro et al., 2019; Kawada et al., 2016; Matthies et al., 2008; Tsuji et al., 2010). Above all, the antioxidant capacity and immune function of the sows from the 5% P. purpureum group were increased, and the mechanism may be due to the increased abundance of coriobacteriaceae and Prevotellaceae_UCG_001, and increased the equol and SCFAs contents, which played a central role in antioxidant capacity and immune function.

5. CONCLUSIONS

This study shows that the additive of P. purpureum can enhance the antioxidant ability and immune function of sow in late gestation. In addition, the additive of 5% P. purpureum in the diet might change the composition of intestinal microbiota of sows, particularly the relative abundance of Coriobacteriaceae increased; however, this warrants further investigation.

CONFLICT OF INTEREST

The authors declare no conflict of interest.

AUTHOR CONTRIBUTIONS

Peng‐Fei Huang: Conceptualization; Supervision; Writing‐original draft; Writing‐review & editing. Qi Mou: Conceptualization; Supervision; Writing‐original draft; Writing‐review & editing. Ying Yang: Investigation. Jiaming Li: Investigation. Minglang Xu: Investigation. Jing Huang: Data curation. Jianzhong Li: Conceptualization. Huansheng Yang: Conceptualization. Xiaoxiao Liang: Data curation. Yulong Yin: Conceptualization.

ETHICAL STATEMENT

The authors confirm that the ethical policies of the journal, as noted on the journal's author guidelines page, have been adhered to and the appropriate Ethical Review Committee approval has been received. All procedures and the use of animals in this experiment were carried out in accordance with the Hunan Normal University Animal Care and Use Committee guidelines (1907017).

PEER REVIEW

The peer review history for this article is available at https://publons.com/publon/10.1002/vms3.450.

ACKNOWLEDGEMENTS

We would like to thank Changsha Haishang Limited Company for their support during the feeding trial.

Huang P‐F, Mou Q, Yang Y, et al. Effects of supplementing sow diets during late gestation with Pennisetum purpureum on antioxidant indices, immune parameters and faecal microbiota. Vet Med Sci. 2021;7:1347–1358. 10.1002/vms3.450

Peng‐Fei Huang and Qi Mou should be considered joint first author.

Funding information

This work was supported by the Natural Science Foundation of Hunan Province (No. 2018JJ3346), Hunan Province's Strategic and Emerging Industrial Projects (2018GK4035), Hunan Province's Changsha‐Zhuzhou‐Xiangtan National Independent Innovation Demonstration Zone Projects (2017XK2058) and Graduates Innovative Experiment Project of Hunan Normal University (No. 2018135).

Contributor Information

Peng‐Fei Huang, Email: perfehuang@foxmail.com.

Huan‐Sheng Yang, Email: perfehuang@foxmail.com, Email: yhs@hunnu.edu.cn.

REFERENCES

  1. Abiru, Y. , Ueno, T. , & Uchiyama, S. (2013). Isolation and characterization of novel S‐equol‐producing bacteria from brines of stinky tofu, a traditional fermented soy food in Taiwan. International Journal of Food Science & Technology, 64(8), 936–943. 10.3109/09637486.2013.816936 [DOI] [PubMed] [Google Scholar]
  2. Alanazi, R. , Alotaibi, M. , & Djouhri, L. (2018). In vitro effects of hydrogen peroxide on rat uterine contraction before and during pregnancy. Croatian Medical Journal, 59(6), 327–334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Al‐Sagheer, A. A. , Abd El‐Hack, M. E. , Alagawany, M. , Naiel, M. A. , Mahgoub, S. A. , Badr, M. M. , Hussein, E. O. S. , Alowaimer, A. N. , & Swelum, A. A. (2019). Paulownia leaves as a new feed resource: Chemical composition and effects on growth, carcasses, digestibility, blood biochemistry, and intestinal bacterial populations of growing rabbits. Animals (Basel), 9(3). 10.3390/ani9030095 [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Atkinson, C. , Frankenfeld, C. L. , & Lampe, J. W. (2005). Gut bacterial metabolism of the soy isoflavone daidzein: Exploring the relevance to human health. Experimental Biology and Medicine (Maywood), 230(3), 155–170. 10.1177/153537020523000302 [DOI] [PubMed] [Google Scholar]
  5. Aube, L. , Guay, F. , Bergeron, R. , Belanger, G. , Tremblay, G. F. , & Devillers, N. (2019). Sows' preferences for different forage mixtures offered as fresh or dry forage in relation to botanical and chemical composition. Animal, 1–11. 10.1017/s1751731119000958 [DOI] [PubMed] [Google Scholar]
  6. Barbato, O. , Holmes, B. , Filipescu, I. E. , & Celi, P. (2019). Dietary supplementation of yerba mate (Ilex paraguariensis) during the dry period improves redox balance in lactating dairy cows. Antioxidants (Basel, Switzerland), 8(2). 10.3390/antiox8020038 [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Berchieri‐Ronchi, C. B. , Kim, S. W. , Zhao, Y. , Correa, C. R. , Yeum, K. J. , & Ferreira, A. L. (2011). Oxidative stress status of highly prolific sows during gestation and lactation. Animal, 5(11), 1774–1779. 10.1017/S1751731111000772 [DOI] [PubMed] [Google Scholar]
  8. Bolger, A. M. , Lohse, M. , & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinform, 30(15), 2114–2120. 10.1093/bioinformatics/btu170 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Calvert, C. C. , Steele, N. C. , & Rosebrough, R. W. (1985). Digestibility of fiber components and reproductive performance of sows fed high levels of alfalfa meal. Journal of Animal Science, 61(3), 595–602. 10.2527/jas1985.613595x [DOI] [PubMed] [Google Scholar]
  10. Cao, M. , Li, Y. , Wu, Q. J. , Zhang, P. , Li, W. T. , Mao, Z. Y. , Wu, D. M. , Jiang, X. M. , Zhuo, Y. , Fang, Z. F. , Che, L. Q. , Xu, S. Y. , Feng, B. , Li, J. , Lin, Y. , & Wu, D. (2019). Effects of dietary Clostridium butyricum addition to sows in late gestation and lactation on reproductive performance and intestinal microbiota. Journal of Animal Science, 97(8), 3426–3439. 10.1093/jas/skz186 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Caporaso, J. G. , Kuczynski, J. , Stombaugh, J. , Bittinger, K. , Bushman, F. D. , Costello, E. K. , Fierer, N. , Pena, A. G. , Goodrich, J. K. , Gordon, J. I. , Huttley, G. A. , Kelley, S. T. , Knights, D. , Koenig, J. E. , Ley, R. E. , Lozupone, C. A. , McDonald, D. , Muegge, B. D. , Pirrung, M. , … Knight, R. (2010). QIIME allows analysis of high‐throughput community sequencing data. Nature Methods, 7(5), 335–336. 10.1038/nmeth.f.303 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Castagnino, D. S. , Kammes, K. L. , Allen, M. S. , Gervais, R. , Chouinard, P. Y. , & Girard, C. L. (2016). Particle length of silages affects apparent ruminal synthesis of B vitamins in lactating dairy cows. Journal of Dairy Science, 99(8), 6229–6236. 10.3168/jds.2016-11274 [DOI] [PubMed] [Google Scholar]
  13. Cerf‐Bensussan, N. , & Gaboriau‐Routhiau, V. (2010). The immune system and the gut microbiota: Friends or foes? Nature Reviews Immunology, 10(10), 735–744. 10.1038/nri2850 [DOI] [PubMed] [Google Scholar]
  14. Chen, L. , Zhang, H. F. , Gao, L. X. , Zhao, F. , Lu, Q. P. , & Sa, R. N. (2013). Effect of graded levels of fiber from alfalfa meal on intestinal nutrient and energy flow, and hindgut fermentation in growing pigs. Journal of Animal Science, 91(10), 4757–4764. 10.2527/jas.2013-6307 [DOI] [PubMed] [Google Scholar]
  15. Clavel, T. , Fallani, M. , Lepage, P. , Levenez, F. , Mathey, J. , Rochet, V. , Serezat, M. , Sutren, M. , Henderson, G. , Bennetau‐Pelissero, C. , Tondu, F. , Blaut, M. , Dore, J. , & Coxam, V. (2005). Isoflavones and functional foods alter the dominant intestinal microbiota in postmenopausal women. Journal of Nutrition, 135(12), 2786–2792. 10.1093/jn/135.12.2786 [DOI] [PubMed] [Google Scholar]
  16. Cools, A. , Maes, D. , Papadopoulos, G. , Vandermeiren, J. A. , Meyer, E. , Demeyere, K. , De Smet, S. , & Janssens, G. P. (2011). Dose‐response effect of fish oil substitution in parturition feed on erythrocyte membrane characteristics and sow performance. Journal of Animal Physiology and Animal Nutrition (Berl), 95(1), 125–136. 10.1111/j.1439-0396.2010.01119.x [DOI] [PubMed] [Google Scholar]
  17. Danciu, C. , Avram, S. , Pavel, I. Z. , Ghiulai, R. , Dehelean, C. A. , Ersilia, A. , Minda, D. , Petrescu, C. , Moaca, E. A. , & Soica, C. (2018). Main isoflavones found in dietary sources as natural anti‐inflammatory agents. Current Drug Targets, 19(7), 841–853. 10.2174/1389450118666171109150731 [DOI] [PubMed] [Google Scholar]
  18. Decroos, K. , Vanhemmens, S. , Cattoir, S. , Boon, N. , & Verstraete, W. (2005). Isolation and characterisation of an equol‐producing mixed microbial culture from a human faecal sample and its activity under gastrointestinal conditions. Archives of Microbiology, 183(1), 45–55. 10.1007/s00203-004-0747-4 [DOI] [PubMed] [Google Scholar]
  19. Dey, P. (2019). Gut microbiota in phytopharmacology: A comprehensive overview of concepts, reciprocal interactions, biotransformations and mode of actions. Pharmacological Research, 147, 104367. 10.1016/j.phrs.2019.104367 [DOI] [PubMed] [Google Scholar]
  20. Edgar, R. C. (2013). UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10), 996. [DOI] [PubMed] [Google Scholar]
  21. Edgar, R. C. , Haas, B. J. , Clemente, J. C. , Quince, C. , & Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinform, 27(16), 2194–2200. 10.1093/bioinformatics/btr381 [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Farrell, D. J. , & Johnson, K. A. (1972). Utilization of cellulose by pigs and its effects on caecal function. Animal Science, 14(02), 209–217. 10.2527/jas1980.501192x [DOI] [Google Scholar]
  23. Gabai, G. , De Luca, E. , Miotto, G. , Zin, G. , Stefani, A. , Da Dalt, L. , Barberio, A. , & Celi, P. (2019). Relationship between protein oxidation biomarkers and uterine health in dairy cows during the postpartum period. Antioxidants (Basel, Switzerland), 8(1). 10.3390/antiox8010021 [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gaykwad, C. K. , De, U. K. , Jadhav, S. E. , Chethan, G. E. , Akhilesh, N. R. , Sahoo, D. B. , Mondal, G. K. , Gaur, M. R. , Verma, M. R. , & Chaudhuri, P. (2019). Adding alpha‐tocopherol‐selenium and ascorbic acid to periparturient sow diets influences hemogram, lipid profile, leptin, oxidant/antioxidant imbalance, performance and neonatal piglet mortality. Research in Veterinary Science, 125, 360–369. 10.1016/j.rvsc.2019.07.014 [DOI] [PubMed] [Google Scholar]
  25. Gitto, E. , Reiter, R. J. , Karbownik, M. , Tan, D. X. , Gitto, P. , Barberi, S. , & Barberi, I. (2002). Causes of oxidative stress in the pre‐ and perinatal period. Biology of the Neonate, 81(3), 146–157. 10.1159/000051527 [DOI] [PubMed] [Google Scholar]
  26. Guadamuro, L. , Azcarate‐Peril, M. A. , Tojo, R. , Mayo, B. , & Delgado, S. (2019). Use of high throughput amplicon sequencing and ethidium monoazide dye to track microbiota changes in an equol‐producing menopausal woman receiving a long‐term isoflavones treatment. AIMS Microbiol, 5(1), 102–116. 10.3934/microbiol.2019.1.102 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hasan, S. , Saha, S. , Junnikkala, S. , Orro, T. , Peltoniemi, O. , & Oliviero, C. (2018). Late gestation diet supplementation of resin acid‐enriched composition increases sow colostrum immunoglobulin G content, piglet colostrum intake and improve sow gut microbiota. Animal, 1–8. 10.1017/S1751731118003518 [DOI] [PubMed] [Google Scholar]
  28. Hazim, S. , Curtis, P. J. , Schar, M. Y. , Ostertag, L. M. , Kay, C. D. , Minihane, A. M. , & Cassidy, A. (2016). Acute benefits of the microbial‐derived isoflavone metabolite equol on arterial stiffness in men prospectively recruited according to equol producer phenotype: A double‐blind randomized controlled trial. American Journal of Clinical Nutrition, 103(3), 694–702. 10.3945/ajcn.115.125690 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. He, Y. , Qiu, Q. , Shao, T. , Niu, W. , Xia, C. , Wang, H. , Li, Q. , Gao, Z. , Yu, Z. , Su, H. , & Cao, B. (2017). Dietary alfalfa and calcium salts of long‐chain fatty acids alter protein utilization, microbial populations, and plasma fatty acid profile in holstein freemartin heifers. Journal of Agriculture and Food Chemistry, 65(50), 10859–10867. 10.1021/acs.jafc.7b04173 [DOI] [PubMed] [Google Scholar]
  30. Holzgraefe, D. P. , Fahey, G. C. Jr , Jensen, A. H. , & Berger, L. L. (1985). Effects of dietary alfalfa: Orchardgrass hay and lasalocid on nutrient utilization by gravid sows. Journal of Animal Science, 60(5), 1247–1259. 10.2527/jas1985.6051247x [DOI] [PubMed] [Google Scholar]
  31. Holzgraefe, D. P. , Jensen, A. H. , Fahey, G. C. Jr , & Grummer, R. R. (1986). Effects of dietary alfalfa‐orchardgrass hay and lasalocid on sow reproductive performance. Journal of Animal Science, 62(5), 1145–1153. 10.2527/jas1986.6251145x [DOI] [PubMed] [Google Scholar]
  32. Hu, C. , Yang, Y. , Li, J. , Wang, H. , Cheng, C. , Yang, L. , Li, Q. , Deng, J. , Liang, Z. , Yin, Y. , Xie, Z. , & Tan, C. (2019). Maternal diet‐induced obesity compromises oxidative stress status and angiogenesis in the porcine placenta by upregulating Nox2 expression. Oxidative Medicine and Cellular Longevity, 2019, 2481592. 10.1155/2019/2481592 [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Huang, Q. , Holman, D. B. , Alexander, T. , Hu, T. , Jin, L. , Xu, Z. , McAllister, T. A. , Acharya, S. , Zhao, G. , & Wang, Y. (2018). Fecal microbiota of lambs fed purple prairie clover (Dalea purpurea Vent.) and alfalfa (Medicago sativa). Archives of Microbiology, 200(1), 137–145. 10.1007/s00203-017-1427-5 [DOI] [PubMed] [Google Scholar]
  34. Imoto, S. , & Namioka, S. (1978). VFA metabolism in the pig. Journal of Animal Science, 2, 2. 10.2527/jas1978.472479x [DOI] [PubMed] [Google Scholar]
  35. Jha, R. , Rossnagel, B. , Pieper, R. , Van Kessel, A. , & Leterme, P. (2010). Barley and oat cultivars with diverse carbohydrate composition alter ileal and total tract nutrient digestibility and fermentation metabolites in weaned piglets. Animal, 4(5), 724–731. 10.1017/s1751731109991510 [DOI] [PubMed] [Google Scholar]
  36. Jiang, J. F. , Song, X. M. , Wu, J. L. , & Jiang, Y. Q. (2014). Effects of alfalfa meal on the intestinal microbial diversity and immunity of growing ducks. Journal of Animal Physiology and Animal Nutrition (Berl), 98(6), 1039–1046. 10.1111/jpn.12167 [DOI] [PubMed] [Google Scholar]
  37. Kass, M. L. , Van, S. P. J. , & Pond, W. G. (1980). Utilization of dietary fiber from alfalfa by growing swine. II. Volatile fatty acid concentrations in and disappearance from the gastrointestinal tract. Journal of Animal Science, 50(1), 192–197. 10.1017/S0003356100010898 [DOI] [Google Scholar]
  38. Kawada, Y. , Yokoyama, S. , Yanase, E. , Niwa, T. , & Suzuki, T. (2016). The production of S‐equol from daidzein is associated with a cluster of three genes in Eggerthella sp. YY7918. Bioscience of Microbiota, Food and Health, 35(3), 113–121. 10.12938/bmfh.2015-023 [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kielland, C. , Rootwelt, V. , Reksen, O. , & Framstad, T. (2015). The association between immunoglobulin G in sow colostrum and piglet plasma. Journal of Animal Science, 93(9), 4453–4462. 10.2527/jas.2014-8713 [DOI] [PubMed] [Google Scholar]
  40. Kim, S. W. , Weaver, A. C. , Shen, Y. B. , & Zhao, Y. (2013). Improving efficiency of sow productivity: Nutrition and health. Journal of Animal Science and Biotechnology, 4(1), 26. 10.1186/2049-1891-4-26 [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Knudsen, K. E. B. (2001). The nutritional significance of ‘dietary fibre’ analysis. Animal Feed Science and Technology, 90(1–2). 10.1016/S0377-8401(01)00193-6 [DOI] [Google Scholar]
  42. Krogh, U. , Bruun, T. S. , Poulsen, J. , & Theil, P. K. (2017). Impact of fat source and dietary fibers on feed intake, plasma metabolites, litter gain and the yield and composition of milk in sows. Animal, 11(6), 975–983. 10.1017/s1751731116002585 [DOI] [PubMed] [Google Scholar]
  43. Lambert, M. N. T. , Thybo, C. B. , Lykkeboe, S. , Rasmussen, L. M. , Frette, X. , Christensen, L. P. , & Jeppesen, P. B. (2017). Combined bioavailable isoflavones and probiotics improve bone status and estrogen metabolism in postmenopausal osteopenic women: A randomized controlled trial. American Journal of Clinical Nutrition, 106(3), 909–920. 10.3945/ajcn.117.153353 [DOI] [PubMed] [Google Scholar]
  44. Lampe, J. W. (2003). Isoflavonoid and lignan phytoestrogens as dietary biomarkers. Journal of Nutrition, 133(Suppl 3), 956s–964s. 10.1093/jn/133.3.956S [DOI] [PubMed] [Google Scholar]
  45. Levy, M. , Thaiss, C. A. , & Elinav, E. (2016). Metabolites: Messengers between the microbiota and the immune system. Genes & Development, 30(14), 1589–1597. 10.1101/gad.284091.116 [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Li, X. , Sun, H. , Zhang, L. , Liu, H. , Li, J. , Wang, C. , Zhang, M. , & Bao, J. (2019). Technical note: Effects of age and confinement on pupillary light reflex in sows1. Journal of Animal Science, 97(5), 2009–2014. 10.1093/jas/skz100 [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Liu, B. , Wang, W. , Zhu, X. , Sun, X. , Xiao, J. , Li, D. , Cui, Y. , Wang, C. , & Shi, Y. (2018). Response of gut microbiota to dietary fiber and metabolic interaction with SCFAs in piglets. Frontiers in Microbiology, 9, 2344. 10.3389/fmicb.2018.02344 [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Liu, J. , Zhang, M. , Xue, C. , Zhu, W. , & Mao, S. (2016). Characterization and comparison of the temporal dynamics of ruminal bacterial microbiota colonizing rice straw and alfalfa hay within ruminants. Journal of Dairy Science, 99(12), 9668–9681. 10.3168/jds.2016-11398 [DOI] [PubMed] [Google Scholar]
  49. Liu, S. , Yuan, M. , Jin, D. , Wang, Z. , Zou, H. , Wang, L. , Xue, B. , Wu, G. , Tian, J. , Cai, T. Y. , & Peng, Q. (2018). Effects of the particle of ground alfalfa hay on the growth performance, methane production and archaeal populations of rabbits. PLoS ONE, 13(9), e0203393. 10.1371/journal.pone.0203393 [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Ma, N. , Tian, Y. , Wu, Y. , & Ma, X. (2017). Contributions of the interaction between dietary protein and gut microbiota to intestinal health. Current Protein and Peptide Science, 18(8), 795–808. 10.2174/1389203718666170216153505 [DOI] [PubMed] [Google Scholar]
  51. Martin, C. , Ferlay, A. , Mosoni, P. , Rochette, Y. , Chilliard, Y. , & Doreau, M. (2016). Increasing linseed supply in dairy cow diets based on hay or corn silage: Effect on enteric methane emission, rumen microbial fermentation, and digestion. Journal of Dairy Science, 99(5), 3445–3456. 10.3168/jds.2015-10110 [DOI] [PubMed] [Google Scholar]
  52. Matthies, A. , Clavel, T. , Gutschow, M. , Engst, W. , Haller, D. , Blaut, M. , & Braune, A. (2008). Conversion of daidzein and genistein by an anaerobic bacterium newly isolated from the mouse intestine. Applied and Environment Microbiology, 74(15), 4847–4852. 10.1128/aem.00555-08 [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Mattioli, S. , Dal Bosco, A. , Combes, S. , Moscati, L. , Crotti, S. , Cartoni Mancinelli, A. , Cotozzolo, E. , & Castellini, C. (2019). Dehydrated alfalfa and fresh grass supply in young rabbits: effect on performance and caecal microbiota biodiversity. Animals (Basel), 9(6). 10.3390/ani9060341 [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Meng, Q. , Guo, T. , Li, G. , Sun, S. , He, S. , Cheng, B. , Shi, B. , & Shan, A. (2018). Dietary resveratrol improves antioxidant status of sows and piglets and regulates antioxidant gene expression in placenta by Keap1‐Nrf2 pathway and Sirt1. Journal of Animal Science and Biotechnology, 9, 34. 10.1186/s40104-018-0248-y [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Merlot, E. , Pastorelli, H. , Prunier, A. , Pere, M. C. , Louveau, I. , Lefaucheur, L. , Perruchot, M. H. , Meunier‐Salaun, M. C. , Gardan‐Salmon, D. , Gondret, F. , & Quesnel, H. (2019). Sow environment during gestation: Part I. Influence on maternal physiology and lacteal secretions in relation with neonatal survival. Animal, 13(7), 1432–1439. 10.1017/s1751731118002987 [DOI] [PubMed] [Google Scholar]
  56. Mou, D. , Ding, D. , Yan, H. , Qin, B. , Dong, Y. , Li, Z. , Che, L. , Fang, Z. , Xu, S. , Lin, Y. , Zhuo, Y. , Li, J. , Huang, C. , Zou, Y. , Li, L. , Briens, M. , Wu, D. , & Feng, B. (2020). Maternal supplementation of organic selenium during gestation improves sows and offspring antioxidant capacity and inflammatory status and promotes embryo survival. Food & Function, 11(9), 7748–7761. 10.1039/d0fo00832j [DOI] [PubMed] [Google Scholar]
  57. National Research Council (NRC) (2012). Nutrient Requirements of Swine: Eleventh, Reviseded. Washington DC: The National Academies Press. 10.17226/13298 [DOI] [Google Scholar]
  58. Osterlundh, I. , Holst, H. , & Magnusson, U. (1998). Hormonal and immunological changes in blood and mammary secretion in the sow at parturition. Theriogenology, 50(3), 465–477. 10.1016/s0093-691x(98)00153-8 [DOI] [PubMed] [Google Scholar]
  59. Peter Stein, T. , Scholl, T. O. , Schluter, M. D. , Leskiw, M. J. , Chen, X. , Spur, B. W. , & Rodriguez, A. (2008). Oxidative stress early in pregnancy and pregnancy outcome. Free Radical Research, 42(10), 841–848. 10.1080/10715760802510069 [DOI] [PubMed] [Google Scholar]
  60. Pillai, M. G. , Thampi, B. S. H. , Menon, V. P. , & Leelamma, S. (1999). Influence of dietary fiber from coconut kernel (Cocos nucifera) on the 1,2‐dimethylhydrazine‐induced lipid peroxidation in rats. Journal of Nutritional Biochemistry, 10, 555–560. 10.1016/s0955-2863(99)00035-2 [DOI] [PubMed] [Google Scholar]
  61. Qi, Z. , Shi, S. , Tu, J. , & Li, S. (2019). Comparative metagenomic sequencing analysis of cecum microbiotal diversity and function in broilers and layers. 3. Biotech, 9(8), 316. 10.1007/s13205-019-1834-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Qiong, W. , Garrity, G. M. , Tiedje, J. M. , & Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environment Microbiology, 73(16), 5261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Reyon, D. , Tsai, S. Q. , Khayter, C. , Foden, J. A. , Sander, J. D. , & Joung, J. K. (2012). FLASH assembly of TALENs for high‐throughput genome editing. Nature Biotechnology, 30(5), 460–465. 10.1038/nbt.2170 [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Serena, A. , Jrgensen, H. , & Knudsen, K. E. B. (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(9), 2208–2216. 10.2527/jas.2006-060 [DOI] [PubMed] [Google Scholar]
  65. Setchell, K. D. , & Clerici, C. (2010). Equol: History, chemistry, and formation. Journal of Nutrition, 140(7), 1355s–1362s. 10.3945/jn.109.119776 [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Shah, A. M. , Ma, J. , Wang, Z. , Zou, H. , Hu, R. , & Peng, Q. (2020). Betaine supplementation improves the production performance, rumen fermentation, and antioxidant profile of dairy cows in heat stress. Animals (Basel), 10(4). 10.3390/ani10040634 [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Su, G. , Zhao, J. , Luo, G. , Xuan, Y. , Fang, Z. , Lin, Y. , Xu, S. , Wu, J. H. , & Che, L. (2017). Effects of oil quality and antioxidant supplementation on sow performance, milk composition and oxidative status in serum and placenta. Lipids in Health and Disease, 16(1), 107. 10.1186/s12944-017-0494-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Tan, C. , Wei, H. , Ao, J. , Long, G. , & Peng, J. (2016). Inclusion of konjac flour in the gestation diet changes the gut microbiota, alleviates oxidative stress, and improves insulin sensitivity in sows. Applied and Environment Microbiology, 82(19), 5899–5909. 10.1128/aem.01374-16 [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Tan, C. , Wei, H. , Sun, H. , Ao, J. , Long, G. , Jiang, S. , & Peng, J. (2015). Effects of dietary supplementation of oregano essential oil to sows on oxidative stress status, lactation feed intake of sows, and piglet performance. BioMed Research International, 2015, 525218. 10.1155/2015/525218 [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Tousen, Y. , Uehara, M. , Abe, F. , Kimira, Y. , & Ishimi, Y. (2013). Effects of short‐term fructooligosaccharide intake on equol production in Japanese postmenopausal women consuming soy isoflavone supplements: A pilot study. Nutrition Journal, 12, 127. 10.1186/1475-2891-12-127 [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Tsuji, H. , Moriyama, K. , Nomoto, K. , Miyanaga, N. , & Akaza, H. (2010). Isolation and characterization of the equol‐producing bacterium Slackia sp. strain NATTS. Archives of Microbiology, 192(4), 279–287. 10.1007/s00203-010-0546-z [DOI] [PubMed] [Google Scholar]
  72. Varel, V. H. (1987). Activity of fiber‐degrading microorganisms in the pig large intestine. Journal of Animal Science, 2, 2. 10.2527/jas1987.652488x [DOI] [PubMed] [Google Scholar]
  73. Verdon, M. , Morrison, R. S. , Rice, M. , & Hemsworth, P. H. (2016). Individual variation in sow aggressive behavior and its relationship with sow welfare. Journal of Animal Science, 94(3), 1203–1214. 10.2527/jas.2015-0006 [DOI] [PubMed] [Google Scholar]
  74. Wang, H. , Hu, C. , Cheng, C. , Cui, J. , Ji, Y. , Hao, X. , Li, Q. , Ren, W. , Deng, B. , Yin, Y. , Deng, J. , & Tan, C. (2019). Unraveling the association of fecal microbiota and oxidative stress with stillbirth rate of sows. Theriogenology, 136. 10.1016/j.theriogenology.2019.06.028 [DOI] [PubMed] [Google Scholar]
  75. Wang, H. , Ji, Y. , Yin, C. , Deng, M. , & Tan, C. (2018). Differential analysis of gut microbiota correlated with oxidative stress in sows with high or low litter performance during lactation. Frontiers in Microbiology, 9, 1665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Wang, J. , Qin, C. , He, T. , Qiu, K. , Sun, W. , Zhang, X. , Jiao, N. , Zhu, W. , & Yin, J. (2018). Alfalfa‐containing diets alter luminal microbiota structure and short chain fatty acid sensing in the caecal mucosa of pigs. Journal of Animal Science and Biotechnology, 9, 11. 10.1186/s40104-017-0216-y [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Wang, X. , Martin, G. B. , Wen, Q. , Liu, S. , Zhang, J. , Yu, Y. , Shi, B. , Guo, X. , Zhao, Y. , & Yan, S. (2019). Linseed oil and heated linseed grain supplements have different effects on rumen bacterial community structures and fatty acid profiles in cashmere kids1. Journal of Animal Science, 97(5), 2099–2113. 10.1093/jas/skz079 [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Wang, Y. S. , Zhou, P. , Liu, H. , Li, S. , Zhao, Y. , Deng, K. , Cao, D. D. , Che, L. Q. , Fang, Z. F. , Xu, S. Y. , Lin, Y. , Feng, B. , Li, J. , & Wu, D. (2016). Effects of inulin supplementation in low‐ or high‐fat diets on reproductive performance of sows and antioxidant defence capacity in sows and offspring. Reproduction in Domestic Animals, 51(4), 492–500. 10.1111/rda.12707 [DOI] [PubMed] [Google Scholar]
  79. Williams, B. A. , Verstegen, M. W. A. , & Tamminga, S. (2002). Fermentation in the large intestine of single‐stomached animals and its relationship to animal health. Nutrition Research Reviews, 14(2), 207–228. 10.1079/NRR200127 [DOI] [PubMed] [Google Scholar]
  80. Xie, C. , Wu, X. , Long, C. , Wang, Q. , Fan, Z. , Li, S. , & Yin, Y. (2016). Chitosan oligosaccharide affects antioxidant defense capacity and placental amino acids transport of sows. BMC Veterinary Research, 12(1). 10.1186/s12917-016-0872-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Xie, Y. , Wang, L. , Sun, H. , Wang, Y. , Yang, Z. , Zhang, G. , & Yang, W. (2019). Immunomodulatory, antioxidant and intestinal morphology‐regulating activities of alfalfa polysaccharides in mice. International Journal of Biological Macromolecules, 133, 1107–1114. 10.1016/j.ijbiomac.2019.04.144 [DOI] [PubMed] [Google Scholar]
  82. Zhao, Y. , Flowers, W. L. , Saraiva, A. , Yeum, K. J. , & Kim, S. W. (2013). Effect of social ranks and gestation housing systems on oxidative stress status, reproductive performance, and immune status of sows. Journal of Animal Science, 91(12), 5848–5858. 10.2527/jas.2013-6388 [DOI] [PubMed] [Google Scholar]
  83. Zheng, M. , Mao, P. , Tian, X. , Guo, Q. , & Meng, L. (2019). Effects of dietary supplementation of alfalfa meal on growth performance, carcass characteristics, meat and egg quality, and intestinal microbiota in Beijing‐you chicken. Poultry Science, 98(5), 2250–2259. 10.3382/ps/pey550 [DOI] [PubMed] [Google Scholar]
  84. Zhou, J. , Xiong, X. , Yin, J. , Zou, L. , Wang, K. , Shao, Y. , & Yin, Y. (2019). Dietary lysozyme alters sow's gut microbiota, serum immunity and milk metabolite profile. Frontiers in Microbiology, 10, 177. 10.3389/fmicb.2019.00177 [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Zhou, Y. , Xu, T. , Wu, Y. , Wei, H. , & Peng, J. (2019). Oxidative stress and inflammation in sows with excess backfat: Up‐regulated cytokine expression and elevated oxidative stress biomarkers in placenta. Animals (Basel), 9(10). 10.3390/ani9100796 [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Zimmer, C. , & Spencer, K. A. (2015). Reduced resistance to oxidative stress during reproduction as a cost of early‐life stress. Comparative Biochemistry and Physiology Part A: Molecular Integrative Physiology, 183, 9–13. 10.1016/j.cbpa.2014.12.032 [DOI] [PubMed] [Google Scholar]

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