Chinese Journal of Animal Nutrition >

2026 , Vol. 38 >Issue 7: 4967 - 4981

DOI: https://doi.org/10.12418/CJAN2026.398

RESEARCH PAPER

Effects of Fermented Honeysuckle on Growth Performance, Immune Function, Antioxidant Capacity and Fecal Microbiota of Weaned Piglets

  • SHI Yinyin , 1, 2 ,
  • WANG Jiancai 1 ,
  • LI Chuanhao 1 ,
  • SUN Houwei 3 ,
  • OUYANG Wenyu 1, 2 ,
  • SHENG Qingkai , 1, * ,
  • LI Haihua , 2, *
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  • 1 Shandong Key Laboratory of Animal Microecologics and Efficient Breeding of Livestock and Poultry, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Ji’nan 250100, China
  • 2 Tianjin Key Laboratory of Agricultural Animal Breeding and Healthy Husbandry, College of Animal Science and Veterinary Medicine, Tianjin Agricultural University, Tianjin 300392, China
  • 3 Zaozhuang Heigai Pig Breeding Co., Ltd., Zaozhuang 277100, China
* SHENG Qingkai, professor, E-mail: ;
LI Haihua, professor, E-mail:

Received date: 2025-12-05

  Online published: 2026-07-13

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Abstract

This experiment was conducted to investigate the effects of fermented honeysuckle on growth performance, immune function, antioxidant capacity and fecal microbiota of weaned piglets. A total of 80 healthy weaned Zaozhuang Heigai piglets with similar body weight of (7.30±0.50) kg were randomly divided into 4 groups with 5 replicates per group and 4 piglets per replicate. The control group (CON group) was fed a basal diet, while the experimental groups were supplemented with 0.8% honeysuckle (HO group), 0.8% honeysuckle plus 0.01% Lactobacillus plantarum (HL group) and 0.8% fermented honeysuckle (FH group) in the basal diet, respectively. The whole trial lasted for 35 days, including a 5-day preliminary trial and a 30-day formal trial. The results showed as follows: 1) compared with the CON group, the final body weight and average daily gain in the HO, HL and FH groups were significantly increased (P<0.05), while the feed-to-gain ratio was significantly decreased (P<0.05). The crude protein digestibility in the FH group was significantly increased (P<0.05). 2) On day 15 of the trial, compared with the CON group, the serum immunoglobulin M (IgM) content in the FH group was significantly increased (P<0.05); the serum interleukin-1β (IL-1β) and tumor necrosis factor-α (TNF-α) contents in the HL and FH groups were extremely significantly decreased (P<0.01), the serum interferon-γ (IFN-γ) content was significantly decreased (P<0.05), the serum swine foot-and-mouth disease type O antibody titer was extremely significantly increased (P<0.01), and the serum classical swine fever antibody blocking rate was significantly increased (P<0.05). On day 30 of the trial, compared with the CON group, the serum immunoglobulin G (IgG), IgM and interleukin-10 (IL-10) contents in the FH group were significantly increased (P<0.05); the serum IL-1β content in the HO, HL and FH groups was significantly decreased (P<0.05), the serum swine foot-and-mouth disease type O antibody titer was extremely significantly increased (P<0.01), and the serum classical swine fever antibody blocking rate was significantly or extremely significantly increased (P<0.05 or P<0.01). 3) Compared with the CON group, on day 15 of the trial, the serum malondialdehyde (MDA) content in the HO, HL and FH groups was significantly decreased (P<0.05), and the serum catalase (CAT) content was significantly increased (P<0.05); on day 30 of the trial, the serum CAT content in the HO, HL and FH groups was extremely significantly increased (P<0.01). 4) Compared with the CON group, the FH group showed increased relative abundance of Selenomonas, Mitsuokella and Eubacterium_ruminantium_group in feces, and decreased relative abundance of Clostridium_sensu_stricto_1. 5) Pearson correlation analysis showed that the relative abundance of UCG-005 in fecal was significantly or extremely significantly positively correlated with serum IgG, IgM, IL-10, glutathione peroxidase (GSH-Px), CAT contents, and apparent crude protein digestibility (P<0.05 or P<0.01); the relative abundance of Clostridium_sensu_stricto_1 was significantly or extremely significantly negatively correlated with serum IgG, IgM, IL-10 and CAT contents (P<0.05 or P<0.01), and was significantly or extremely significantly positively correlated with serum interleukin-6 (IL-6), IL-1β and IFN-γ contents (P<0.05 or P<0.01). In conclusion, dietary supplementation with fermented honeysuckle can promote the growth of weaned piglets, enhance immune function and antioxidant capacity, and optimize the composition of intestinal microbiota.

Key words： weaned piglets; fermented honeysuckle; growth performance; immune function; antioxidant capacity; fecal microbiota

Cite this article

SHI Yinyin , WANG Jiancai , LI Chuanhao , SUN Houwei , OUYANG Wenyu , SHENG Qingkai , LI Haihua . Effects of Fermented Honeysuckle on Growth Performance, Immune Function, Antioxidant Capacity and Fecal Microbiota of Weaned Piglets[J]. Chinese Journal of Animal Nutrition, 2026 , 38(7) : 4967 -4981 . DOI: 10.12418/CJAN2026.398

断奶仔猪受母源分离、环境突变、病原微生物感染等因素影响,抗病力较差,肠道菌群易发生紊乱,常出现生长发育受阻等问题[1]。为减缓断奶应激的不良影响,生产中常在饲粮中添加金银花等中草药以提高机体免疫力,以及添加益生菌类饲料添加剂以调节肠道菌群。金银花又名银花、双花、金藤花,是植物忍冬的干燥花蕾,作为我国认定的第一批药食同源植物,其富含有机酸类、黄酮类、皂苷类和环烯醚萜类等功能性成分,具有抗氧化、抗病毒、抗炎、抑菌等作用[2-3]。益生菌是一类对动物健康有益的活性微生物,可通过在动物肠道内定植,调节肠道菌群平衡、与肠道致病菌形成生态竞争,进而增强机体免疫力,改善动物健康状态[4-5]。益生菌发酵法作为中草药的炮制方法之一,可提高中草药活性成分含量,便于动物肠道吸收利用,进而增强机体免疫功能和抗氧化能力,促进仔猪生长发育[6]。此外,中草药中的一些天然化合物可作为益生元,促进肠道内有益代谢物的合成,改善肠道菌群组成,维护肠道微生态平衡[7-8]。发酵金银花兼具益生菌的微生态调节功能与金银花本身的药用价值,现有研究证实其可缓解酒精性肝病模型小鼠肝脏损伤,提升肠道菌群α多样性指数[9]。但目前关于发酵金银花对断奶仔猪生长及肠道菌群的影响鲜见报道。此外,为降低病毒感染风险,生产中仔猪通常会先后免疫接种猪口蹄疫疫苗和猪瘟疫苗,而饲喂发酵金银花对仔猪疫苗免疫后抗体水平的影响也未见报道。因此,本试验拟探究发酵金银花对断奶仔猪生长性能、免疫功能、抗氧化能力及粪便菌群的影响,分析养分消化吸收、机体免疫应答、抗氧化性能与肠道菌群之间的关系,旨在为生猪健康养殖提供参考。

1 材料与方法

1.1 试验材料

试验猪由枣庄黑盖猪养殖有限公司提供;猪口蹄疫O型疫苗购自金宇保灵生物药品有限公司,猪瘟疫苗购自武汉科前生物股份有限公司;金银花购自山东中平药业有限公司,品种为北花一号;植物乳杆菌购自济宁玉园生物科技有限公司,活菌数为1×109 CFU/g。发酵金银花由山东省农业科学院畜牧兽医研究所利用植物乳杆菌将金银花厌氧发酵7 d制得,成品pH为5.1,总黄酮含量为57 mg/g,绿原酸含量为45.8 mg/g,乳酸菌数量为1×108 CFU/g。

1.2 试验设计

本研究的动物试验方案和程序已获得山东省农业科学院畜牧兽医研究所的批准(批准号:SAAS-2024-067)。选取80头体重[(7.30±0.50) kg]相近、健康的断奶枣庄黑盖仔猪,随机分为4组,每组5个重复,每个重复4头猪。对照组(CON组)饲喂基础饲粮,试验组分别在基础饲粮中添加0.8%金银花(HO组)、0.8%金银花+0.01%植物乳杆菌(HL组)及0.8%发酵金银花(FH组)。试验期35 d,其中预试期5 d,正试期30 d。试验第1天和第8天分别免疫接种猪口蹄疫疫苗和猪瘟疫苗。基础饲粮参照《猪营养需要量》(GB/T 39235—2020)中肉脂型仔猪营养标准配制,其组成及营养水平见表1。
表1 基础饲粮组成及营养水平(风干基础)

Table 1 Composition and nutrient levels of the basal diet (air-dry basis) %

项目Items 含量Content
原料Ingredients
玉米Corn 60.00
豆粕Soybean meal 15.50
膨化豆粕Expanded soybean meal 10.60
膨化大豆Expanded soybean 7.00
鱼粉Fish meal 1.00
大豆油Soybean oil 1.50
石粉Limestone 1.10
磷酸二氢钙Ca(H2PO4)2 1.00
食盐NaCl 0.40
赖氨酸Lys 0.65
蛋氨酸Met 0.25
预混料Premix1) 1.00
合计Total 100.00
营养水平Nutrient levels2)
消化能DE/(MJ/kg) 14.82
干物质DM 89.08
粗蛋白质CP 17.97
粗脂肪EE 4.05
中性洗涤纤维NDF 9.79
酸性洗涤纤维ADF 4.76
钙Ca 0.78
总磷TP 0.62
标准全消化道可消化磷STTD P 0.36
标准回肠可消化赖氨酸SID Lys 1.16
标准回肠可消化蛋氨酸+半胱氨酸
SID Met+Cys		 0.67
标准回肠可消化色氨酸SID Trp 0.21
标准回肠可消化苏氨酸SID Thr 0.63

1)预混料为每千克饲粮提供 The premix provided the following per kg of the diet:VA 15 000 IU,VB1 15 mg,VB2 5.0 mg,VD3 3 000 IU,VE 120 IU,VK 30 IU,叶酸 folic acid 2.0 mg,烟酸 nicotinic acid 30 mg,D-泛酸 D-pantothenic acid 20 mg,生物素 biotin 63 mg,Fe (as ferrous sulfate) 100 mg,Mn (as manganese sulfate) 10 mg,Cu (as copper sulfate) 40 mg,Zn (as zinc sulfate) 60 mg,Se (as sodium selenite) 0.3 mg,I (as potassium iodide) 0.4 mg。

2)干物质、粗蛋白质、粗脂肪、中性洗涤纤维、酸性洗涤纤维、钙和总磷为实测值,其余为根据《猪营养需要量》(GB/T 39235—2020)所得计算值。DM, CP, EE, NDF, ADF, Ca and TP were measured values, while the others were calculated values according to Nutrient Requirements of Swine (GB/T 39235—2020).

1.3 饲养管理

养殖试验于枣庄黑盖猪养殖基地开展。试验前对猪舍进行全面消毒及灭菌,舍内采用自然光照与自然通风模式。根据试验设计,在基础饲粮中分别添加相应剂量的金银花、植物乳杆菌及发酵金银花,充分混匀后进行饲喂。试验期间每日08:00、12:00、16:00、20:00各饲喂1次,每次饲喂量以料槽中略有剩余为准,猪只自由采食和饮水。预试验前对试验猪进行编号,按照猪场常规程序进行免疫接种及饲养管理,每日清理漏粪地板,保证圈舍通风良好、环境干燥卫生。

1.4 样品采集与指标测定

1.4.1 饲粮营养水平

饲粮中干物质(GB/T 6435—2014)、粗蛋白质(GB/T 6432—2018)、粗脂肪(GB/T 6433—2006)、中性洗涤纤维(GB/T 20806—2022)、酸性洗涤纤维(NY/T 1459—2022)、钙(GB/T 6436—2018)和总磷(GB/T 6437—2018)含量参照国家标准或农业行业标准测定。

1.4.2 生长性能

在正试期第1天和第30天晨饲前对仔猪进行空腹称重,分别记为初重和末重,计算平均日增重(ADG);每周记录各重复的总采食量,计算平均日采食量(ADFI);并根据ADG和ADFI计算料重比(F/G)。相关计算公式如下:
ADFI=消耗饲粮总量/(试验天数×试验猪头数);
ADG=(末重-初重)/试验天数;
F/G=ADFI/ADG。

1.4.3 养分表观消化率

在正试期最后3 d,每重复随机选取1头仔猪,每日18:00采集新鲜粪便样品50 g,置于-20 ℃冷冻保存。试验结束后将每头仔猪3 d粪样充分混匀,于65 ℃烘箱烘干,置于室温条件下自然回潮24 h,粉碎后保存待测。采用盐酸不溶灰分(AIA)作为内源指示剂测定养分表观消化率。粪便中干物质、粗蛋白质和粗脂肪含量参照1.4.1中方法测定;饲粮和粪便总能参照GB/T 45104—2024进行测定,AIA含量参照GB/T 23742—2009进行测定。养分表观消化率计算公式如下:
某养分表观消化率(%)=[1-(饲粮中AIA含量×粪便中该养分含量)/(粪便中AIA含量×饲粮中该养分含量)]×100。

1.4.4 血清指标

在正试期第15天和第30天,每重复随机选取2头仔猪进行前腔静脉采血,采血量为10 mL,静置2 h后,1 095×g离心10 min分离血清备用。采用南京建成生物工程研究所生产的试剂盒测定血清总抗氧化能力(T-AOC);采用武汉基因美生物科技有限公司生产的酶联免疫吸附测定(ELISA)试剂盒测定血清免疫球蛋白G(IgG)、免疫球蛋白M(IgM)、免疫球蛋白A(IgA)、白细胞介素-4(IL-4)、白细胞介素-6(IL-6)、白细胞介素-10(IL-10)、白细胞介素-1β(IL-1β)、肿瘤坏死因子-α(TNF-α)、干扰素-γ(IFN-γ)及超氧化物歧化酶(SOD)、丙二醛(MDA)、过氧化氢酶(CAT)、谷胱甘肽过氧化物酶(GSH-Px)含量;采用武汉科前生物股份有限公司生产的ELISA试剂盒测定血清猪瘟抗体阻断率;采用兰州兽研生物科技有限公司生产的ELISA试剂盒测定血清猪口蹄疫O型抗体效价。

1.4.5 粪便短链脂肪酸(SCFAs)含量

在正试期第15天和第30天,每重复随机选取1头仔猪,采集新鲜粪便样品,置于冻存管中,投入液氮保存。粪便SCFAs含量采用气相色谱仪(7890A,Agilent,美国)测定。取粪便样品,与超纯水按照质量比1∶9混匀,每1 mL混悬液中加入200 μL 25%偏磷酸,混匀后12 879×g离心10 min,吸取上清液,经0.22 μm有机滤膜过滤后,置于进样瓶中上机检测。

1.4.6 粪便菌群分析

取1.4.5中采集的粪便样品,采用天根生化科技(北京)有限公司生产的粪便基因组DNA提取试剂盒进行DNA提取,通过1%琼脂糖凝胶电泳检测DNA的纯度和浓度。选取细菌16S rRNA基因V3~V4区为扩增区域,所用特异性引物序列为341F:5'-CCTAYGGGRBGCASCAG-3';806R:5'-GGACTACNNGGGTATCTAAT-3'。PCR反应体系:15 μL Phusion高保真PCR预混液,上、下游引物各0.2 μL,10 μL DNA模板,用ddH2O补足至30 μL。扩增程序为98 ℃预变性1 min;98 ℃变性10 s,50 ℃退火30 s,72 ℃延伸30 s,共30次循环;72 ℃终延伸5 min。PCR扩增产物经混匀、纯化处理后,送至北京诺禾致源科技股份有限公司,利用Illumina HiSeq高通量测序平台开展测序及生物信息学分析。

1.5 数据统计分析

试验数据采用SPSS 25.0软件进行统计分析,利用Levene’s对数据进行方差齐性检验,对生长性能、养分表观消化率及血清指标等数据进行单因素方差分析(one-way ANOVA),并采用Duncan氏法进行多重比较;对粪便SCFAs含量和菌群数据进行独立样本t检验,采用Pearson相关性分析评估养分表观消化率、血清免疫和抗氧化指标与粪便菌群以及血清免疫指标与抗氧化指标之间的关系。结果以平均值±标准差(mean±SD)表示,P<0.05表示差异显著,P<0.01表示差异极显著。

2 结果与分析

2.1 发酵金银花对断奶仔猪生长性能的影响

由表2可知,与CON组相比,HO组、HL组和FH组末重及ADG均显著提高(P<0.05),F/G显著降低(P<0.05),其中以FH组仔猪的生长性能最佳。
表2 发酵金银花对断奶仔猪生长性能的影响

Table 2 Effects of fermented honeysuckle on growth performance of weaned piglets

项目
Items		 组别Groups P值
P-value
CON HO HL FH
初重IBW/kg 7.45±0.09 7.48±0.09 7.46±0.24 7.44±0.27 0.999
末重FBW/kg 18.35±0.21c 19.15±0.23b 19.31±0.33ab 19.74±0.49a 0.016
平均日增重ADG/(g/d) 311.46±9.53c 333.18±7.04b 338.29±12.52ab 351.29±9.26a 0.032
平均日采食量ADFI/(g/d) 610.85±12.06 624.02±25.96 637.16±8.54 655.80±16.10 0.301
料重比F/G 1.96±0.03a 1.88±0.08b 1.90±0.06b 1.85±0.06b 0.041

同行数据肩标无字母或相同小写字母表示差异不显著(P>0.05),不同小写字母表示差异显著(P<0.05),不同大写字母表示差异极显著(P<0.01)。下表同。

In the same row, values with no letter or the same lowercase letter superscripts mean no significant difference (P>0.05), while with different lowercase letter superscripts mean significant difference (P<0.05), and with different capital letter superscripts mean extremely significant difference (P<0.01). The same as below.

2.2 发酵金银花对断奶仔猪养分表观消化率的影响

由表3可知,与CON组相比,FH组粗蛋白质表观消化率显著提高(P<0.05),总能及干物质表观消化率有所提高,但差异不显著(P>0.05),这表明发酵金银花可促进断奶仔猪对养分的消化利用。
表3 发酵金银花对断奶仔猪养分表观消化率的影响

Table 3 Effects of fermented honeysuckle on nutrient apparent digestibility of weaned piglets %

项目
Items		 组别Groups P值
P-value
CON HO HL FH
总能GE 81.14±0.27 81.20±0.37 82.03±0.32 82.55±0.65 0.080
粗蛋白质CP 76.40±0.34c 77.63±0.54bc 77.93±0.57ab 79.10±0.89a 0.037
粗脂肪EE 60.14±1.12 62.46±1.84 63.79±2.43 64.47±1.41 0.470
干物质DM 88.35±1.55 89.80±1.27 89.74±1.28 91.19±1.16 0.053

2.3 发酵金银花对断奶仔猪血清免疫指标的影响

由表4可知,试验第15天,与CON组相比,FH组血清IgM含量显著提高(P<0.05);HO组、HL组和FH组血清IL-1β和TNF-α含量极显著降低(P<0.01),血清IFN-γ含量显著降低(P<0.05),血清猪口蹄疫O型抗体效价极显著提高(P<0.01);HL组和FH组血清猪瘟抗体阻断率显著提高(P<0.05)。试验第30天,与CON组相比,FH组血清IgG、IgM和IL-10含量显著提高(P<0.05);HO组、HL组和FH组血清IL-1β含量显著降低(P<0.05),血清猪口蹄疫O型抗体效价极显著提高(P<0.01),血清猪瘟抗体阻断率显著或极显著提高(P<0.05或P<0.01)。试验第15天和第30天,与CON组相比,FH组血清猪瘟抗体阻断率和猪口蹄疫O型抗体效价提升幅度均为最大,第15天分别提高23.71%和16.15%,第30天分别提高19.39%和13.51%,表明发酵金银花可以提高断奶仔猪的免疫功能。
表4 发酵金银花对断奶仔猪血清免疫指标的影响

Table 4 Effects of fermented honeysuckle on serum immune indices of weaned piglets

项目
Items		 组别Groups P值
P-value
CON HO HL FH
第15天Day 15
免疫球蛋白A IgA/(pg/mL) 215.39±4.73 221.87±4.08 222.11±8.92 222.58±3.15 0.845
免疫球蛋白G IgG/(μg/mL) 11.31±0.22 12.27±0.96 12.33±0.29 13.36±0.12 0.085
免疫球蛋白M IgM/(ng/mL) 222.78±2.63b 224.58±4.04b 229.97±2.70ab 240.26±6.20a 0.037
白细胞介素-4 IL-4/(pg/mL) 113.94±1.70 116.82±2.34 120.67±2.59 122.85±3.32 0.104
白细胞介素-6 IL-6/(pg/mL) 40.15±0.49 39.38±0.93 39.18±1.27 37.75±0.87 0.356
白细胞介素-10 IL-10/(pg/mL) 135.82±2.01 140.66±3.10 140.73±2.66 140.79±2.69 0.482
白细胞介素-1β IL-1β/(pg/mL) 12.32±0.09Aa 10.90±0.19Bb 10.86±0.17Bb 10.48±0.15Bb 0.001
肿瘤坏死因子-α TNF-α/(pg/mL) 144.28±1.28Aa 139.43±0.71Bb 140.82±0.79Bb 135.75±1.41Cc 0.001
干扰素-γ IFN-γ/(pg/mL) 61.37±0.68a 55.02±2.18b 56.01±1.20b 53.10±1.74b 0.011
猪瘟抗体阻断率
CSF antibody blocking rate/%		 27.33±0.82c 29.01±0.27c 31.30±0.66b 33.81±0.52a 0.012
猪口蹄疫O型抗体效价
Swine FMD type O antibody titer/log2		 1.30±0.04Bb 1.41±0.03Aa 1.46±0.05Aa 1.51±0.04Aa 0.001
第30天Day 30
免疫球蛋白A IgA/(pg/mL) 203.89±7.25 199.69±10.02 203.96±7.91 198.78±6.56 0.950
免疫球蛋白G IgG/(μg/mL) 10.93±0.48b 11.74±0.34b 11.89±0.54ab 13.15±0.39a 0.022
免疫球蛋白M IgM/(ng/mL) 215.90±2.03b 216.42±4.87b 217.61±2.42b 230.20±1.78a 0.012
白细胞介素-4 IL-4/(pg/mL) 108.20±3.53 113.48±5.92 116.20±5.64 117.73±3.45 0.528
白细胞介素-6 IL-6/(pg/mL) 37.57±0.42 35.88±0.94 37.38±0.37 36.10±0.44 0.135
白细胞介素-10 IL-10/(pg/mL) 126.07±1.71b 131.56±2.81ab 130.53±1.89b 137.97±2.57a 0.017
白细胞介素-1β IL-1β/(pg/mL) 11.70±0.46a 10.61±0.18b 10.52±0.19b 10.24±0.27b 0.011
肿瘤坏死因子-α TNF-α/(pg/mL) 139.25±3.74 138.74±3.47 137.71±1.48 136.03±2.21 0.865
干扰素-γ IFN-γ/(pg/mL) 57.03±1.10 53.81±0.45 54.31±1.20 54.18±0.79 0.095
猪瘟抗体阻断率
CSF antibody blocking rate/%		 56.63±1.17Bc 59.46±0.72ABb 61.91±0.85Ab 67.61±1.10Aa 0.002
猪口蹄疫O型抗体效价
Swine FMD type O antibody titer/log2		 1.48±0.02Bb 1.61±0.03Aa 1.62±0.08Aa 1.68±0.03Aa 0.002

2.4 发酵金银花对断奶仔猪血清抗氧化指标的影响

由表5可知,与CON组相比,试验第15天HO组、HL组和FH组血清MDA含量显著降低(P<0.05),血清CAT含量显著提高(P<0.05);试验第30天HO组、HL组和FH组血清CAT含量极显著提高(P<0.01)。其中,FH组在试验第15天和第30天血清CAT含量提升幅度均为最大,分别提高10.49%和9.87%。
表5 发酵金银花对断奶仔猪血清抗氧化指标的影响

Table 5 Effects of fermented honeysuckle on serum antioxidant indices of weaned piglets

项目
Items		 组别Groups P值
P-value
CON HO HL FH
第15天Day 15
总抗氧化能力T-AOC/(mmol/L) 0.18±0.01 0.19±0.01 0.18±0.01 0.19±0.02 0.095
超氧化物歧化酶SOD/(pg/mL) 501.90±4.40 524.32±11.85 521.40±16.05 525.40±16.23 0.557
丙二醛MDA/(ng/mL) 131.42±1.10a 121.69±3.90b 119.83±3.47b 117.25±2.91b 0.024
谷胱甘肽过氧化物酶GSH-Px/(ng/mL) 4.77±0.06 4.90±0.15 4.96±0.07 4.99±0.13 0.508
过氧化氢酶CAT/(pg/mL) 729.24±9.07b 779.08±22.02a 786.00±8.54a 805.77±13.01a 0.011
第30天Day 30
总抗氧化能力T-AOC/(mmol/L) 0.14±0.01 0.19±0.22 0.18±0.04 0.19±0.05 0.068
超氧化物歧化酶SOD/(pg/mL) 537.07±14.21 542.83±17.62 543.07±14.70 543.98±20.38 0.991
丙二醛MDA/(ng/mL) 138.70±4.44 134.16±4.03 133.97±3.79 133.24±5.56 0.822
谷胱甘肽过氧化物酶GSH-Px/(ng/mL) 4.96±0.06 5.11±0.12 5.17±0.20 5.23±0.26 0.725
过氧化氢酶CAT/(pg/mL) 753.64±8.47Bb 807.76±8.99Aa 801.84±18.60Aa 828.00±13.51Aa 0.007

2.5 发酵金银花对断奶仔猪粪便SCFAs含量和菌群的影响

综合上述试验结果可知,FH组在改善断奶仔猪生长性能、免疫功能及抗氧化能力方面的效果更为突出,因此本试验选取FH组与CON组开展粪便SCFAs含量和菌群组成结构的分析。
如图1所示,试验第15天和第30天,FH组粪便总SCFAs含量均极显著高于CON组(P<0.01)。
图1 粪便总SCFAs含量

**表示差异极显著(P<0.01)。** indicated extremely significant difference (P<0.01). CON-15 d和CON-30 d分别表示试验第15天和第30天CON组的粪便样本,FH-15 d和FH-30 d分别表示试验第15天和第30天FH组的粪便样本。下图同。

Fig.1 Total SCFAs content in feces

CON-15 d and CON-30 d represented fecal samples of the CON group on day 15 and day 30 of the trial, respectively; FH-15 d and FH-30 d represented fecal samples of the FH group on day 15 and day 30 of the trial, respectively. The same as below.

如图2所示,试验第15天,2组粪便样本共获得2 349个操作分类单元(OTUs),FH组较CON组多39个OTUs;试验第30天,2组粪便样本共获得2 437个OTUs,FH组较CON组多90个OTUs。如图3所示,试验第30天,FH组粪便菌群Chao1指数和Shannon指数较CON组显著提高(P<0.05),Simpson指数无显著差异(P>0.05),表明FH组粪便菌群的丰度和多样性显著提升。主坐标分析(PCoA)结果(图3-D)显示,发酵金银花对断奶仔猪粪便菌群结构具有极显著影响(P<0.01)。
图2 粪便菌群OTUs韦恩图

Fig.2 Venn diagram of OTUs of fecal microbiota

图3 粪便菌群多样性分析

*表示差异显著(P<0.05)。

Fig.3 Diversity analysis of fecal microbiota

* indicated significant difference (P<0.05).

如图4-A所示,在门水平上,2组粪便的优势菌群均为厚壁菌门(Firmicutes)和拟杆菌门(Bacteroidota),占微生物总数的80%以上。试验第15天,与CON组相比,FH组拟杆菌门相对丰度升高;试验第30天,与CON组相比,FH组厚壁菌门相对丰度降低,拟杆菌门相对丰度升高。如图4-B所示,在属水平上,试验第30天,FH组链球菌属(Streptococcus)相对丰度高于CON组;CON组粪便优势菌群为甲烷短杆菌属(Methanobrevibacter)和狭义梭菌属1(Clostridium_sensu_stricto_1),FH组粪便优势菌群为乳杆菌属(Lactobacillus)。采用线性判别分析(LDA)效应大小(LEfSe)分析,在属水平上筛选组间差异显著的关键物种,以LDA得分≥3和P<0.05为筛选标准,结果如图4-C所示,试验第15天,CON组富集狭义梭菌属1(Clostridium_sensu_stricto_1)和乳杆菌属,FH组富集月形单胞菌属(Selenomonas)、光冈菌属(Mitsuokella)和反刍真杆菌群(Eubacterium_ruminantium_group);试验第30天,CON组富集普雷沃氏菌属(Prevotella)、富尼埃菌属(Fournierella)、罗姆布茨菌属(Romboutsia)、肠杆菌属(Intestinibacter)和氨基酸球菌属(Acidaminococcus),FH组富集狭义梭菌属6(Clostridium_sensu_stricto_6)。
图4 粪便菌群组成及差异物种分析

A:门水平粪便菌群组成;B:属水平粪便菌群组成;C:LDA得分分布直方图。A: composition of fecal microbiota at phylum level; B: composition of fecal microbiota at genus level; C: histogram of LDA score distribution.
Firmicutes:厚壁菌门;Bacteroidota:拟杆菌门;Euryarchaeota:广古菌门;Proteobacteria:变形菌门;Actinobacteriota:放线菌门;Spirochaetota:螺旋体门;Desulfobacterota:脱硫杆菌门;Cyanobacteria:蓝细菌门;Verrucomicrobiota:疣微菌门;Patescibacteria:髌骨细菌门;Others:其他;Lactobacillus:乳杆菌属;Streptococcus:链球菌属;Methanobrevibacter:甲烷短杆菌属;Clostridium_sensu_stricto_1:狭义梭菌属1;Agathobacter:阿加索杆菌属;Prevotellaceae_NK3B31_group:普雷沃氏菌科NK3B31群;Escherichia-Shigella:大肠杆菌-志贺氏菌属;Subdoligranulum:罕见小球菌属;Phascolarctobacterium:考拉杆菌属;Rikenellaceae_RC9_gut_group:理研菌科RC9肠道群;Faecalibacterium:粪杆菌属;Oscillospira:颤螺旋菌属;Lachnospiraceae_XPB1014_group:毛螺菌科XPB1014群;Christensenellaceae_R-7_group:克里斯坦森菌科R-7群;Blautia:布劳特氏菌属;Clostridium_sensu_stricto_6:狭义梭菌属6;Lachnospiraceae_NK4A136_group:毛螺菌科NK4A136群;Terrisporobacter:土孢杆菌属;Acidaminococcus:氨基酸球菌属;Romboutsia:罗姆布茨菌属;Intestinibacter:肠杆菌属;Fournierella:富尼埃菌属;Prevotella:普雷沃氏菌属;Selenomonas:月形单胞菌属;Mitsuokella:光冈菌属;Eubacterium_ruminantium_group:反刍真杆菌群。下图同 the same as below。

Fig.4 Composition of fecal microbiota and differential species analysis

2.6 相关性分析

血清免疫和抗氧化指标与粪便菌群的Pearson相关性分析结果(图5-A)表明,血清IgG、IgM、IL-10、GSH-Px和CAT含量与UCG-005相对丰度呈显著或极显著正相关(P<0.05或P<0.01);血清IL-1β和IFN-γ含量与链球菌属相对丰度呈显著或极显著负相关(P<0.05或P<0.01);血清IL-6、IL-1β和IFN-γ含量与狭义梭菌属1相对丰度呈显著或极显著正相关(P<0.05或P<0.01),而血清IgG、IgM、IL-10、CAT含量和猪口蹄疫O型抗体效价与狭义梭菌属1相对丰度呈显著或极显著负相关(P<0.05或P<0.01);血清IL-10和IL-4含量与乳杆菌属相对丰度呈显著或极显著正相关(P<0.05或P<0.01)。养分表观消化率与粪便菌群的Pearson相关性分析结果(图5-B)表明,干物质表观消化率与普雷沃氏菌科NK3B31群(Prevotellaceae_NK3B31_group)相对丰度呈显著正相关(P<0.05);总能表观消化率与罕见小球菌属(Subdoligranulum)相对丰度呈显著负相关(P<0.05);粗蛋白质表观消化率与UCG-005相对丰度呈极显著正相关(P<0.01)。上述结果提示,养分表观消化率的提升、机体免疫功能与抗氧化能力的增强均与粪便菌群结构变化密切相关。
图5 血清免疫和抗氧化指标(A)及养分表观消化率(B)与粪便菌群的相关性分析

*表示显著相关(P<0.05),**表示极显著相关(P<0.01)。* indicated significant correlation (P<0.05), and ** indicated extremely significant correlation (P<0.01).
IgG:免疫球蛋白G immunoglobulin G;IgM:免疫球蛋白M immunoglobulin M;IgA:免疫球蛋白A immunoglobulin A;IL-10:白细胞介素-10 interleukin-10;IL-4:白细胞介素-4 interleukin-4;IL-6:白细胞介素-6 interleukin-6;IL-1β:白细胞介素-1β interleukin-1β;TNF-α:肿瘤坏死因子-α tumor necrosis factor-α;IFN-γ:干扰素-γ interferon-γ;MDA:丙二醛 malondialdehyde;GSH-Px:谷胱甘肽过氧化物酶 glutathione peroxidase;CAT:过氧化氢酶 catalase;SOD:超氧化物歧化酶 superoxide dismutase;T-AOC:总抗氧化能力 total antioxidant capacity;猪瘟抗体阻断率:classical swine fever antibody blocking rate;猪口蹄疫O型抗体效价:swine foot-and-mouth disease type O antibody titer;CP:粗蛋白质 crude protein;GE:总能 gross energy;DM:干物质 dry matter。下图同 the same as below。

Fig.5 Correlation analysis of serum immune and antioxidant indices (A) and nutrient apparent digestibility (B) with fecal microbiota

血清免疫指标与抗氧化指标的Pearson相关性分析结果(图6)表明,血清IgM含量与IgA、IL-10、IL-4含量呈显著或极显著正相关(P<0.05或P<0.01);血清IL-10含量与IL-4含量及T-AOC呈极显著正相关(P<0.01);血清IL-4含量与CAT含量及T-AOC呈显著或极显著正相关(P<0.05或P<0.01);血清IL-6含量与IL-1β、IFN-γ含量呈显著正相关(P<0.05),与MDA、CAT、SOD含量呈显著负相关(P<0.05);血清IL-1β含量与IFN-γ含量呈极显著正相关(P<0.01),与GSH-Px、CAT含量呈显著或极显著负相关(P<0.05或P<0.01)。上述结果提示,机体免疫功能的改善与抗氧化能力的提升存在密切关联。
图6 血清免疫指标与抗氧化指标的相关性分析

Fig.6 Correlation analysis between serum immune indices and antioxidant indices

3 讨论

3.1 发酵金银花对断奶仔猪生长性能和养分表观消化率的影响

生长性能是评估动物营养状态最直接、最有价值的指标。有研究指出,在动物饲粮中添加金银花可有效改善其生长性能。Li等[10]研究表明,饲粮中添加金银花提取物可显著提高肉鹅的ADG,显著降低F/G;黄毅等[11]发现,饲喂金银花发酵饲料可提高热应激肉鸭的ADG和ADFI;王曼等[12]在育肥猪饲粮中添加发酵金银花渣,结果显示试验组ADG与ADFI较对照组显著提高。本研究中,与CON组相比,HO组、HL组和FH组仔猪末重和ADG均显著升高,F/G显著降低,且FH组改善效果最优。推测其原因可能在于,发酵金银花并非金银花与乳酸菌的简单混合,发酵过程中乳酸菌产生的纤维素酶等胞外酶可破坏金银花细胞壁结构,促进绿原酸、黄酮类等活性物质释放溶出,提高其生物利用度[13-14];同时,发酵过程中产生的有机酸、酶解产物及微生物代谢物,与金银花原有活性成分形成协同效应,共同促进断奶仔猪的生长发育。
养分表观消化率是衡量动物消化功能和饲料营养价值的重要指标之一。研究表明,在育肥猪饲粮中添加0.5%金银花和0.5%葛根提取物,可显著提高粗蛋白质和磷的表观消化率[15]。本研究中,FH组粗蛋白质表观消化率显著高于CON组,推测是由于在乳酸菌发酵过程中,会产生大量酶类及有机酸,可将金银花中大分子物质降解为小分子活性成分,更易被仔猪肠道吸收利用,进而提升肠道上皮细胞对粗蛋白质的消化吸收能力[6]。但其具体调控机制,仍需进一步深入研究。

3.2 发酵金银花对断奶仔猪免疫功能的影响

断奶仔猪免疫防御系统尚未发育完善,易患各种炎症性疾病,进而导致仔猪死亡,降低养殖经济效益。IgG、IgM和IgA是动物机体重要的免疫球蛋白,其在血清中的含量可以反映机体的抗病能力;白细胞介素、干扰素等细胞因子主要由免疫细胞合成并分泌,参与机体炎症反应调控,而过度的炎症反应会对动物机体造成损伤[16]。已有研究证实,金银花具有提升动物免疫力的作用。Wang等[17]发现,母猪妊娠晚期及哺乳期补充金银花与黄芩提取物,可显著增加乳汁中IL-10、IgA及IgG含量;在蛋鸡饲粮中添加金银花,可显著降低输卵管中IL-6、IL-1β、TNF-α和IFN-γ的mRNA表达量[18]。在水产动物中,金银花也被广泛用于提升机体免疫活性[19]。此外,金银花对热应激奶牛血液中的炎症因子含量也有改善作用[20]。本研究中,试验第15天和第30天时,HO组、HL组和FH组血清IgG和IgM含量均较CON组有不同程度提升,其中FH组提升效果最为明显,表明发酵金银花可有效增强断奶仔猪的特异性免疫功能。
口蹄疫病毒(foot-and-mouth disease virus,FMDV)和猪瘟病毒(classical swine fever virus,CSFV)是养猪业面临的2种重要病毒性病原,具有急性、高发病率和广泛传播性等特点;患病猪常伴随异常的促炎反应,即“细胞因子风暴”[21-22]。金银花作为一种药食同源的天然植物,具有抗菌、抗病毒的作用[23],且FMDV的衣壳在pH低于6.5的环境中会解离成独立五聚体亚单位[24]。因此,发酵金银花在CSFV和FMDV防御方面具有潜在应用价值,而现阶段有关金银花及发酵金银花调控机体抵御FMDV、CSFV的相关研究较为匮乏。本研究中,试验第15天和第30天时,HO组、HL组和FH组血清猪口蹄疫O型抗体效价和猪瘟抗体阻断率均较CON组有不同程度升高,其中FH组效果最优。究其原因,在于发酵金银花融合了金银花的天然抗炎抑菌功效与植物乳杆菌的生理作用,其酸性环境可能促使FMDV衣壳解离。该结果也表明,在仔猪免疫接种阶段,饲粮添加金银花或发酵金银花均可正向促进机体免疫应答,且发酵金银花的应用效果更具优势。

3.3 发酵金银花对断奶仔猪抗氧化能力的影响

仔猪断奶初期易受母仔分离、环境改变及营养水平变化等因素影响,产生氧化应激,进而导致腹泻、患病甚至死亡[25]。仔猪体内存在内源性抗氧化系统,主要由SOD、CAT、GSH-Px等酶类构成。其中,SOD可催化超氧化物阴离子自由基转化为氧气(O2)与过氧化氢(H2O2);产生的H2O2在CAT的催化下进一步分解为水(H2O)和O2;GSH-Px作为重要的抗氧化酶,能够催化谷胱甘肽还原H2O2及有机氢过氧化物,生成相应的醇和H2O,从而保护细胞免受氧化应激的损伤[26]。研究表明,饲粮中添加金银花提取物可提高育肥猪血清中GSH-Px活性[27];在热应激奶牛饲粮中添加金银花提取物后,其血清中T-AOC和SOD活性显著提高[20,28];Liu等[18]将金银花提取物添加到蛋鸡饲粮中,发现输卵管中CAT和GSH-Px的mRNA表达量显著上调,MDA的mRNA表达量显著下调。本研究结果表明,与CON组相比,HO组、HL组及FH组在试验第15天和第30天的血清CAT含量均显著或极显著升高,且第15天血清MDA含量显著降低,推测这可能是由于金银花中所含的绿原酸、原儿茶酸、芦丁、马钱苷等功能成分发挥了抗氧化作用;进一步分析发现,FH组在第15天和第30天的血清CAT含量均高于HO组与HL组,推测可能是发酵过程改变了微生物群落组成及金银花的代谢产物[29-30],增加了有机酸、菌群、酶等功能成分,从而增强了金银花的抗氧化功能。

3.4 发酵金银花对断奶仔猪粪便菌群的影响

肠道健康状况是评判动物机体健康水平的重要依据,而肠道菌群与肠道健康密切相关。厚壁菌门与拟杆菌门为动物肠道中的核心优势菌群。在哺乳动物体内,拟杆菌门可参与机体免疫调节,还能为肠道内其他微生物供给营养物质[31]。本研究发现,断奶仔猪粪便中厚壁菌门和拟杆菌门占微生物总数的80%以上;试验第15天和第30天,FH组断奶仔猪粪便拟杆菌门相对丰度均高于CON组,该变化规律与发酵金银花提升仔猪免疫功能、改善养分表观消化率的试验结果相互印证。α多样性指数常用来评估单一样本内微生物群落物种丰富度与多样性,β多样性则可反映组间微生物群落结构的整体差异。试验第30天,FH组仔猪粪便菌群Chao1指数与Shannon指数均显著高于CON组,说明饲粮中添加发酵金银花能够有效提升断奶仔猪粪便微生物群落丰富度与多样性。基于PCoA结果可知,CON组与FH组粪便菌群结构区分明显,证实发酵金银花可显著调控断奶仔猪肠道菌群组成,这与Liu等[15]的研究结果相似。
月形单胞菌属、光冈菌属在维护肠道黏膜完整性、促进营养物质吸收及维持机体能量稳态中发挥重要作用[32-33]。Mahmud等[34]研究发现,生长性能优良的高增重仔猪直肠粪便中光冈菌属相对丰度显著升高,该菌属可促进小肠上皮细胞生长与增殖,进而改善仔猪肠道健康。反刍真杆菌群可降解饲粮中碳水化合物,并产生提供能量和维护肠道健康的SCFAs[35]。狭义梭菌属1作为典型有害菌,其相对丰度升高与动物肠道炎症及发病程度密切相关[36]。本研究结果表明,FH组粪便总SCFAs含量极显著高于CON组;在发酵金银花的干预下,断奶仔猪粪便微生物部分有益菌属(月形单胞菌属、光冈菌属、反刍真杆菌群)的相对丰度增加,同时狭义梭菌属1等有害菌相对丰度降低。综上可知,饲粮添加发酵金银花可通过富集肠道有益菌、抑制有害菌增殖的方式,改善断奶仔猪肠道微生态环境,进而保障仔猪机体健康,但其调控肠道菌群的具体分子作用机制仍有待进一步探究。

3.5 养分表观消化率、血清免疫和抗氧化指标与粪便菌群间的相关性分析

Pearson相关性分析结果表明,断奶仔猪粪便中UCG-005、链球菌属、狭义梭菌属1和乳杆菌属的相对丰度与养分消化、免疫及抗氧化等多项指标具有相关性,提示发酵金银花可能通过调节肠道菌群,进而促进养分消化、提升机体免疫及抗氧化性能。UCG-005是肠道内参与SCFAs合成的重要菌属,主要富集于盲肠、结肠等远端肠道组织。Tang等[37]报道,UCG-005相对丰度与仔猪体重、ADG呈显著正相关;Song等[38]研究发现,UCG-005相对丰度与肠道内容物游离总氨基酸含量呈负相关,这与本研究中UCG-005相对丰度与粗蛋白质表观消化率呈正相关的研究结果相符,推测发酵金银花提高蛋白质消化率的机制可能是UCG-005增强了黏液层的厚度与质量,维护了肠道内环境稳态。本研究发现,断奶仔猪粪便狭义梭菌属1的相对丰度与血清免疫球蛋白(IgG、IgM)、CAT含量及猪口蹄疫O型抗体效价呈负相关,而与炎症因子IL-6、IL-1β和IFN-γ含量呈正相关,进一步证实该菌属相对丰度升高易诱发肠道炎症,抑制机体免疫与抗氧化性能。本研究还发现,断奶仔猪粪便普雷沃氏菌科NK3B31群相对丰度与干物质表观消化率呈显著正相关,推测可能是该菌属参与碳水化合物、氨基酸、脂质和核苷酸等代谢途径,促进饲粮大分子向能源载体SCFAs的转化[39],使动物摄入的干物质更有效转化为可吸收的能量,提高干物质的表观消化率。本研究结果显示,断奶仔猪粪便罕见小球菌属相对丰度与总能表观消化率呈显著负相关,这与Liu等[40]的研究结果相似。此外,本研究还发现,机体免疫功能的提升与抗氧化能力的增强密切相关,这一关联可能与体内自由基代谢平衡机制有关[41]。发酵金银花富含绿原酸、原儿茶酸、芦丁、马钱苷等多种天然抗氧化活性成分,可通过清除体内过量自由基提升机体抗氧化能力,而抗氧化能力的增强又可能间接促进机体免疫功能的改善。但目前关于发酵金银花调控断奶仔猪生长性能、增强机体免疫力的深层作用机制,仍有待进一步探究。

4 结论

饲粮中添加发酵金银花可有效改善断奶仔猪生长性能,提升养分表观消化率,增强机体抗氧化能力与免疫功能,提高猪瘟抗体阻断率及猪口蹄疫O型抗体效价;同时,还可优化肠道菌群结构,富集有益菌、抑制有害菌生长,通过调控肠道微生态与提升抗氧化能力共同维护仔猪机体健康。与单独添加金银花或金银花配伍植物乳杆菌相比,发酵金银花在促进断奶仔猪增重、提高粗蛋白质表观消化率及增强机体免疫功能等方面效果更优。

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