Chinese Journal of Animal Nutrition >

2024 , Vol. 36 >Issue 9: 5630 - 5641

DOI: https://doi.org/10.12418/CJAN2024.480

RESEARCH PAPER

Effects of Isochlorogenic Acid on Growth Performance, Nutrient Apparent Metabolic Rates of Broilers and Antioxidant Capacity of Broilers under Lipopolysaccharide Stress

  • JIANG Haotian , 1 ,
  • ZHOU Siyuan 1 ,
  • WANG Yujia 1 ,
  • ZHAO Ziyin 1 ,
  • WEI Xu 1 ,
  • YAN An 1 ,
  • LIU Guohua 2 ,
  • LIU Shudong , 1, * ,
  • CHEN Baojiang , 1, *
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  • 1 College of Animal Science and Technology, Hebei Agricultural University, Baoding 071001, China
  • 2 Feed Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100080, China
* LIU Shudong, lecturer, E-mail: ;
CHEN Baojiang, professor, E-mail:

Received date: 2024-03-20

  Online published: 2024-09-08

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Abstract

This experiment was conducted to study the effects of isochlorogenic acid (ICGA) on the growth performance, nutrient apparent metabolic rates of broilers, as well as the antioxidant capacity of broilers challenged by lipopolysaccharide (LPS). A total of 320 one-day-old healthy Cobb broilers with similar body weight were selected according to a 2×2 two-factor experimental design (with or without ICGA intervention; with or without LPS-induced) were randomly divided into 4 groups: CON group, L-CON group, ICGA group and L-ICGA group. Each group had 8 replicates, with 10 broilers in each replicate. Broilers in the CON group and L-CON group were fed a basal diet, while those in the ICGA group and L-ICGA group were fed the basal diet supplemented with 2 000 mg/kg of ICGA. At 42 days of age, broilers in L-CON group and L-ICGA group were injected with LPS at 200 μg/kg BW in breast muscle, and broilers in the CON group and ICGA group were injected with the same amount of normal saline. The antioxidant indexes were measured by sampling 2 hours after the injection. The results showed as follows: 1) diet supplemented with ICGA significantly increased the average daily gain and final body weight of broilers (P<0.05), and significantly reduced the feed to gain ratio of broilers (P<0.05); 2) diet supplemented with ICGA significantly increased the apparent metabolic rates of crude protein and calcium of broilers (P<0.05); 3) diet supplemented with ICGA could reverse the increase of serum alanine aminotransferase and alkaline phosphatase activity caused by LPS challenge (P<0.05), at the same time, the content of serum high density lipoprotein cholesterol was significantly increased (P<0.05); 4) diet supplemented with ICGA could significantly up-regulate the mRNA relative expression levels of superoxide dismutase-1 and glutathione catalase in ileum (P<0.05), significantly increase the superoxide dismutase activity in serum, ileum and liver and the activity of glutathione catalase in serum and ileum (P<0.05), and significantly decrease the content of malondialdehyde in serum and ileum of broilers challenged by LPS (P<0.05). In summary, ICGA can improve the growth performance and the apparent metabolic rates of crude protein and calcium of broilers, and can respond to LPS-induced oxidative stress by regulating serum lipid metabolism, upregulating antioxidant gene expression, increasing antioxidant enzyme activities, and reducing lipid peroxide products.

Key words： isochlorogenic acid; broilers; lipopolysaccharide; growth performance; apparent metabolic rate; antioxidant capacity

Cite this article

JIANG Haotian , ZHOU Siyuan , WANG Yujia , ZHAO Ziyin , WEI Xu , YAN An , LIU Guohua , LIU Shudong , CHEN Baojiang . Effects of Isochlorogenic Acid on Growth Performance, Nutrient Apparent Metabolic Rates of Broilers and Antioxidant Capacity of Broilers under Lipopolysaccharide Stress[J]. Chinese Journal of Animal Nutrition, 2024 , 36(9) : 5630 -5641 . DOI: 10.12418/CJAN2024.480

在集约化养殖过程中,高饲养密度、饲粮加工工艺缺陷以及环境中外源致病菌的影响等都会造成畜禽肠道内环境失衡,引发机体应激反应。脂多糖(LPS)又称内毒素,是大多数革兰氏阴性菌外膜的组成部分之一,在保护细菌免受应激、机体产生免疫反应等过程中起着重要作用[1]。在健康状态下,LPS不会进入血液循环,但当机体发生应激反应时,肠道内微生物平衡被破坏,细菌死亡或发生裂解,LPS被释放出来,并与宿主细胞相互作用,释放出炎症因子,积累氧自由基,对机体造成损害[2]。在我国饲料行业抗生素禁用、限用的政策下,寻找安全有效的抗生素替代品来预防或减缓肉鸡氧化应激损伤具有重要的现实意义。
甜叶菊自引种栽培成功以来,在我国被广泛种植。但是伴随甜叶菊的大量种植和有效成分的提取,产生了大量的甜叶菊废渣,将甜叶菊废渣简单堆积、燃烧、填埋处理会对环境造成严重污染[3]。有报道称,甜叶菊废渣中含有多种酚酸类物质,如绿原酸(CGA)、异绿原酸(ICGA)等,具有清除自由基、抗菌消炎等多种生物活性[4]。CGA是一种由奎宁酸和咖啡酸产生的酚酸,其中的酚环和羟基使其具有多种生物活性,如抗炎、抗氧化和免疫调节等[5-6]。然而,CGA化学性质不稳定,在脂肪中的溶解度有限,生物利用度差,易被酯酶降解[7]。ICGA作为比CGA多了1个咖啡基的异构体,具有更稳定的结构,抗菌、抗炎、抗氧化等效果更明显[8]。ICGA可从植物、水果、蔬菜、咖啡等渠道提取,在医学、药学、动物学等研究领域都具有广泛的应用价值。实际生产中,经常在饲粮中添加酸化剂以改善畜禽肠道健康,从调节肠道pH、提高抗氧化能力、调节肠道微生态平衡等方面来提升动物的生产性能,增加经济效益[9-10]。ICGA作为一种有机酸化剂,目前的研究大多集中在生物学和药代动力学方面[11],动物试验主要集中在小鼠模型上[12-13],在畜牧生产比如肉鸡上的研究较少。因此,本研究主要探讨甜叶菊残渣提取物ICGA对肉鸡生长性能以及LPS诱导的氧化应激状态下抗氧化能力的影响,以期为ICGA在肉鸡饲粮中的合理利用以及拓宽甜叶菊产业链提供参考和依据。

1 材料与方法

1.1 试验材料

试验用ICGA来源于甜叶菊废渣,纯度≥55%,为市售产品;LPS(血清型O55∶B5,L2880)来源于大肠杆菌,购自Sigma公司。

1.2 试验设计

选取健康、体重[(44.20±0.16) g]相近的1日龄科宝肉雏鸡320只,采用2×2双因素试验设计(因素1:有或无ICGA干预;因素2:有或无LPS处理)随机分为4组,分别为CON组、L-CON组、ICGA组、L-ICGA组,每组8个重复,每个重复10只(公母各占1/2)。其中,CON组和L-CON组饲喂基础饲粮,ICGA组和L-ICGA组在基础饲粮的基础上添加2 000 mg/kg的ICGA,ICGA的添加剂量是采用的预试验确定的最佳剂量。L-CON组和L-ICGA组肉鸡在42日龄时胸肌注射200 μg/kg BW LPS,CON组和ICGA组注射等量生理盐水。LPS的给药方法和剂量参照前人的报道[14-15]。

1.3 基础饲粮及饲养管理

基础饲粮参考《鸡饲养标准》(NY/T 33—2004)中肉鸡营养需求配制而成,其组成及营养水平见表1。整个试验在冬季进行,采用笼养法,试验期间参考《现代肉鸡生产手册》进行人为温湿度控制,保证鸡舍干净,且有良好的空气流通与充足的光照,保证饲粮、饮水充足,并将鸡只按照正常免疫程序进行免疫接种。
表1 基础饲粮组成及营养水平(干物质基础)

Table 1 Composition and nutrient levels of basal diets (DM basis) %

项目
Items		 含量Content
1~21日龄
1 to 21
days of age		 22~42日龄
22 to 42
days of age
原料Ingredients
玉米Corn 48.20 51.45
豆粕Soybean meal 41.80 36.50
豆油Soybean oil 5.00 7.05
预混料Premix1) 5.00 5.00
合计Total 100.00 100.00
营养水平Nutrient levels2)
代谢能ME/(MJ/kg) 12.71 13.31
粗蛋白质CP 21.04 20.18
钙Ca 0.85 0.75
总磷TP 0.65 0.55
总能GE/(MJ/kg) 19.48 19.70
赖氨酸Lys 1.59 1.45
可消化赖氨酸D-Lys 1.45 1.33
蛋氨酸Met 0.60 0.57
可消化蛋氨酸D-Met 0.57 0.54
苏氨酸Thr 1.00 0.92
可消化苏氨酸D-Thr 0.87 0.80
胱氨酸Cys 0.34 0.31
可消化胱氨酸D-Cys 0.28 0.26
色氨酸Trp 0.27 0.24
可消化色氨酸D-Trp 0.24 0.21

1)5%预混料含1.5%的石粉、1.5%的磷酸氢钙、0.5%的食盐和1.5%的多维多矿和氨基酸,多维多矿为每千克饲粮提供 The 5% premix contained 1.5% limestone, 1.5% CaHPO4, 0.5% NaCl and 1.5% multi-vitamins & minerals, and multi-vitamins & minerals provided the following per kilogram of diets:VA 750 IU,VD3 3 000 IU,VE 20 IU,VK3 2 mg,VB1 2 mg,VB2 6 mg,VB6 3 mg,VB12 0.02 mg,泛酸钙 calcium pantothenate 10 mg,烟酰胺 nicotinamide 40 mg,生物素 biotin 0.12 mg,Cu 10 mg,Fe 20 mg,Zn 80 mg,Mn 90 mg,Se 0.2 mg,I 1 mg。

2)代谢能、氨基酸与可消化氨基酸依据NY/T 33—2004计算得出,粗蛋白质、钙、总磷和总能为实测值。ME, amino acids and digestible amino acids were calculated based on the NY/T 33—2004, while CP, Ca, TP and GE were measured values.

1.4 样品采集

在试验第42天屠宰前12 h内禁止采食。在注射LPS和生理盐水2 h后从每个重复中随机抽取1只鸡,每组8只(n=8),翅下静脉采血,静置1 h后以630×g离心10 min,取上清液于离心管中,-20 ℃冰箱保存待测。采血结束后将肉鸡进行屠宰,取适量肝脏和回肠组织样本于冻存管中,液氮速冻后放置在-80 ℃冰箱保存待测。

1.5 检测指标与方法

1.5.1 生长性能

记录试验期间的采食量,并于试验第1天和第42天记录各组鸡的体重。试验期间如有鸡只死亡,则立即称余料量和死亡鸡只重,并记录数据,以消除死亡鸡只对试验结果的影响。根据记录的数据计算各组鸡的平均日采食量(ADFI)、平均日增重(ADG)和料重比(F/G)。

1.5.2 营养物质表观代谢率

在40~42日龄,采用内源指示剂法进行为期3 d的消化代谢试验。收集肉鸡新鲜粪便,从粪便中去除羽毛、皮屑、灰尘等颗粒后将收集的粪便分为2份,一份添加10%盐酸固氮,用于测定粗蛋白质(CP)含量,另一份用于测定其他养分含量。参照AOAC(2005)[16]的方法对饲粮和粪样中的干物质(DM)、CP、钙(Ca)、总磷(TP)含量和总能(GE)进行测定,并参照Wu等[17]的方法计算营养物质表观代谢率。

1.5.3 血清生化指标

将血清样品从-20 ℃冰箱取出,室温解冻后采用江苏酶免实业有限公司生产的酶联免疫吸附测定(ELISA)试剂盒测定血清谷丙转氨酶(ALT)、谷草转氨酶(AST)、碱性磷酸酶(AKP)活性以及低密度脂蛋白胆固醇(LDL-C)、高密度脂蛋白胆固醇(HDL-C)含量,具体操作按照说明书步骤进行。

1.5.4 血清、肝脏、回肠抗氧化指标

将肝脏和回肠样品从-80 ℃冰箱取出后,使用分析天平称取适量的肝脏或回肠样品于2 mL的EP管中,按照1∶9的比例加入生理盐水后低温研磨,制成10%的组织匀浆。将血清样品从-20 ℃冰箱取出,室温解冻。采用江苏酶免实业有限公司生产的ELISA试剂盒测定血清、肝脏、回肠的总抗氧化能力(T-AOC)以及谷胱甘肽过氧化物酶(GSH-Px)、过氧化氢酶(CAT)、超氧化物歧化酶(SOD)活性和丙二醛(MDA)含量,具体操作按照说明书步骤进行。

1.5.5 回肠抗氧化相关基因mRNA相对表达量

从-80 ℃冰箱中取出回肠样品,送至上海派森诺生物技术有限公司采用实时荧光定量PCR(qRT-PCR)方法检测回肠中SOD-1和GSH-Px的mRNA相对表达量。本研究使用的引物如表2所示,以肌动蛋白(actin)作为内参基因,引物序列来自国家生物技术信息中心(NCBI)。
表2 实时荧光定量PCR引物序列

Table 2 Sequence of primers for real-time qRT-PCR

基因名称
Gene names		 引物序列
Primer sequences (5'—3')		 GenBank登录号
GenBank accession No.
肌动蛋白Actin F:CTTCCAGCCATCTTTCTT
R:ATATCCACATCACACTTCAT		 ENSGALG00010021232
超氧化物歧化酶-1 SOD-1 F:TTCTGTCATTTCTCTTAC
R:TAGTTTGCTCTCATTATC		 ENSGALG00010011746
谷胱甘肽过氧化物酶GSH-Px F:GATGAGATCCTGAGAGTGGTGGAC
R:TCATCAGGTAAGGTGGGCACAA		 NM_000581.4

1.6 数据统计与分析

试验数据通过SPSS 26.0软件进行分析,其中生长性能和营养物质表观代谢率数据采用独立样本t检验分析组间差异显著性,其余指标采用一般线性模型(GLM)程序进行双因素方差分析,模型主效应包括LPS、ICGA及两者的互作效应。当互作效应显著时,使用Duncan氏法进行组间多重比较。数据以平均值和均值标准误表示。以P<0.05表示差异显著,P>0.05表示差异不显著。

2 结果与分析

2.1 饲粮中添加ICGA对肉鸡生长性能的影响

如表3所示,与CON组相比,肉鸡饲喂添加了ICGA的饲粮后的末重(42日龄体重)和ADG显著提高(P<0.05),F/G显著降低(P<0.05)。
表3 饲粮中添加ICGA对肉鸡生长性能的影响

Table 3 Effects of dietary ICGA supplementation on growth performance of broilers

项目
Items		 组别Groups 均值标准误
SEM		 P值
P-value
CON ICGA
末重FBW/kg 2.01 2.10 0.022 0.003
平均日采食量ADFI/(g/d) 80.62 78.04 2.211 0.265
平均日增重ADG/(g/d) 49.25 51.32 0.552 0.003
料重比F/G 1.64 1.52 0.457 0.026

2.2 饲粮中添加ICGA对肉鸡营养物质表观代谢率的影响

如表4所示,与CON组相比,肉鸡饲喂添加了ICGA的饲粮后CP、Ca表观代谢率显著提高(P<0.05)。
表4 饲粮中添加ICGA对肉鸡营养物质表观代谢率的影响

Table 4 Effects of dietary ICGA supplementation on nutrient apparent metabolic rates of broilers %

项目
Items		 组别Groups 均值标准误
SEM		 P值
P-value
CON ICGA
粗蛋白质CP 63.09 65.63 0.957 0.021
钙Ca 61.72 64.82 0.522 <0.001
总磷TP 63.45 63.62 0.157 0.299
总能GE 64.45 63.62 0.423 0.059
干物质DM 60.84 60.94 0.074 0.201

2.3 饲粮中添加ICGA对LPS刺激肉鸡血清生化指标的影响

饲粮中添加ICGA对LPS刺激肉鸡血清生化指标的影响见表5。双因素方差分析结果显示:LPS刺激显著增加了血清ALT、AKP活性(P<0.05),显著降低了血清HDL-C含量(P<0.05);饲粮中添加ICGA能够显著降低血清ALT、AKP活性(P<0.05),显著增加血清HDL-C含量(P<0.05);饲粮中添加ICGA与LPS刺激对血清ALT和AKP活性和HDL-C含量存在显著的互作效应(P<0.05)。组间多重比较结果显示:非应激状态下,与CON组相比,ICGA组的血清生化指标无显著差异(P>0.05);应激状态下,与L-CON组相比,L-ICGA组的血清ALT和AKP活性显著降低(P<0.05),血清HDL-C含量显著升高(P<0.05)。
表5 饲粮中添加ICGA对LPS刺激肉鸡血清生化指标的影响

Table 5 Effects of dietary ICGA supplementation on serum biochemical indices of broilers challenged by LPS

项目
Items		 组别Groups 均值
标准误
SEM		 P值P-value
CON L-CON ICGA L-ICGA 脂多糖
LPS		 异绿原酸
ICGA		 互作效应
Interaction
谷丙转氨酶ALT/(U/L) 2.32bc 2.61a 2.27c 2.42b 0.033 <0.001 0.001 0.048
谷草转氨酶AST/(U/L) 352.54 357.82 347.42 352.39 2.692 0.069 0.062 0.953
碱性磷酸酶AKP/(U/L) 452.92b 460.11a 450.85b 451.60b 1.515 0.015 0.002 0.044
低密度脂蛋白胆固醇
LDL-C/(mmol/L)		 0.94 0.96 0.90 0.93 0.023 0.248 0.148 0.758
高密度脂蛋白胆固醇
HDL-C/(mmol/L)		 2.48a 2.36c 2.51a 2.45b 0.013 <0.001 <0.001 0.016

同行数据肩标不同小写字母表示差异显著(P<0.05),无字母或有相同字母表示差异不显著(P>0.05)。下表同。

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

2.4 饲粮中添加ICGA对LPS刺激肉鸡血清抗氧化指标的影响

饲粮中添加ICGA对LPS刺激肉鸡血清抗氧化指标的影响见表6。双因素方差分析结果显示:LPS刺激显著降低了血清SOD、GSH-Px、CAT活性和T-AOC(P<0.05),显著增加了血清MDA含量(P<0.05);饲粮中添加ICGA能够显著增加血清SOD、GSH-Px、CAT活性及T-AOC(P<0.05),显著降低血清MDA含量(P<0.05);饲粮中添加ICGA与LPS刺激对血清SOD、GSH-Px活性和MDA含量存在显著的互作效应(P<0.05)。组间多重比较结果显示:非应激状态下,与CON组相比,ICGA组血清SOD活性显著提高(P<0.05);应激状态下,与L-CON组相比,L-ICGA组血清SOD和GSH-Px活性显著提高(P<0.05),血清MDA含量显著降低(P<0.05)。
表6 饲粮中添加ICGA对LPS刺激肉鸡血清抗氧化指标的影响

Table 6 Effects of dietary ICGA supplementation on serum antioxidant indices of broilers challenged by LPS

项目
Items		 组别Groups 均值
标准误
SEM		 P值P-value
CON L-CON ICGA L-ICGA 脂多糖
LPS		 异绿原酸
ICGA		 互作效应
Interaction
超氧化物歧化酶
SOD/(U/mL)		 194.04b 146.39c 214.46a 191.14b 5.648 <0.001 <0.001 0.041
谷胱甘肽过氧化物酶
GSH-Px/(U/mL)		 223.62a 138.79b 231.52a 201.53a 9.788 <0.001 0.001 0.010
过氧化氢酶CAT/(U/mL) 67.23 59.51 79.53 65.43 1.633 <0.001 <0.001 0.062
总抗氧化能力T-AOC/(U/mL) 0.80 0.70 1.02 0.88 0.056 0.037 0.002 0.682
丙二醛MDA/(nmol/mL) 6.25b 8.33a 6.24b 6.42b 0.354 0.004 0.012 0.013

2.5 饲粮中添加ICGA对LPS刺激肉鸡肝脏抗氧化指标的影响

饲粮中添加ICGA对LPS刺激肉鸡肝脏抗氧化指标的影响见表7。双因素方差分析结果显示:LPS刺激显著降低了肝脏SOD、GSH-Px、CAT活性及T-AOC(P<0.05);饲粮中添加ICGA能够显著增加肝脏SOD、GSH-Px活性及T-AOC(P<0.05),显著降低肝脏MDA含量(P<0.05);饲粮中添加ICGA与LPS刺激对肝脏GSH-Px活性存在显著的互作效应(P<0.05)。组间多重比较结果显示:非应激状态下,与CON组相比,ICGA组肝脏GSH-Px活性显著提高(P<0.05);应激状态下,与L-CON组相比,L-ICGA组肝脏GSH-Px活性显著提高(P<0.05)。
表7 饲粮中添加ICGA对LPS刺激肉鸡肝脏抗氧化指标的影响

Table 7 Effects of dietary ICGA supplementation on liver antioxidant indices of broilers challenged by LPS

项目
Items		 组别Groups 均值
标准误
SEM		 P值P-value
CON L-CON ICGA L-ICGA 脂多糖
LPS		 异绿原酸
ICGA		 互作效应
Interaction
超氧化物歧化酶
SOD/(U/mg prot)		 11.84 8.06 12.72 10.55 0.474 <0.001 0.002 0.101
谷胱甘肽过氧化物酶
GSH-Px/(U/mg prot)		 10.67b 8.43c 12.99a 12.25a 0.360 <0.001 <0.001 0.049
过氧化氢酶CAT/(U/mg prot) 4.95 3.93 5.29 4.10 0.230 <0.001 0.273 0.719
总抗氧化能力
T-AOC/(U/mg prot)		 0.11 0.09 0.13 0.11 0.008 0.005 0.018 0.729
丙二醛MDA/(nmol/mg prot) 0.52 0.58 0.45 0.48 0.039 0.229 0.033 0.637

2.6 饲粮中添加ICGA对LPS刺激肉鸡回肠抗氧化指标的影响

饲粮中添加ICGA对LPS刺激肉鸡回肠抗氧化指标的影响见表8。双因素方差分析结果显示:LPS刺激显著降低了回肠SOD、GSH-Px、CAT活性及T-AOC(P<0.05),显著增加了回肠MDA含量(P<0.05);饲粮中添加ICGA能够显著增加回肠SOD、GSH-Px、CAT活性及T-AOC(P<0.05),显著降低回肠MDA含量(P<0.05);饲粮中添加ICGA与LPS刺激对回肠SOD、GSH-Px活性和MDA含量存在显著的互作效应(P<0.05)。组间多重比较结果显示:非应激状态下,与CON组相比,ICGA组回肠SOD和GSH-Px活性显著提高(P<0.05),回肠MDA含量显著降低(P<0.05);应激状态下,与L-CON组相比,L-ICGA组回肠SOD和GSH-Px活性显著提高(P<0.05),回肠MDA含量显著降低(P<0.05)。
表8 饲粮中添加ICGA对LPS刺激肉鸡回肠抗氧化指标的影响

Table 8 Effects of dietary ICGA supplementation on ileal antioxidant indices of broilers challenged by LPS

项目
Items		 组别Groups 均值
标准误
SEM		 P值P-value
CON L-CON ICGA L-ICGA 脂多糖
LPS		 异绿原酸
ICGA		 互作效应
Interaction
超氧化物歧化酶
SOD/(U/mg prot)		 22.00b 16.21c 25.45a 22.36b 0.557 <0.001 <0.001 0.024
谷胱甘肽过氧化物酶
GSH-Px/(U/mg prot)		 19.73c 15.46d 25.35a 22.71b 0.379 <0.001 <0.001 0.040
过氧化氢酶
CAT/(U/mg prot)		 9.02 7.11 10.13 9.23 0.471 0.006 0.002 0.293
总抗氧化能力
T-AOC/(U/mg prot)		 0.13 0.08 0.14 0.11 0.005 <0.001 0.002 0.066
丙二醛
MDA/(nmol/mg prot)		 0.89b 1.20a 0.56c 0.67c 0.047 <0.001 <0.001 0.043

2.7 饲粮中添加ICGA对LPS刺激肉鸡回肠抗氧化基因表达的影响

饲粮中添加ICGA对LPS刺激肉鸡回肠抗氧化基因表达的影响见图1。双因素方差分析结果显示:LPS刺激显著降低了回肠SOD-1、GSH-Px的mRNA相对表达量(P<0.05);饲粮中添加ICGA能够显著增加回肠SOD-1、GSH-Px的mRNA相对表达量(P<0.05);饲粮添加ICGA与LPS刺激对回肠SOD-1和GSH-Px的mRNA相对表达量存在显著的互作效应(P<0.05)。组间多重比较结果显示:非应激状态下,与CON组相比,ICGA组回肠SOD-1、GSH-Px的mRNA相对表达量显著提高(P<0.05);应激状态下,与L-CON组相比,L-ICGA组回肠SOD-1、GSH-Px的mRNA相对表达量显著提高(P<0.05)。
图1 饲粮中添加ICGA对LPS刺激肉鸡回肠抗氧化基因表达的影响

同一指标,数据柱标注不同小写字母表示差异显著(P<0.05),无字母或有相同字母表示差异不显著(P>0.05)。

Fig.1 Effects of dietary ICGA supplementation on expression of antioxidant genes in ileum of broilers challenged by LPS

For the same index, data columns with different small letter superscripts mean significant difference (P<0.05), while with no letter or the same letter superscripts mean no significant difference (P>0.05).

3 讨论

3.1 饲粮中添加ICGA对肉鸡生长性能的影响

生长性能是衡量动物机体生长状态的最直观的指标,选用合适的方式提高畜禽的生长性能是提高饲养经济效益的有效方式。ICGA作为一种比CGA多1个咖啡酰基的酚酸化合物,其在体内逐级水解可以生成单咖啡酰基奎宁酸、咖啡酸、奎宁酸,进一步经肝肠循环代谢或肠道菌群代谢等代谢途径生成阿魏酸、异阿魏酸、马尿酸等[18-19]。这些代谢产物在体内发挥着促生长、调控肠道健康等作用。例如,阿魏酸具有提高肉鸡肠道抗氧化能力、改善肠道结构等功效[19-20];咖啡酸具有抗凋亡、抗氧化、抗炎等功效[21-22]。Xiong等[23]研究表明,饲粮中添加甜叶菊废渣提取物[CGA类活性成分含量:异绿原酸A(ICGAa)>CGA>异绿原酸C(ICGAc)]显著提高了育肥猪1~75日龄的ADG,并有提高ADFI的趋势。Chen等[24]研究表明,饲粮中添加CGA可以通过提高肠道消化酶活性、增强肠道结构完整性、改善肠道微生物组成等方式提高断奶兔的生长性能。本试验结果显示,饲粮中添加ICGA可以显著提高肉鸡的ADG和末重,显著降低F/G。ADG越高、F/G越低,说明肉鸡生长性能越好。这可能是ICGA在体内代谢产生地酚酸类化合物发挥了抗菌、抗炎等作用,改善了肠道结构,抑制了有害菌的入侵,使得更多的能量用于生长。
同时,本试验所用ICGA作为甜叶菊废渣提取物,在低成本的前提下提高了肉鸡养殖的经济效益,并且改善了甜叶菊废渣对环境造成的污染,拓宽了甜叶菊产业链,可为饲料和养殖企业降本增效提供参考。

3.2 饲粮中添加ICGA对肉鸡营养物质表观代谢率的影响

实际生产中,畜禽常常因自身或外界因素导致消化道损伤、免疫系统受损、消化酶活性降低,对饲粮中营养物质的消化、吸收和利用能力无法达到最佳效果,因此需要外源饲料添加剂改善肠道功能[25]。本研究发现,饲粮中添加ICGA可以显著提高肉鸡对CP和Ca的表观代谢率。CP是肉鸡机体内所有生物代谢过程中的必需营养物质[26]。Ca是机体含量最多的矿物质之一,对机体的代谢和骨骼生长发挥着重要作用[27],其在肠道的停留时间和溶解度是肠道Ca吸收的重要因素[28],而溶解度主要取决于肠道pH[29]。前人研究发现,可以通过在饲料中添加酸化剂的方法提高饲料转化率[30-31]。本试验中,ICGA在肠道中的代谢产物可能在一定程度上降低肠道pH,这有利于肠道消化酶更好的发挥生理活性,提高饲粮的软化、养分的溶解和水解,抑制病原菌的生长,提高饲料转化率。

3.3 饲粮中添加ICGA对LPS刺激肉鸡血清生化指标的影响

血清生化指标可以反映出动物机体的健康状况。当机体受到氧化应激时,细胞膜通透性增大,血清生化指标发生变化,反映出机体组织器官的损伤[32]。当肝细胞受损时,转氨酶和AKP释放到血液中,血清ALT、AST、AKP活性的变化可以反映肝脏损伤情况[33]。LDL-C和HDL-C是肝脏运输胆固醇的载体。当受到氧化应激时,LDL-C中的不饱和脂肪酸被氧自由基氧化修饰为氧化型LDL-C(ox-LDL-C),沉积于血管内膜生成泡沫细胞,导致动脉粥样硬化[34]。HDL-C具有清除血管中过多胆固醇的作用,有助于防止血管堵塞,改善脂质代谢,当机体发生氧化应激时,HDL-C中的胆固醇向胆固醇脂的转化受到抑制,引起HDL-C结构发生改变,加速血管炎症损伤[35]。本试验中,LPS刺激后血清ALT、AKP活性显著升高,HDL-C含量显著降低,表明机体受到了氧化损伤,肝脏功能受损,脂质代谢紊乱;饲粮中添加ICGA则可以显著缓解氧化应激造成的肝脏损伤,缓解血清中HDL-C含量的降低,调节脂质代谢。Liu等[36]研究发现,异绿原酸B(ICGAb)可以缓解小鼠肝纤维化导致的血清ALT、AST活性的升高。王子琴[37]研究表明,饲粮中添加CGA可以显著降低鱼油氧化酸败导致的斑点叉尾 血清ALT、AST活性的提高。周艳[38]研究表明,CGA可以通过增加大鼠血清HDL-C含量抑制LPS造成的应激。本试验结果与前人研究结果一致,说明ICGA可以改善肉鸡的肝脏应激损伤,并且可以通过增加血清HDL-C含量抑制LPS引起的氧化应激,改善脂质代谢。

3.4 饲粮中添加ICGA对LPS刺激肉鸡抗氧化能力的影响

正常生理状态下,机体的氧化和抗氧化状态保持相对平衡,但当这种平衡被打破时,氧自由基过度积累会导致机体发生氧化应激。T-AOC是机体抗氧化物质和抗氧化酶的抗氧化能力的总和,通常作为评价抗氧化能力的综合指标[39];SOD可以催化超氧阴离子转化为过氧化氢,阻止自由基的生成[40];GSH-Px和CAT可以将体内诱发的过氧化物清除[41-42];MDA是活性氧和多不饱和脂肪酸在体内反应产生的脂质过氧化物,其含量可以反映氧化损伤的程度[43]。Tang等[44]研究发现,热应激可以造成肉鸡肝脏发生氧化损伤,具体表现在血清AST活性增加,肝脏MDA含量的增加、核因子E2相关因子2(Nrf2)-Kelch样环氧氯丙烷相关蛋白1(Keap1)信号通路关键基因表达下调以及自噬功能障碍,并且降低了肉鸡的增重和饲料转化率。雷震宇[45]研究发现,霉变饲粮会对机体造成应激反应,具体表现在仔猪血清、肝脏、空肠GSH-Px活性以及空肠T-AOC、总超氧化物歧化酶(T-SOD)活性的降低,此外,霉变饲粮还造成肉鸡ADFI显著下降,对肉鸡生长性能产生负面影响。本研究发现,LPS刺激后,肉鸡血清、回肠、肝脏抗氧化酶活性以及回肠SOD-1和GSH-Px的mRNA相对表达量发生不同程度的降低,而MDA含量则提高,表明肉鸡受到了严重的氧化应激。ICGA理可在一定程度上缓解LPS诱导的氧化应激。Liu等[36]研究发现,蛋氨酸和胆碱缺乏诱导的肝纤维化可以显著降低小鼠肝脏抗氧化酶GSH-Px、SOD、CAT活性以及谷胱甘肽(GSH)含量,显著提高MDA含量,在饲粮中添加异绿原酸B可以通过激活核因子E2相关因子2(Nrf2)信号通路缓解肝纤维化对肝脏造成的氧化损伤。Cao等[46]研究表明,异绿原酸C可以通过上调谷胱甘肽还原酶、葡萄糖-6-磷酸脱氢酶、GSH-Px活性来提高GSH的抗氧化能力,进而减轻Vero细胞受71型肠道病毒感染所导致的氧化损伤。Liu等[47]研究发现,饲粮中添加CGA可以通过激活Nrf2信号通路缓解LPS刺激导致的肠道GSH-Px、SOD、CAT、血红素氧合酶-1和谷胱甘肽S-转移酶活性的降低以及MDA和蛋白羰基含量的升高。ICGA作为比CGA多1个咖啡基的异构体,结构更稳定,抗氧化效果更明显[48-49]。结合前人研究,本试验中ICGA可能是通过激活肠道Nrf2信号通路来调控下游SOD-1、GSH-Px的表达,进而提高抗氧化酶的活性以及降低MDA的含量;ICGA经肠道吸收后经血液循环进入肝脏[50-51],有效地降低了LPS刺激导致的血清和肝脏的氧化应激。

4 结论

综上所述,饲粮中添加ICGA可以改善肉鸡的生长性能和营养物质表观代谢率,尤其对CP和Ca的表观代谢率表现出积极作用。在LPS刺激的情况下,饲粮中添加ICGA可上调回肠抗氧化基因的表达,提高回肠、血清、肝脏抗氧化酶活性,并降低脂质过氧化物产生,提高机体抗氧化能力,缓解LPS刺激诱导的肉鸡氧化应激损伤。

References

Publishing order | Descend order by publishing year | Descend order by cited within
[1]
HICKS G, JIA Z C. Structural basis for the lipopolysaccharide export activity of the bacterial lipopolysaccharide transport system[J]. International Journal of Molecular Sciences, 2018, 19(9):2680.

[2]
REISINGER N, EMSENHUBER C, DOUPOVEC B, et al. Endotoxin translocation and gut inflammation are increased in broiler chickens receiving an oral lipopolysaccharide (LPS) bolus during heat stress[J]. Toxins, 2020, 12(10):622.

[3]
熊云霞, 刘帅, 肖昊, 等. 饲粮添加甜叶菊废渣提取物对断奶仔猪生长性能及内脏组织病理的影响[J]. 动物营养学报, 2023, 35(10):6289-6300.

DOI

XIONG Y X, LIU S, XIAO H, et al. Effects of dietary stevia residue extract supplementation on growth performance and visceral histopathology of weaned piglets[J]. Chinese Journal of Animal Nutrition, 2023, 35(10):6289-6300. (in Chinese)

DOI

[4]
席利莎, 木泰华, 孙红男. 绿原酸类物质的国内外研究进展[J]. 核农学报, 2014, 28(2):292-301.

DOI

XI L S, MU T H, SUN H N. Research progress of chlorogenic acids at home and abroad[J]. Journal of Nuclear Agricultural Sciences, 2014, 28(2):292-301. (in Chinese)

[5]
FENG S Y, ZHANG Y H, FU S D, et al. Application of chlorogenic acid as a substitute for antibiotics in multidrug-resistant Escherichia coli-induced mastitis[J]. International Immunopharmacology, 2023, 114:109536.

[6]
ZHAO J S, DENG W, LIU H W. Effects of chlorogenic acid-enriched extract from Eucommia ulmoides leaf on performance,meat quality,oxidative stability,and fatty acid profile of meat in heat-stressed broilers[J]. Poultry Science, 2019, 98(7):3040-3049.

[7]
PSOTOVÁ J,CHLOPČÍKOVÁ Š,MIKETOVÁ P,et al. Chemoprotective effect of plant phenolics against anthracycline-induced toxicity on rat cardiomyocytes.Part Ⅲ.Apigenin, baicalelin, kaempherol,luteolin and quercetin[J]. Phytotherapy Research,2004,18(7):516-521.

[8]
WANG H N, SHEN Z, LIU Q, et al. Isochlorogenic acid (ICGA):natural medicine with potentials in pharmaceutical developments[J]. Chinese Journal of Natural Medicines, 2020, 18(11):860-871.

[9]
ZOU X, JI J, QU H, et al. Effects of sodium butyrate on intestinal health and gut microbiota composition during intestinal inflammation progression in broilers[J]. Poultry Science, 2019, 98(10):4449-4456.

DOI PMID

[10]
SUN L, GUO L W, XU G Q, et al. Quercetin reduces inflammation and protects gut microbiota in broilers[J]. Molecules, 2022, 27(10):3269.

[11]
MAMAT N, DOU J, LU X Y, et al. Isochlorogenic acid A promotes melanin synthesis in B16 cell through the β-catenin signal pathway[J]. Acta Biochimica et Biophysica Sinica, 2017, 49(9):800-807.

DOI PMID

[12]
NIE R Z, DANG M Z, GE Z Z, et al. Interactions of chlorogenic acid and isochlorogenic acid A with model lipid bilayer membranes:insights from molecular dynamics simulations[J]. Chemistry and Physics of Lipids, 2021, 240:105136.

[13]
WANG J, WANG H, PENG Y, et al. Isochlorogenic acid A affects P450 and UGT enzymes in vitro and in vivo[J]. Chinese Journal of Natural Medicines, 2016, 14(11):865-870.

[14]
LIU S D, SONG M H, YUN W, et al. Effect of carvacrol essential oils on immune response and inflammation-related genes expression in broilers challenged by lipopolysaccharide[J]. Poultry Science, 2019, 98(5):2026-2033.

DOI PMID

[15]
WANG B, CUI Y, ZHANG Q J, et al. Selenomethionine alleviates LPS-induced JNK/NLRP3 inflammasome-dependent necroptosis by modulating miR-15a and oxidative stress in chicken lungs[J]. Metallomics, 2021, 13(8):mfab048.

[16]
HORWITZ W,JR ASSISTANT G W L. Official methods of analysis of AOAC international[S]. 18th ed.Gaithersburg, Mary Land: AOAC International, 2005.

[17]
WU F Y, WANG H N, LLI S, et al. Effects of dietary supplementation with quercetagetin on nutrient digestibility,intestinal morphology,immunity,and antioxidant capacity of broilers[J]. Frontiers in Veterinary Science, 2022, 9:1060140.

[18]
NARANJO PINTA M, MONTOLIU I, AURA A M, et al. In vitro gut metabolism of [U-13C]-quinic acid,the other hydrolysis product of chlorogenic acid[J]. Molecular Nutrition & Food Research, 2018, 62(22):e1800396.

[19]
CLIFFORD M N, KERIMI A, WILLIAMSON G. Bioavailability and metabolism of chlorogenic acids (acyl-quinic acids) in humans[J]. Comprehensive Reviews in Food Science and Food Safety, 2020, 19(4):1299-1352.

DOI PMID

[20]
LI J, WANG S P, WANG Y Q, et al. Comparative metabolism study on chlorogenic acid,cryptochlorogenic acid and neochlorogenic acid using UHPLC-Q-TOF MS coupled with network pharmacology[J]. Chinese Journal of Natural Medicines, 2021, 19(3):212-224.

[21]
裴亚萍, 赵瑾, 孙娜, 等. 咖啡酸对玉米赤霉烯酮诱导小鼠卵巢颗粒细胞凋亡的保护作用[J]. 畜牧兽医学报, 2020, 51(12):3068-3075.

DOI

PEI Y P, ZHAO J, SUN N, et al. The effect of caffeic acid on zearalenone-induced ovarian granulosa cell apoptosis in mice[J]. Acta Veterinaria et Zootechnica Sinica, 2020, 51(12):3068-3075. (in Chinese)

DOI

[22]
SHAMSABADI S, NAZER Y, GHASEMI J, et al. Promising influences of zingerone against natural and chemical toxins:a comprehensive and mechanistic review[J]. Toxicon, 2023, 233:107247.

[23]
XIONG Y X, LIU S, XIAO H, et al. Dietary stevia residue extract supplementation improves the performance and antioxidative capacity of growing-finishing pigs[J]. Journal of the Science of Food and Agriculture, 2022, 102(11):4724-4735.

DOI PMID

[24]
CHEN J L, SONG Z C, JI R M, et al. Chlorogenic acid improves growth performance of weaned rabbits via modulating the intestinal epithelium functions and intestinal microbiota[J]. Frontiers in Microbiology, 2022, 13:1027101.

[25]
谢童, 董涛, 王伟唯, 等. 复合乳酸菌制剂对黄羽肉鸡生长性能、胃肠道pH、肠道形态和盲肠微生物的影响[J]. 动物营养学报, 2022, 34(1):254-263.

DOI

XIE T, DONG T, WANG W W, et al. Effects of compound Lactobacillus preparation on growth performance,gastrointestinal pH,intestinal morphology and cecal microorganism of yellow-feathered broilers[J]. Chinese Journal of Animal Nutrition, 2022, 34(1):254-263. (in Chinese)

[26]
李洪滨, 刘延杰, 陈宁, 等. 不同蛋白质水平饲粮中添加酸性蛋白酶对肉鸡生长性能和养分表观消化率的影响[J]. 动物营养学报, 2023, 35(5):2943-2955.

DOI

LI H B, LIU Y J, CHEN N, et al. Effects of acid protease supplementation in diets with different protein levels on growth performance and nutrient apparent digestibility of broilers[J]. Chinese Journal of Animal Nutrition, 2023, 35(5):2943-2955. (in Chinese)

DOI

[27]
DAVID L S, ANWAR M N, ABDOLLAHI M R, et al. Calcium nutrition of broilers:current perspectives and challenges[J]. Animals, 2023, 13(10):1590.

[28]
ARECO V, RIVOIRA M A, RODRIGUEZ V, et al. Dietary and pharmacological compounds altering intestinal calcium absorption in humans and animals[J]. Nutrition Research Reviews, 2015, 28(2):83-99.

PMID

[29]
PAZIANAS M. Effectiveness of calcium and vitamin D supplementation in osteoporosis[J]. Annals of the New York Academy of Sciences, 2018, 1433(1):5-6.

DOI PMID

[30]
张燕利, 陈宇辰, 尹苗, 等. 复合酸化剂和植物精油对白羽肉鸡生长性能、屠宰性能、肉品质及养分消化率的影响[J]. 中国畜牧杂志, 2022, 58(11):250-255.

ZHANG Y L, CHEN Y C, YIN M, et al. Effects of compound acidifier and plant essential oil on growth performance,slaughter performance,meat quality and nutrient digestibility of white feather broilers[J]. Chinese Journal of Animal Science, 2022, 58(11):250-255. (in Chinese)

[31]
刘新泽, 胡友军, 赵晓南, 等. 饲粮中添加不同类型和水平的酸化剂对肉鸡生长性能、养分表观代谢率及血清生化、抗氧化和免疫指标的影响[J]. 动物营养学报, 2022, 34(5):2949-2960.

DOI

LIU X Z, HU Y J, ZHAO X N, et al. Effects of dietary different types and different levels of acidifiers on growth performance,nutrient apparent metabolic rates and serum biochemical,antioxidant and immune indexes of broilers[J]. Chinese Journal of Animal Nutrition, 2022, 34(5):2949-2960. (in Chinese)

[32]
焦靖娴, 王瑶, 彭煜畅, 等. L-精氨酸对脂多糖应激下大鼠抗氧化能力、免疫功能和肠道健康的影响[J]. 动物营养学报, 2023, 35(11):7401-7410.

DOI

JIAO J X, WANG Y, PENG Y C, et al. Effects of L-arginine on antioxidant capacity,immune function and intestinal health of rats under lipopolysaccharide stress[J]. Chinese Journal of Animal Nutrition, 2023, 35(11):7401-7410. (in Chinese)

[33]
ZHOU Q, ZHU J M, LIU B, et al. Effects of high-dose of copper amino acid complex on laying performance,hematological and biochemical parameters,organ index,and histopathology in laying hens[J]. Biological Trace Element Research, 2021, 199(8):3045-3052.

[34]
张晶梅, 苏珍珍, 徐秀芬, 等. 糖尿病合并颈动脉斑块患者血浆ox-LDL-C与氧化应激相关性研究[J]. 国际检验医学杂志, 2023, 44(15):1863-1867.

ZHANG J M, SU Z Z, XU X F, et al. Correlation between plasma ox-LDL-C and oxidative stress in patients with diabetes mellitus complicated with carotid plaque[J]. International Journal of Laboratory Medicine, 2023, 44(15):1863-1867. (in Chinese)

[35]
李婷婷, 张媚琰. HbA1c、LDL-C、HDL-C联合检测在2型糖尿病肾病中的诊断价值[J]. 中外医学研究, 2024, 22(4):67-71.

LI T T, ZHANG M Y. Diagnostic value of HbA1c,LDL-C and HDL-C combined detection in type 2 diabetic nephropathy[J]. Chinese and Foreign Medical Research, 2024, 22(4):67-71. (in Chinese)

[36]
LIU X, HUANG K, NIU Z R, et al. Protective effect of isochlorogenic acid B on liver fibrosis in non-alcoholic steatohepatitis of mice[J]. Basic & Clinical Pharmacology & Toxicology, 2019, 124(2):144-153.

[37]
王子琴. 绿原酸或牛磺酸缓解氧化鱼油胁迫下斑点叉尾鮰免疫应激的研究[D]. 硕士学位论文. 长沙: 湖南农业大学, 2021.

WANG Z Q. Chlorogenic acid or taurine alleviate immune stress in channel catfish (Ietalurus punetaus) induced by oxidized fish oil[D]. Master’s Thesis. Changsha: Hunan Agricultural University, 2021. (in Chinese)

[38]
周艳. 杜仲叶多酚提取物对猪肉品质及绿原酸缓解肝-肠损伤研究[D]. 博士学位论文. 南昌: 南昌大学, 2015.

ZHOU Y. Effect of polyphenols extract from Eucommia ulmoides oliver leaf on meat quality and chlorogenic acid ameliorate liver-intestine injury[D]. Ph.D.Thesis. Nanchang: Nanchang University, 2015. (in Chinese)

[39]
WANG Y, WU P, SHEN H Y. Effect of ampicillin wastewater on the T-AOC and LDH activities of zebrafish[J]. IOP Conference Series:Earth and Environmental Science, 2019, 295(2):012018.

[40]
ZHAO H Q, ZHANG R F, YAN X Y, et al. Superoxide dismutase nanozymes:an emerging star for anti-oxidation[J]. Journal of Materials Chemistry B, 2021, 9(35):6939-6957.

[41]
陶旭哲, 陈艾玲, 马婷婷, 等. 种鸽饲粮添加不同硒源对乳鸽生长性能、肝脏抗氧化能力和谷胱甘肽过氧化物酶系基因表达的影响[J]. 动物营养学报, 2023, 35(7):4564-4574.

DOI

TAO X Z, CHEN A L, MA T T, et al. Effects of supplementation of different selenium sources in diets of breeding pigeons on growth performance,liver antioxidant capacity and glutathione peroxidase system gene expression of squabs[J]. Chinese Journal of Animal Nutrition, 2023, 35(7):4564-4574. (in Chinese)

[42]
马维梅, 赖世雄, 杨佳, 等. 牛樟芝多糖和锌对肉鸡生长性能、血清生化指标以及抗氧化能力的影响[J]. 动物营养学报, 2023, 35(6):3684-3697.

DOI

MA W M, LAI S X, YANG J, et al. Effects of antrodia cinnamomea polysaccharide on growth performance,serum biochemical indexes and antioxidant capacity of broilers[J]. Chinese Journal of Animal Nutrition, 2023, 35(6):3684-3697. (in Chinese)

[43]
任继武, 陈哲秀, 乔君毅, 等. 葡萄籽原花青素对四川白鹅生长性能和抗氧化能力的影响[J]. 动物营养学报, 2023, 35(12):7817-7827.

DOI

REN J W, CHEN Z X, QIAO J Y, et al. Effects of grape seed proanthocyanidins on growth performance and antioxidant capacity of Sichuan white geese[J]. Chinese Journal of Animal Nutrition, 2023, 35(12):7817-7827. (in Chinese)

[44]
TANG L P, LIU Y L, ZHANG J X, et al. Heat stress in broilers of liver injury effects of heat stress on oxidative stress and autophagy in liver of broilers[J]. Poultry Science, 2022, 101(10):102085.

[45]
雷震宇. 霉变饲粮添加霉菌毒素降解剂对断奶仔猪生长性能、免疫功能、抗氧化能力及肠道健康的影响[D]. 硕士学位论文. 雅安: 四川农业大学, 2023.

LEI Z Y. Effects of adding mycotoxin degraders to diet natural contaminated with mycotoxins on growth performance,immune function,antioxidant capacity and intestinal health of weaned piglets[D]. Master’s Thesis. Ya’an: Sichuan Agricultural University, 2023. (in Chinese)

[46]
CAO Z Y, DING Y, CAO L, et al. Isochlorogenic acid C prevents enterovirus 71 infection via modulating redox homeostasis of glutathione[J]. Scientific Reports, 2017, 7(1):16278.

DOI PMID

[47]
LIU H, MENG H, DU M, et al. Chlorogenic acid ameliorates intestinal inflammation by inhibiting NF-κB and endoplasmic reticulum stress in lipopolysaccharide-challenged broilers[J]. Poultry Science, 2024, 103(5):103586.

[48]
MISHIMA S, INOH Y, NARITA Y, et al. Identification of caffeoylquinic acid derivatives from Brazilian propolis as constituents involved in induction of granulocytic differentiation of HL-60 cells[J]. Bioorganic & Medicinal Chemistry, 2005, 13(20):5814-5818.

[49]
XU J G, HU Q P, LIU Y. Antioxidant and DNA-protective activities of chlorogenic acid isomers[J]. Journal of Agricultural and Food Chemistry, 2012, 60(46):11625-11630.

[50]
FARAH A,DE PAULA LIMA J. CHAPTER 16:chlorogenic acids:daily consumption through coffee,metabolism and potential health effects[M]// FARAHA. Coffee:consumption and health implications. London: The Royal Society of Chemistry, 2019:364-415.

[51]
宋志成. 绿原酸对肉兔生产性能和肠道屏障的影响[D]. 硕士学位论文. 泰安: 山东农业大学, 2023.

SONG Z C. Effects of chlorogenic acid on production performance and intestinal barrier of meat rabbits[D]. Master’s Thesis. Tai’an: Shandong Agricultural University, 2023. (in Chinese)

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