Chinese Journal of Animal Nutrition >

2023 , Vol. 35 >Issue 12: 7759 - 7773

DOI: https://doi.org/10.12418/CJAN2023.705

RESEARCH PAPER

Effects of Probiotics Combined with Acidifiers on Growth Performance, Antioxidant Capacity and Intestinal Health of Broilers

  • JIN Xu , 1 ,
  • WU Qiong 1 ,
  • LI Zhen 1 ,
  • LONG Lingbo 1 ,
  • LI Yang 1 ,
  • DING Xiaoling 1 ,
  • MU Yuyun 2 ,
  • LI Peng 2 ,
  • ZHANG Cheng , 1, *
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  • 1 College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China
  • 2 Novus International Trading Co., Ltd., Shanghai 200080, China
* professor, E-mail:

Received date: 2023-06-15

  Online published: 2023-12-11

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Abstract

This experiment was conducted to explore the effects of three probiotics combined with acidifiers on growth performance, antioxidant capacity and intestinal health of broilers, aiming to provide evidence for the combination of probiotics and acidifiers. A total of 875 male Arbor Acres broilers of 1-day-old were randomly divided into 5 groups as control group (CON group), acidifier group (ACI group), acidifier+Bacillus licheniformis group (ACI+BL group), acidifier+Bacillus coagulans group (ACI+BC group) and acidifier+Clostridium butyricum group (ACI+CB group) with 7 replicates per group and 25 broilers per replicate. Broilers in CON group were fed a basal diet, those in ACI group were fed a basal diet supplemented with 250 mg/kg acidifier, and those in ACI+BL group, ACI+BC group and ACI+CB group were fed the basal diet supplemented with 250 mg/kg acidifier as well as Bacillus licheniformis (1 to 21 days of age, 9×109 CFU/kg; 22 to 42 days of age, 3×109 CFU/kg), Bacillus coagulans (1 to 21 days of age, 3.0×1010 CFU/kg; 22 to 42 days of age, 1.0×1010 CFU/kg) and Clostridium butyricum (1 to 21 days of age, 1.5×109 CFU/kg; 22 to 42 days of age, 0.5×109 CFU/kg), respectively. The experiment lasted for 42 days. The results showed as follows: 1) compared with CON group, the average daily gain (ADG) of broilers from 1 to 21 days of age, the villus height to crypt depth ratio (V/C) in jejunum at 21 days of age, and the lipid activity in jejunum and the zonula occludens-1 (ZO-1) mRNA relative expression level in jejunal mucosa at 42 days of age in ACI group were significantly increased (P<0.05); the bursa of Fabricius index at 21 days of age, the serum catalase (CAT) activity at 42 days of age, the villus height (VH) in ileum at 21 days of age, the V/C in jejunum and ileum at 21 and 42 days of age, and the activities lipase and trypsin in jejunum and ZO-1 mRNA relative expression level in jejunal mucosa at 42 days of age in ACI+BL group were significantly increased (P<0.05); the ADG from 1 to 21 days of age, the bursa of Fabricius index and glutathione peroxidase (GPX) activity in serum at 21 days of age, the activities of CAT and superoxide dismutase (SOD) in serum at 42 days of age, the VH in ileum at 21 days of age, the V/C in jejunum and ileum at 21 and 42 days of age, and the activities of lipase and trypsin in jejunum and mRNA relative expression levels of ZO-1, nuclear factor E2-related factor 2 (Nrf2), SOD and interleukin-10 (IL-10) in jejunal mucosa at 21 and 42 days of age in ACI+BC group were significantly increased (P<0.05), while the ratio of feed to gain (F/G) in each growth stage and the malondialdehyde (MDA) content in serum as well as the mRNA relative expression levels of nuclear factor-κB (NF-κB) and tumor necrosis factor-α (TNF-α) in jejunal mucosa at 42 days of age were significantly decreased (P<0.05); the ADG from 1 to 21 days of age, the activities of CAT and SOD in serum at 42 days of age, the V/C in jejunum and ileum at 21 and 42 days of age, and the relative mRNA expression levels of ZO-1 and Nrf2 in jejunum mucosa at 42 days of age in ACI+CB group were significantly increased (P<0.05), while the F/G in each growth stage and the TNF-α mRNA relative expression level in jejunum mucosa at 42 days of age were significantly decreased (P<0.05). 2) Compared with ACI group, the bursa of Fabricius index and GPX activity in serum of broilers at 21 days of age, the activities of CAT and SOD in serum at 42 days of age, the VH in ileum at 21 days of age, the V/C in ileum at 42 days of age, and the trypsin activity in jejunum and mRNA relative expression levels of ZO-1, SOD and IL-10 in jejunum mucosa at 42 days of age in ACI+BC group were significantly increased (P<0.05), while the MDA content in serum and NF-κB mRNA relative expression level in jejunum mucosa at 42 days of age were significantly decreased (P<0.05); the activities of CAT and SOD in serum and the V/C in jejunum and ileum at 42 days of age in ACI+CB group were significantly increased (P<0.05). In conclusion, the combination of probiotics and acidifiers can improve growth performance, immunity, antioxidant capacity and intestinal health of broilers, and the effect is better than that of acidifier alone. The mechanism of combining probiotics with acidifiers to improve intestinal health may be related to promoting the Nrf2 antioxidant pathway and inhibiting the expression of NF-κB inflammatory pathway related factors. Under the experimental conditions, the combination of Bacillus coagulans and acidifier has a better effect.

Key words： broilers; probiotics; acidifiers; growth performance; antioxidant capacity; intestinal health

Cite this article

JIN Xu , WU Qiong , LI Zhen , LONG Lingbo , LI Yang , DING Xiaoling , MU Yuyun , LI Peng , ZHANG Cheng . Effects of Probiotics Combined with Acidifiers on Growth Performance, Antioxidant Capacity and Intestinal Health of Broilers[J]. Chinese Journal of Animal Nutrition, 2023 , 35(12) : 7759 -7773 . DOI: 10.12418/CJAN2023.705

饲用抗生素具有抑制有害细菌增殖和提高动物生长性能等特性,在过去几十年里极大的推动了畜牧业的发展。然而,抗生素的过度使用造成耐药性细菌的出现、畜禽产品及环境抗生素污染问题,影响畜禽业的健康发展和人类健康。为此,欧盟、美国等主要发达国家和地区相继颁布了禁止在饲料中添加抗生素的条令。我国农业农村部于2019年发布了第194号公告,全面禁止了生产含有除中药类外促生长类饲料添加剂的商品饲料。因此,寻找绿色、安全的抗生素替代品及综合替代方案已成为当前的研究热点。不过,当前仍未开发出能完全替代饲用抗生素的单一的饲料添加剂,将2种或2种以上的具有替抗功能的添加剂联合使用是当前行业普遍采用的替抗手段[1]。其中,酸化剂和益生菌具有替抗潜能,已作为饲用抗生素的替代品广泛用于动物生产[2]。研究表明,大多数致病菌在pH接近7的环境下更易存活[3]。与之相反,有益菌具有一定的耐酸能力,在pH 5.8~6.2的环境下具有更强的增殖能力[4]。酸化剂具有降低胃肠道pH的作用,有利于有益菌的生长,这为其可促进益生菌的应用效果奠定了理论基础。刁蓝宇等[5]和曹要玲等[6]研究发现,益生菌与酸化剂联合使用可显著提高肉鸡的生长性能和肉品质。在蛋鸭[7]和鱼[8]上的研究表明,“酸化剂+益生菌”的组合方案在增强机体免疫力和提高肠道健康方面具有积极的效应。然而,益生菌种类繁多,不同益生菌与酸化剂组合使用具有更好的应用效果尚不明确,值得深入探究。芽孢杆菌可产生抗应激能力强的孢子,相较于乳酸杆菌等其他类型的益生菌而言能更有效地应对饲料储存、运输和加工等过程,从而更易成功定植于肠道中,发挥其改善肠道健康、促进动物免疫功能和生长的功能[9],因此,芽孢杆菌类益生菌当前被畜牧生产中被广泛应用。为此,本研究选取同为芽孢杆菌类益生菌的地衣芽孢杆菌、凝结芽胞杆菌和丁酸梭菌分别与酸化剂联合使用,考察其对肉鸡生长性能、抗氧化能力和肠道健康的影响,从而筛选出与酸化剂联合使用具有最佳效果的益生菌,为在肉鸡生产中更加合理应用益生菌提供理论依据。

1 材料与方法

1.1 试验设计

本试验选取健康1日龄雄性爱拔益加(Arbor Acres,AA)肉鸡875羽,随机分为5组:对照组(CON组)、酸化剂组(ACI组)、酸化剂+地衣芽孢杆菌组(ACI+BL组)、酸化剂+凝结芽孢杆菌组(ACI+BC组)和酸化剂+丁酸梭菌组(ACI+CB组),每组7个重复,每个重复25只。CON组饲喂基础饲粮,ACI组饲喂在基础饲粮中添加250 mg/kg酸化剂(主要成分为苯甲酸和富马酸)的饲粮,ACI+BL组、ACI+BC组和ACI+CB组饲喂在基础饲粮中添加250 mg/kg酸化剂的基础上分别添加地衣芽孢杆菌(1~21日龄,9×109 CFU/kg;22~42日龄,3×109 CFU/kg)、凝结芽孢杆菌(1~21日龄,3.0×1010 CFU/kg;22~42日龄,1.0×1010 CFU/kg)和丁酸梭菌(1~21日龄,1.5×109 CFU/kg;22~42日龄,0.5×109 CFU/kg)的饲粮。试验期42 d。基础饲粮参考NRC(1994)营养需要标准进行配制,其组成及营养水平见表1。本研究所用的3种芽孢杆菌及酸化剂均由某贸易有限公司提供,添加水平依据前期预试验结果。
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		 1~14日龄
1 to 14 days of age		 15~28日龄
15 to 28 days of age		 29~42日龄
29 to 42 days of age
原料Ingredients
玉米Corn 59.20 58.80 60.30
豆粕Soybean meal 27.60 31.60 30.50
大豆油Soybean oil 1.60 2.70 2.80
鱼粉Fish meal 0.80 0.80
玉米蛋白粉Corn gluten meal 7.20 2.00 2.00
氯化钠NaCl 0.25 0.25 0.25
氯化胆碱Choline chloride 0.20 0.20 0.20
磷酸氢钙CaHPO4 1.90 1.84 1.55
石粉Limestone 1.30 1.16 1.11
DL-蛋氨酸DL-Met 0.21 0.25 0.14
L-赖氨酸盐酸盐L-Lys·HCl 0.30 0.16 0.11
预混料Premix1) 0.24 0.24 0.24
合计Total 100.00 100.00 100.00
营养水平Nutrient levels2)
代谢能ME/(MJ/kg) 12.56 12.51 12.61
粗蛋白质CP 21.33 20.27 19.81
赖氨酸Lys 1.19 1.17 1.11
蛋氨酸Met 0.58 0.57 0.46
蛋氨酸+半胱氨酸Met+Cys 0.92 0.90 0.79
有效磷AP 0.45 0.44 0.38
钙Ca 1.02 0.99 0.91

1)预混料为每千克饲粮提供 The premix provided the following per kilogram of diets:Fe(FeSO4) 80 mg,Cu(CuSO4) 10 mg,Zn(ZnSO4) 100 mg,Mn(MnSO4) 80 mg,I(KI) 0.6 mg,Se(Na2SeO3) 0.15 mg,VA 4 000 IU,VD3 8 000 IU,VE 44 IU,VB1 3.6 mg,VB2 3.75 mg,VB6 5 mg,VB12 0.015 mg,VK3 0.5 mg,生物素 biotin 0.2 mg,叶酸 folic acid 1.3 mg,泛酸 pantothenic acid 12 mg,烟酸 nicotinic acid 40 mg。

2)营养水平均为计算值。Nutrient levels were all calculated values.

1.2 饲养管理

本试验采用3层笼养的方式进行分阶段饲养。试验第1周鸡舍温度控制在(35±1) ℃,之后开始逐步降温,每周降温2~3 ℃,直到最终温度达到(22±1) ℃。鸡舍相对湿度保持在55%~65%。饲养全期鸡只自由采食和饮水,常规免疫。每日记录肉鸡采食量和死亡淘汰情况。

1.3 样品采集

分别于肉鸡21和42日龄,在每个重复中选择接近平均体重的1只鸡进行采血后屠宰。血液样本在4 ℃条件下以3 000×g离心15 min后获得血清,保存于-20 ℃低温冰箱中用于后续抗氧化相关指标的测定;将胸腺、脾脏和法氏囊分离并放置在电子秤上称重;分别从十二指肠、空肠和回肠的中间部分切下约2 cm长的肠段,生理盐水冲洗后,保存在10%福尔马林溶液中,用于观测肠道形态结构;收集十二指肠、空肠和回肠内容物样品,用于测定消化酶活性;刮取剩余空肠段黏膜,放置于-80 ℃下保存,用于后续基因表达分析。

1.4 检测指标及方法

1.4.1 生长性能

记录肉鸡的每日饲粮采食量,并在试验第1、21和42天以重复为单位称量肉鸡的体重。根据收集的肉鸡体重和饲粮采食量数据,计算各组的平均日增重(ADG)、平均日采食量(ADFI)和料重比(F/G)。

1.4.2 免疫器官指数

将上述称重后的免疫器官(胸腺、脾脏和法氏囊)按照以下公式计算免疫器官指数:
免疫器官指数(g/kg)=免疫器官重量(g)/宰前肉鸡活体重量(kg)。

1.4.3 血清抗氧化指标

取储存于-20 ℃冰箱的血清样品,依照南京建成生物工程研究所生产的试剂盒说明书测定血清过氧化氢酶(CAT)、超氧化物歧化酶(SOD)、谷胱甘肽过氧化物酶(GPX)活性和总抗氧化能力(T-AOC)以及丙二醛(MDA)含量。

1.4.4 肠道形态结构

将保存于福尔马林溶液中的小肠段经过脱水、清理、切片及苏木精-伊红染色后,在光学显微镜下测量小肠绒毛高度(villus height,VH)和隐窝深度(crypt depth,CD),并计算绒隐比(绒毛高度/隐窝深度,V/C)。

1.4.5 肠道消化酶活性

将冻存于-80 ℃的肠道内容物样品取出,于4 ℃条件下解冻。参照南京建成生物工程研究所检测试剂盒说明书,称取一定质量内容物,在生理盐水中用全自动样品快速研磨仪匀浆破碎,制备组织匀浆液。在4 ℃、3 000 r/min条件下,离心10 min,取上清液,测定淀粉酶、脂肪酶和胰蛋白酶活性。

1.4.6 空肠黏膜相关基因表达

本研究前期测定的小肠形态结构和消化酶活性结果表明,益生菌与酸化剂联用对空肠具有最优效果,故选用空肠来进一步研究其可能的作用机制。使用Trizol试剂(Yeasen Biotechnology)提取空肠黏膜中的总RNA,然后将总RNA按照逆转录试剂盒(Yeasen Biotechnology)反转录为cDNA。测定基因包括:闭合小环蛋白-1(ZO-1)、闭锁蛋白(occludin)、核因子E2相关因子2(Nrf2)、GPX、SOD、CAT、核因子-κB(NF-κB)、白细胞介素-6(IL-6)、白细胞介素-10(IL-10)、白细胞介素1β(IL-1β)和肿瘤坏死因子-α(TNF-α)。引物序列参见课题组前期成果[10],基因信息及引物序列见表2。所有引物均由南京擎科生物科技有限公司合成,在ABI 7500 Real-Time PCR系统(Applied Biosystems,美国)上进行实时荧光定量PCR。PCR体系和热循环条件参照本课题组前期研究[11]进行设置。以β-肌动蛋白(β-actin)为内参基因,采用2-ΔΔCt法计算靶基因mRNA相对表达量。
表2 基因信息及引物序列

Table 2 Genes information and primer sequences

基因
Genes		 GenBank登录号
GenBank accession number		 引物序列
Primer sequences (5'—3')		 扩增大小
Amplicon size/bp
闭合小环蛋白-1 ZO-1 XM_015278975.3 F:TCCCTAAAGGCGAAGAAGTA 66
R:CAACAATGCGACGATAAACA
闭锁蛋白Occludin NM_205128.1 F:TCCTCATCGTCATCCTGCTCTG 157
R:CCATCCGCCACGTTCTTCAC
核因子E2相关因子Nrf2 NM_205117.1 F:AGTGACCCAGTCTTCATTTC 110
R:TCTTCCCAAACTTGCTCTAT
谷胱甘肽过氧化物酶GPX NM_001277853.3 F:GGCAAAGTGCTGCTGGTGGTC 166
R:TCTCCTCGTTGGTGGCGTTCT
超氧化物歧化酶SOD NM_205064.2 F:AAGGGAGGAGTGGCAGAAGT 164
R:GCTAAACGAGGTCCAGCAT
过氧化氢酶CAT NM_001031215.2 F:CTTCCTGGTCTTTCTACATTC 179
R:ATACGCCATCTGTTCTACCT
核因子-κB NF-κB NM_001001472.2 F:ACTTGGCGATCATTCACGAGG 109
R:ATACGCCATCTGTTCTACCT
白细胞介素-6 IL-6 NM_204628.1 F:GAAATCCCTCCTCGCCAATCT 106
R:CCTCACGGTCTTCTCCATAAACG
白细胞介素-10 IL-10 NM_001004414.2 F:GCTGTCACCGCTTCTTCACC 87
R:TCCCGTTCTCATCCATCTTCTC
白细胞介素-1β IL-1β NM_204524.1 F:GACCAAACTGCTGCGGAGGC 155
R:CGAAGGACTGTGAGCGGGTGT
肿瘤坏死因子-α TNF-α NM_204267.2 F:TGTTCTATGACCGCCCAGTT 169
R:TTCAGAGCATCAACGCAAAA
β-肌动蛋白β-actin NM_205518.1 F:TGCGTGACATCAAGGAGAAG 188
R:GGACTCCATACCCAAGAAAGAT

1.5 数据统计分析

试验所得数据利用Excel 2021进行初步统计,数据符合正态分布特征,采用SPSS 26.0统计软件进行单因素方差分析,并采用Duncan氏法进行多重比较,试验结果以平均值和均值标准误(SEM)表示,P<0.05表示差异显著。

2 结果与分析

2.1 益生菌与酸化剂联用对肉鸡生长性能的影响

由表3可知,与CON组相比,ACI组、ACI+BC组和ACI+CB组肉鸡1~21日龄ADG显著提高(P<0.05),ACI+BC组和ACI+CB组肉鸡1~21日龄、22~42日龄和1~42日龄F/G显著降低(P<0.05)。
表3 益生菌与酸化剂联用对肉鸡生长性能的影响

Table 3 Effects of probiotics combined with acidifiers on growth performance of broilers

项目
Items		 组别Groups 均值标准误
SEM		 P值
P-value
CON ACI ACI+BL ACI+BC ACI+CB
1~21日龄1 to 21 days of age
平均日采食量ADFI/g 53.86 54.33 53.06 52.17 51.77 0.40 0.222
平均日增重ADG/g 30.79b 32.35a 31.00b 32.42a 32.18a 0.21 0.012
料重比F/G 1.75a 1.68ab 1.71a 1.61b 1.61b 0.02 0.011
22~42日龄22 to 42 days of age
平均日采食量ADFI/g 141.12 138.87 141.08 141.20 133.72 1.64 0.408
平均日增重ADG/g 71.71 73.18 74.69 76.99 72.91 0.95 0.609
料重比F/G 1.96a 1.90ab 1.89ab 1.84b 1.84b 0.02 0.047
1~42日龄1 to 42 days of age
平均日采食量ADFI/g 97.49 97.35 97.07 96.68 92.75 0.89 0.390
平均日增重ADG/g 51.55 52.77 52.84 54.31 52.47 0.46 0.488
料重比F/G 1.89a 1.83ab 1.84ab 1.78b 1.79b 0.01 0.019

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

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

2.2 益生菌与酸化剂联用对肉鸡免疫器官指数的影响

由表4可知,与CON组相比,ACI+BL组和ACI+BC组肉鸡21日龄法氏囊指数显著提高(P<0.05);与ACI组相比,ACI+BC组21日龄法氏囊指数显著提高(P<0.05)。
表4 益生菌与酸化剂联用对肉鸡免疫器官指数的影响

Table 4 Effects of probiotics combined with acidifiers on immune organ indices of broilersg/kg

项目 组别Groups 均值标准误 P值
Items CON ACI ACI+BL ACI+BC ACI+CB SEM P-value
21日龄21 days of age
脾脏指数Spleen index 0.68 0.78 0.82 0.87 0.81 0.03 0.283
胸腺指数Thymus index 1.96 2.07 2.32 2.47 2.21 0.08 0.152
法氏囊指数Bursa of Fabricius index 1.70c 1.83bc 2.48ab 2.61a 2.38abc 0.12 0.04
42日龄42 days of age
脾脏指数Spleen index 1.16 1.2 1.23 1.25 1.46 0.06 0.642
胸腺指数Thymus index 1.21 1.36 1.37 1.82 1.76 0.02 0.635
法氏囊指数Bursa of Fabricius index 0.49 0.52 0.63 0.6 0.55 0.03 0.506

2.3 益生菌与酸化剂联用对肉鸡血清抗氧化指标的影响

由表5可知,CON组和ACI组肉鸡血清抗氧化指标均无显著差异(P>0.05)。与CON组相比,ACI+BC组21日龄血清GPX活性显著提高(P<0.05),ACI+BL组、ACI+BC组和ACI+CB组42日龄血清CAT活性显著提高(P<0.05),ACI+BC组和ACI+CB组42日龄血清SOD活性显著提高(P<0.05),而ACI+BC组42日龄血清MDA含量显著降低(P<0.05)。与ACI组相比,ACI+BC组和ACI+CB组42日龄血清CAT和SOD活性显著提高(P<0.05);此外,ACI+BC组21日龄血清GPX活性显著提高(P<0.05),42日龄血清MDA含量显著降低(P<0.05)。
表5 益生菌与酸化剂联用对肉鸡血清抗氧化指标的影响

Table 5 Effects of probiotics combined with acidifiers on serum antioxidant indices of broilers

项目
Items		 组别Groups 均值标准误
SEM		 P值
P-value
CON ACI ACI+BL ACI+BC ACI+CB
21日龄21 days of age
过氧化氢酶CAT/(U/mL) 16.71 19.42 21.23 22.04 22.47 0.80 0.072
丙二醛MDA/(nmol/mL) 2.50 2.44 2.32 2.02 2.29 0.06 0.168
谷胱甘肽过氧化物酶GPX/(U/mL) 888.89b 915.56b 995.56ab 1 062.17a 986.67ab 19.64 0.018
超氧化物歧化酶SOD/(U/mL) 81.67 86.58 90.48 94.75 91.93 1.67 0.072
总抗氧化能力T-AOC/(U/mL) 0.45 0.46 0.49 0.52 0.51 0.06 0.324
42日龄42 days of age
过氧化氢酶CAT/(U/mL) 25.75c 27.01bc 30.99ab 33.76a 32.64a 0.88 0.004
丙二醛MDA/(nmol/mL) 3.88a 3.37a 3.16ab 2.66b 3.61a 0.13 0.013
谷胱甘肽过氧化物酶GPX/(U/mL) 763.53 776.93 790.32 794.79 833.86 18.10 0.791
超氧化物歧化酶SOD/(U/mL) 80.72b 87.07b 91.85b 110.86a 108.35a 3.16 <0.001
总抗氧化能力T-AOC/(U/mL) 0.62 0.65 0.66 0.67 0.66 0.01 0.154

2.4 益生菌与酸化剂联用对肉鸡肠道形态结构的影响

由表6可知,与CON组相比,ACI组肉鸡21日龄空肠V/C显著提高(P<0.05),ACI+BL组、ACI+BC组和ACI+CB组21和42日龄空肠和回肠V/C显著提高(P<0.05);此外,ACI+BL组和ACI+BC组21日龄回肠VH显著提高(P<0.05)。与ACI组相比,ACI+BL组、ACI+BC组和ACI+CB组肉鸡42日龄回肠V/C显著提高(P<0.05),ACI+BC组21日龄回肠VH和ACI+CB组42日龄空肠V/C显著提高(P<0.05)。
表6 益生菌与酸化剂联用对肉鸡肠道形态结构的影响

Table 6 Effects of probiotics combined with acidifiers on intestinal morphology and structure of broilers

项目
Items		 组别Groups 均值标准误
SEM		 P值
P-value
CON ACI ACI+BL ACI+BC ACI+CB
21日龄21 days of age
十二指肠
Duodenum		 绒毛高度VH/μm 1 227.22 1 283.29 1 303.94 1 327.47 1 298.66 14.05 0.298
隐窝深度CD/μm 245.91 232.11 225.99 226.87 213.19 5.45 0.486
绒隐比V/C 5.07 5.59 5.78 5.89 6.11 0.12 0.056
空肠
Jejunum		 绒毛高度VH/μm 1 114.36 1 159.55 1 181.28 1 196.87 1 177.37 14.45 0.519
隐窝深度CD/μm 205.86 197.27 195.04 187.23 184.43 3.30 0.339
绒隐比V/C 5.42b 6.01a 6.10a 6.39a 6.40a 0.10 0.019
回肠
Ileum		 绒毛高度VH/μm 816.45c 840.84bc 895.48ab 905.66a 859.80abc 10.55 0.027
隐窝深度CD/μm 157.13 152.25 153.31 152.39 145.55 1.80 0.489
绒隐比V/C 5.21b 5.53ab 5.84a 5.95a 5.92a 0.08 0.005
42日龄42 days of age
十二指肠
Duodenum		 绒毛高度VH/μm 1 464.36 1 473.76 1 482.50 1 497.65 1 498.92 4.70 0.076
隐窝深度CD/μm 243.97 241.52 237.02 227.31 230.50 3.60 0.632
绒隐比V/C 6.01 6.13 6.26 6.62 6.51 0.10 0.277
空肠
Jejunum		 绒毛高度VH/μm 1 503.35 1 514.43 1 540.23 1 556.49 1 539.95 8.90 0.329
隐窝深度CD/μm 241.05 228.14 214.56 212.22 207.15 4.29 0.057
绒隐比V/C 6.28c 6.64bc 7.23ab 7.34ab 7.46a 0.14 0.014
回肠
Ileum		 绒毛高度VH/μm 1 103.50 1 142.07 1 147.86 1 155.39 1 150.00 8.59 0.224
隐窝深度CD/μm 210.85 205.40 200.83 204.05 201.18 2.31 0.639
绒隐比V/C 5.24b 5.57b 5.72a 5.67a 5.72a 0.06 0.028

2.5 益生菌与酸化剂联用对肉鸡肠道消化酶活性的影响

由表7可知,与CON组相比,ACI组肉鸡42日龄空肠脂肪酶活性显著提高(P<0.05),ACI+BC组和ACI+BL组42日龄空肠脂肪酶和胰蛋白酶活性均显著提高(P<0.05);与ACI组相比,ACI+BC组42日龄空肠胰蛋白酶活性显著提高(P<0.05)。
表7 益生菌与酸化剂联用对肉鸡肠道消化酶活性的影响

Table 7 Effects of probiotics combined with acidifiers on intestinal digestive enzyme activities of broilers

项目
Items		 组别Groups 均值标准误
SEM		 P值
P-value
CON ACI ACI+BL ACI+BC ACI+CB
21日龄21 days of age
十二指肠
Duodenum		 淀粉酶
Amylase/(U/mg prot)		 0.51 0.74 0.97 1.11 0.92 0.07 0.063
脂肪酶
Lipase/(U/g prot)		 26.29 28.82 32.22 33.16 32.78 0.87 0.056
胰蛋白酶
Trypsin/(U/mg prot)		 3 157.23 3 763.11 4 161.06 4 480.27 4 544.32 188.95 0.079
空肠
Jejunum		 淀粉酶
Amylase/(U/mg prot)		 0.72 0.94 0.95 1.08 0.87 0.06 0.441
脂肪酶
Lipase/(U/g prot)		 20.93 24.76 22.52 31.46 22.71 1.75 0.338
胰蛋白酶
Trypsin/(U/mg prot)		 4 226.20 4 410.37 4 491.17 5 461.29 5 039.20 223.14 0.429
项目
Items		 组别Groups 均值标准误
SEM		 P值
P-value
CON ACI ACI+BL ACI+BC ACI+CB
回肠
Ileum		 淀粉酶
Amylase/(U/mg prot)		 0.94 1.21 1.31 1.61 1.63 1.08 0.393
脂肪酶
Lipase/(U/g prot)		 29.06 33.87 35.27 34.47 35.19 1.64 0.756
胰蛋白酶
Trypsin/(U/mg prot)		 6 506.98 7 357.66 7 985.47 8 300.95 7 842.95 261.11 0.277
42日龄42 days of age
十二指肠
Duodenum		 淀粉酶
Amylase/(U/mg prot)		 0.85 0.90 1.24 1.25 0.96 0.06 0.108
脂肪酶
Lipase/(U/g prot)		 81.32 88.80 94.73 105.24 104.98 4.19 0.303
胰蛋白酶
Trypsin/(U/mg prot)		 8 119.05 8 430.48 9 287.42 9 745.44 9 738.02 258.98 0.103
空肠
Jejunum		 淀粉酶
Amylase/(U/mg prot)		 1.07 1.11 1.59 1.43 1.63 0.12 0.497
脂肪酶
Lipase/(U/g prot)		 74.30b 109.16a 116.02a 121.35a 98.91ab 5.42 0.023
胰蛋白酶
Trypsin/(U/mg prot)		 8 237.77c 9 108.22bc 10 225.28ab 10 849.10a 9 799.23abc 288.04 0.040
回肠
Ileum		 淀粉酶
Amylase/(U/mg prot)		 1.77 1.85 2.19 2.40 2.37 1.90 0.133
脂肪酶
Lipase/(U/g prot)		 81.12 88.52 92.93 99.61 102.47 3.31 0.286
胰蛋白酶
Trypsin/(U/mg prot)		 8 763.72 9 344.43 9 825.51 9 890.74 9 576.01 184.12 0.315

2.6 益生菌与酸化剂联用对42日龄肉鸡空肠ZO-1和occludin表达的影响

如图1所示,与CON组相比,ACI组、ACI+BL组、ACI+BC组和ACI+CB组肉鸡42日龄空肠黏膜ZO-1的mRNA相对表达量显著提高(P<0.05);与ACI组相比,ACI+BC组42日龄空肠黏膜ZO-1的mRNA相对表达量显著提高(P<0.05)。各组之间肉鸡空肠黏膜occludin的mRNA相对表达量无显著差异(P>0.05)。
图1 益生菌与酸化剂联用对42日龄肉鸡空肠ZO-1和occludin表达的影响

数据柱标注不同字母表示差异显著(P<0.05),相同字母或者无字母表示差异不显著(P>0.05)。

Fig.1 Effects of probiotics combined with acidifiers on ZO-1 and occludin expression in jejunum of broilers at 42 days of age

Value columns with different letters mean significant difference (P<0.05), while with the same letter or no letter mean no significant difference (P>0.05).

2.7 益生菌与酸化剂联用对42日龄肉鸡空肠Nrf2抗氧化通路和NF-κB炎症通路相关基因表达的影响

由表8可知,ACI组与CON组之间肉鸡空肠Nrf2抗氧化通路和NF-κB炎症通路相关基因的mRNA相对表达量无显著差异(P>0.05)。与CON组相比,ACI+BC组和ACI+CB组空肠黏膜Nrf2的mRNA相对表达量显著提高(P<0.05),ACI+BC组和ACI+CB组TNF-α的mRNA相对表达量显著降低(P<0.05)。此外,与CON组和ACI组相比,ACI+BC组空肠SOD和IL-10的mRNA相对表达量显著提高(P<0.05),而空肠NF-κB的mRNA相对表达量显著降低(P<0.05)。
表8 益生菌与酸化剂联用对42日龄肉鸡空肠Nrf2抗氧化通路和NF-κB炎症通路相关基因表达的影响

Table 8 Effects of probiotics combined with acidifiers on expression of genes related to Nrf2 antioxidant pathway and NF-κB inflammatory pathway in jejunum of broilers at 42 days of age

项目
Items		 组别Groups 均值标准误
SEM		 P值
P-value
CON ACI ACI+BL ACI+BC ACI+CB
核因子E2相关因子Nrf2 1.00b 1.07ab 1.13ab 1.35a 1.32a 0.05 0.040
过氧化氢酶CAT 1.00 1.06 1.12 1.12 1.09 0.02 0.090
超氧化物歧化酶SOD 1.00b 1.03b 1.04b 1.21a 1.05b 0.02 0.007
谷胱甘肽过氧化物酶GPX 1.00 1.02 1.05 1.08 1.05 0.03 0.879
核因子-κB NF-κB 1.00a 0.96a 0.79ab 0.67b 0.83ab 0.04 0.047
肿瘤坏死因子-α TNF-α 1.00a 0.81ab 0.77ab 0.65b 0.69b 0.04 0.018
白细胞介素-1β IL-1β 1.00 0.89 0.92 0.88 0.88 0.03 0.666
白细胞介素-6 IL-6 1.00 0.82 0.72 0.77 0.73 0.04 0.142
白细胞介素-10 IL-10 1.00b 1.03b 1.18ab 1.27a 1.22ab 0.04 0.041

3 讨论

3.1 益生菌与酸化剂联用对肉鸡生长性能的影响

Ragaa等[12]研究发现,在肉鸡饲粮中使用富马酸可以提高其ADG,并降低F/G。许丽惠[13]研究表明,使用复合酸化剂可显著提高黄羽肉鸡的终末体重。本研究表明,在饲粮中添加酸化剂可提高肉鸡1~21日龄ADG。Salehi等[8]研究表明,丙酸和芽孢杆菌混合物联用可显著提高亚洲鲈鱼的饲料转化率。Fatufe等[14]研究证实,饲喂含有有机酸和益生菌混合物的饲粮对提高肉鸡ADFI和饲料转化率具有显著效果。然而,也有研究人员发现,联合使用酸化剂和益生菌并不能改善肉鸡生长性能[15]。这种差异可能是由于添加剂量、酸化剂和益生菌的种类以及试验环境等不同所导致的。在本试验中,与CON组相比,“酸化剂+地衣芽孢杆菌”的组合并不能改善肉鸡的生长性能,而酸化剂与凝结芽孢杆菌或丁酸梭菌联合使用均提高了肉鸡的ADG,并降低了F/G。此外,本研究还发现,酸化剂与凝结芽孢杆菌的组合在提高肉鸡生长性能方面表现出了最佳的效果。

3.2 益生菌与酸化剂联用对肉鸡免疫器官指数的影响

免疫器官的相对重量可以用来反映动物免疫状态[16]。Yang等[17]研究发现,在肉仔鸡的饲粮中添加酸化剂可显著提高其脾脏指数。在本试验中,ACI组和CON组之间肉鸡的免疫器官指数并无显著差异,这与许金根等[18]报道的结果一致。产生这种差异的原因或许是试验中选用的酸化剂种类不同引起的。本研究表明,酸化剂与地衣芽孢杆菌或凝结芽孢杆菌联合使用对21日龄肉鸡的法氏囊指数具有显著提高作用,但3种益生菌与酸化剂的组合对42日龄肉鸡的免疫器官指数无显著作用,这可能是由于肉鸡早期免疫力低下,免疫系统尚处于快速发育阶段,对于营养调控更加敏感所致。因此,益生菌与酸化剂联合使用可促进早期肉鸡免疫器官的发育,从而提高其免疫能力,利于肉鸡的健康生长。然而,不同的益生菌与酸化剂配伍的效果有明显差异,本试验条件下凝结芽孢杆菌与酸化剂的组合表现出了较好的效果。

3.3 益生菌与酸化剂联用对肉鸡抗氧化能力的影响

抗氧化酶活性反映了机体对氧化应激的抵抗水平,与动物的免疫功能亦密切相关。本研究观察到酸化剂对提高肉鸡抗氧化能力无显著影响,这与Wang等[19]的研究结果一致。Wu等[20]在哺乳母猪上的研究表明,益生菌(成分为乳酸杆菌和酵母菌)与复合酸化剂联用可显著提高其血清SOD活性。Salehi等[8]发现丙酸与芽孢杆菌混合物联用可显著提高鲈鱼肝脏中谷胱甘肽硫转移酶的活性。本研究表明,地衣芽孢杆菌、凝结芽孢杆菌或丁酸梭菌与酸化剂联合应用增强了肉鸡的抗氧化能力。此外,数据亦显示,凝结芽孢杆菌或丁酸梭菌与酸化剂组合在提高抗氧化能力方面的效果更佳,这可能与凝结芽孢杆菌可产生具有极强抗氧化活性的胞外多糖及丁酸梭菌可产生消除活性氧并增强抗氧化酶活性的氢气有关[21-22]。

3.4 益生菌与酸化剂联用对肉鸡肠道形态结构的影响

VH和V/C提高以及CD降低可作为评估肠道完整性的重要标准[23]。Giannenas等[24]研究发现,饲喂含有0.3%苯甲酸的饲粮可提高肉鸡空肠VH。沈一茹等[25]研究发现,酸化剂可提高肉鸡42日龄空肠V/C。本试验表明,酸化剂显著提高了肉鸡空肠V/C。Elhassan等[26]研究发现,酸化剂与益生菌联用对肉鸡小肠形态无显著影响;而另一项研究发现,有机酸与益生菌(主要成分为产孢乳杆菌和酿酒酵母)联用可提高其小肠VH[27]。出现这些差异的原因可能是试验中使用的酸化剂和益生菌类型不同所导致的。本研究表明,3种益生菌和酸化剂联合使用均显著改善了肉鸡空肠和回肠形态结构。在鱼上的研究观察到,与单独使用酸化剂相比,酸化剂与益生菌联合使用可显著提高其小肠VH和降低CD[28]。与此一致,本试验结果表明,与单独使用酸化剂相比,凝结芽孢杆菌或丁酸梭菌与酸化剂联合使用对改善肉鸡空肠和回肠形态结构具有显著的促进作用。此外,本研究还发现,酸化剂与凝结芽孢杆菌的组合对改善小肠形态结构具有最佳效果。

3.5 益生菌与酸化剂联用对肉鸡肠道消化酶活性的影响

消化酶活性的高低对营养物质消化及动物的生长具有重要意义[29]。刘新泽等[30]研究发现,酸化剂可提高肉鸡腺胃和肌胃胃蛋白酶活性。本研究表明,饲粮中添加酸化剂可提高肉鸡空肠脂肪酶活性。前人研究表明,益生菌与复合酸化剂(富马酸、甲酸、丙酸和柠檬酸)联合使用对增强肉鸡小肠的消化酶活性无显著效果[31]。然而,本试验观察到,相较于CON组,酸化剂与地衣芽孢杆菌或凝结芽孢杆菌联合使用可显著增强空肠脂肪酶和胰蛋白酶活性,这与Kalantarian等[28]在鱼上的研究结果类似。此外,本研究亦发现,与酸化剂相比,酸化剂与凝结芽孢杆菌的组合可显著增强肉鸡空肠胰蛋白酶活性。综合来看,在本试验条件下,酸化剂与凝结芽孢杆菌组合在提高小肠消化酶活性方面效果最佳。

3.6 益生菌与酸化剂联用对肉鸡空肠紧密连接蛋白相关基因表达的影响

ZO-1和occludin是肠道黏膜中最重要的紧密连接蛋白,在维持肠道屏障功能方面起着至关重要的作用[32]。本试验发现,饲粮中添加酸化剂可上调肉鸡空肠黏膜ZO-1的mRNA相对表达量,这与前人的研究结果[33]一致。蒲俊宁[34]研究发现,苯甲酸与凝结芽孢杆菌组合可显著提高仔猪空肠黏膜occludin的mRNA相对表达量。本研究表明,酸化剂与地衣芽孢杆菌、凝结芽孢杆菌或丁酸梭菌联用均可提高空肠黏膜ZO-1的mRNA相对表达量,但对空肠黏膜occludin的mRNA相对表达量无显著影响。此外,本研究还观察到,相比单独使用酸化剂,酸化剂与凝结芽孢杆菌联合使用可显著提高空肠黏膜ZO-1的mRNA相对表达量,提示酸化剂和凝结芽孢杆菌的组合在保护肠道屏障方面具有更佳效果。

3.7 益生菌与酸化剂联用对42日龄肉鸡空肠Nrf2抗氧化通路和NF-κB炎症通路相关基因表达的影响

增强肠道抗氧化能力对维持其结构完整性至关重要[35]。Nrf2是调控SOD、CAT等抗氧化酶基因表达的关键转录因子,Nrf2信号通路表达情况与抗氧化能力密切相关[36]。Bai等[35]报道称,枯草芽孢杆菌可提高肉鸡空肠中Nrf2和SOD的mRNA表达水平。体外研究显示,凝结芽孢杆菌可通过激活Nrf2信号通路来上调CAT和SOD mRNA表达水平,从而缓解氧化应激[37]。然而,关于益生菌与酸化剂联用对肉鸡小肠Nrf2信号通路的影响鲜见报道。本研究发现,酸化剂与凝结芽孢杆菌或丁酸梭菌联用可显著提高肉鸡空肠黏膜Nrf2的mRNA相对表达量;另外,酸化剂与凝结芽孢杆菌联用还可上调肉鸡空肠黏膜SOD的mRNA相对表达量,提示“酸化剂+凝结芽孢杆菌”的组合可能具有激活Nrf2信号通路,提高肠道抗氧化能力的作用。NF-κB作为转录因子可调控多种炎症相关分子的表达,在免疫炎症反应中起着关键作用[38]。前人研究表明,Nrf2信号通路的激活可抑制NF-κB信号通路,上调抗炎因子基因[白细胞介素-4(IL-4)和IL-10]的表达和下调促炎因子基因(IL-1β和TNF-α)的表达,从而增强机体免疫力[39]。Jiang等[40]研究发现,脑受损的小鼠在敲除Nrf2后,NF-κB的活性增强,进而导致炎症因子IL-6、TNF-α和IL-1β水平的提高。本研究发现,酸化剂与凝结芽孢杆菌或丁酸梭菌联用可显著下调肉鸡空肠TNF-α的mRNA相对表达量,这可能与Nrf2信号通路的激活有关。蒲俊宁[34]研究表明,苯甲酸与凝结芽孢杆菌组合使用可降低大肠杆菌攻毒仔猪空肠黏膜NF-κB p65表达水平。本研究亦发现,酸化剂与凝结芽孢杆菌联用可显著下调NF-κB的mRNA相对表达量,提示“酸化剂+凝结芽孢杆菌”的组合在抑制NF-κB通路激活和降低肠道炎症反应方面具有较优的效果。综合上述结果,酸化剂与凝结芽孢杆菌联合使用可能通过激活Nrf2信号通路和抑制NF-κB通路激活来改善肠道健康,但仍需开展进一步研究。

4 结论

① 益生菌与酸化剂联用能够提高肉鸡生长性能、免疫力和抗氧化能力,改善肠道健康,且效果优于单独使用酸化剂。
② 益生菌与酸化剂联用改善肠道健康的机制可能与其上调紧密连接蛋白相关基因表达量、激活Nrf2信号通路和抑制NF-κB信号通路过度活化有关。
③ 在本试验条件下,凝结芽孢杆菌与酸化剂联合使用表现出更佳效果。

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