Chinese Journal of Animal Nutrition >

2023 , Vol. 35 >Issue 11: 7036 - 7048

DOI: https://doi.org/10.12418/CJAN2023.641

Original article

Effects of Tannic Acid on Growth Performance, Antioxidant Capacity and Intestinal Morphology of Broilers Co-Infected with Coccidia and Clostridium perfringens

  • XU Pengtao , 1 ,
  • CHEN Yabing 2 ,
  • CHEN Jing 1 ,
  • HE Lai 1 ,
  • LIU Chengao 1 ,
  • GUO Shuangshuang 1 ,
  • ZHANG Zhengfan , 1, ** ,
  • DING Binying , 1, **
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  • 1 Hubei Key Laboratory of Animal Nutrition and Feed Science, Engineering Research Center of Feed Protein Resources on Agricultural By-Products of Ministry of Education, Wuhan Polytechnic University, Wuhan 430023, China
  • 2 Tianmen Agricultural and Rural Bureau, Tianmen 431700, China
** ZHANG Zhengfan, associate professor, E-mail: ; DING Binying, professor, E-mail:

*Contributed equally

Received date: 2023-05-31

  Online published: 2023-11-12

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Abstract

This study was conducted to investigate the effects of tannic acid on growth performance, organ indexes, serum biochemical indices, serum and liver antioxidant indices and intestinal morphology of broilers co-infected with coccidia and Clostridium perfringens. A total of 294 one-day-old Arbor Acres broilers were randomly divided into 3 groups with 7 replicates in each group and 14 birds in each replicate. Treatments were as follows: broilers in control group (CON group) and co-infected group (CCP group) were fed a basal diet, and those in tannic acid+co-infected group (CTA group) were fed the basal diet supplemented with 1 000 mg/kg hydrolyzed tannic acid (content≥80%). The experiment lasted for 28 d. Broilers in the CCP and CTA groups were infected with coccidia on 7 and 10 days of age, and infected with Clostridium perfringens during 16 to 20 days of age. The results showed as follows: 1) compared with the CON group, the average body weight gain and average daily feed intake during 1 to 14, 15 to 21 and 1 to 28 days of age in the CCP group were significantly decreased (P<0.05), and the feed/gain ratio was significantly increased (P<0.05). Compared with the CCP group, supplementation of 1 000 mg/kg tannic acid had not significant improvement on the growth performance decreasing of broilers after co-infection with coccidia and Clostridium perfringens. 2) Compared with the CON group, the liver index was significantly increased and the thymus index was significantly decreased in the CCP and CTA groups on 14 days of age (P<0.05); the liver index in the CTA group and the spleen index in the CCP group were significantly increased on 28 days of age (P<0.05). 3) The contents of serum total cholesterol (TC) and high-density lipoprotein (HDL) on 14 days of age and serum HDL content on 28 days of age in the CCP and CAT groups were significantly lower than those in the CON group (P<0.05), and the activities of γ-glutamyl transferase (GGT) and lactate dehydrogenase (LDH) on 21 days of age were significantly higher than those in the CON group (P<0.05). 4) The activity of serum total superoxide dismutase (T-SOD) in serum on 14 and 21 days of age and the activities of serum glutathione peroxidase (GSH-Px) and catalase (CAT) on 21 days of age were highest in the CTA group, and significantly higher than those in the CCP group (P<0.05). On 14 and 28 days of age, the serum hydrogen peroxide (H2O2) content in the CTA group was significantly lower than that in the CCP group (P<0.05), but had no significant differences between CTA and CON groups (P>0.05). 5) The liver CAT activity on 14 and 21 days of age and the liver T-SOD activity on 21 and 28 days of age were significantly increased in the CTA group compared with the CCP group (P<0.05). The contents of liver H2O2 and MDA on 14 and 28 days of age and the content of liver H2O2 on 21 days of age in the CON and CTA groups were significantly lower than those in the CCP group (P<0.05). 6) The villus height (VH) and villus height/crypt depth (V/C) of duodenum on 14 days of age in the CTA group were significantly increased and the crypt depth (CD) of duodenum and jejunum was significantly decreased compared with the CON and CCP groups (P<0.05). Compared with the CON group, the VH and V/C of duodenum, jejunum and ileum on 21 and 28 days of age were significantly decreased and the CD of duodenum and jejunum was significantly increased in the CCP group (P<0.05). In conclusion, the co-infection of coccidia and Clostridium perfringens can reduce the growth performance and antioxidant capacity, and cause intestinal morphological structure damage of broilers. Although dietary supplementation with 1 000 mg/kg tannic acid tannins cannot improve the growth performance of broilers co-infected with coccidia and Clostridium perfringens, it can improve the antioxidant capacity, and repair the intestinal morphological structure damage of broilers co-infected with coccidia and Clostridium perfringens.

Key words： broilers; coccidia; Clostridium perfringens; tannic acid

Cite this article

XU Pengtao , CHEN Yabing , CHEN Jing , HE Lai , LIU Chengao , GUO Shuangshuang , ZHANG Zhengfan , DING Binying . Effects of Tannic Acid on Growth Performance, Antioxidant Capacity and Intestinal Morphology of Broilers Co-Infected with Coccidia and Clostridium perfringens[J]. Chinese Journal of Animal Nutrition, 2023 , 35(11) : 7036 -7048 . DOI: 10.12418/CJAN2023.641

坏死性肠炎是肉鸡养殖中常见的传染性消化道疾病,主要由A型和G型产气荚膜梭菌引起,通常与球虫病一起发生或由球虫病继发感染,造成肉鸡食欲减退、肠道出血和溃疡、腹泻率增加,生长性能下降,急性感染可导致鸡群大量死亡,造成巨大经济损失[1⇓-3]。在我国饲料禁抗、养殖过程限抗和减抗的时代背景下,寻找天然、绿色的饲料添加剂防控家禽坏死性肠炎迫在眉睫。单宁酸(tannic acid,TA)是一类多酚类化合物,广泛存在于五倍子、栗木和高粱等植物中,具有抗炎、抗氧化、抗菌和抗腹泻等多种功效[4]。研究表明,饲粮中添加水解单宁酸可通过改善营养物质消化吸收率提高饲料转化效率,改善肉鸡生长性能,还可以通过清除自由基降低氧化应激,提高肉鸡抗氧化能力,并能够防止肝脏代偿性增大[5⇓⇓-8]。但是单宁酸是否能通过促进肠道发育和提高抗氧化能力改善球虫和产气荚膜梭菌混合感染引起的坏死性肠炎尚不明确。因此,本研究旨在探讨单宁酸对球虫和产气荚膜梭菌混合感染肉鸡生长性能、器官指数、血清生化指标、血清和肝脏抗氧化指标以及肠道形态结构的影响,为单宁酸对肉鸡坏死性肠炎的防护提供一定数据参考和理论支撑。

1 材料与方法

1.1 试验材料

产气荚膜梭菌由中国兽医微生物菌种保藏管理中心(CVCC2030)提供。球虫四价活疫苗购自佛山市某生物技术有限公司。水解单宁酸(含量≥80%)由湖北省某生物科技有限公司提供。

1.2 试验设计

试验采用单因素完全随机设计,选取平均体重为(46.40±0.40) g的1日龄爱拔益加(AA)肉仔鸡294只,随机分为3组,分别为对照组(CON组)、混合感染组(CCP组)和单宁酸+感染组(CTA组),每组7个重复,每个重复14只,公母各占1/2。CON组、CCP组饲喂基础饲粮,CTA组在基础饲粮中添加1 000 mg/kg水解单宁酸,试验期为28 d。基础饲粮参照《Arbor Acres Broiler Nutrition Specifications(2019)》并结合实际配制,其组成及营养水平见表1。其中,粗蛋白质(CP)、钙(Ca)含量分别参照GB/T 6432—2018、GB/T 6436—2018的方法测定;分别参照GB/T 6437—2018与苏琪等[9]的方法测定总磷(TP)和植酸磷(PP)含量,计算得出非植酸磷(NPP)含量;代谢能(ME)和可消化氨基酸含量根据《中国饲料成分及营养价值表(2021年第32版)》中数据计算得出。在第7天和第10天,CCP组和CTA组每只鸡按照球虫疫苗制造商推荐剂量的30倍灌服1 mL球虫悬液(灭菌生理盐水配制,含3×104个孢子囊/mL),CON组灌服1 mL灭菌生理盐水。试验第16~20天,CCP组和CTA组每只鸡每天灌服1 mL产气荚膜梭菌新鲜菌液(活菌数为1×108 CFU/mL),CON组灌服1 mL灭菌疱肉培养基。肉鸡自由采食,充足饮水,按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(风干基础)

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

项目
Items		 1~14日龄
1 to 14
days of age		 15~28日龄
15 to 28
days of age
原料Ingredients
玉米Corn 10.00 10.00
小麦Wheat 55.42 58.90
豆粕Soybean meal 23.50 19.37
鱼粉Fish meal 5.00 5.00
大豆油Soybean oil 2.50 3.80
磷酸氢钙CaHPO4 1.05 0.75
石粉Limestone 1.00 0.80
食盐NaCl 0.35 0.35
L-赖氨酸盐酸盐L-Lys·HCl 0.35 0.25
DL-蛋氨酸DL-Met 0.20 0.15
D-苏氨酸D-Thr 0.15 0.15
氯化胆碱Choline chloride 0.25 0.25
预混料Premix1) 0.23 0.23
合计Total 100.00 100.00
营养水平Nutrient levels2)
代谢能ME/(MJ/kg) 12.20 12.70
粗蛋白质CP 21.53 20.14
钙Ca 0.96 0.86
非植酸磷NPP 0.45 0.40
可消化赖氨酸DLys 1.25 1.05
可消化蛋氨酸DMet 0.53 0.46
可消化苏氨酸DThr 0.81 0.76
可消化色氨酸DTrp 0.23 0.22

1)预混料为每千克饲粮提供The premix provided the following per kg of diets:Cu 10 mg,Zn 100 mg,Fe 80 mg,Mn 100 mg,Se 0.3 mg,I 0.7 mg,VA 12 000 IU,VD3 3 000 IU,VK3 3.2 mg,VB1 3 mg,VB2 8.0 mg,VB12 0.025 mg,VE 44 IU,生物素 biotin 0.032 5 mg,叶酸 folic acid 2.00 mg,泛酸 pantothenic acid 15 mg,尼克酸 nicotinic acid 15 mg。

2)非植酸磷、代谢能和可消化氨基酸为计算值,粗蛋白质和钙为实测值。NPP, ME and digestible amino acids were calculated values, while CP and Ca were measured values.

1.3 样品采集

试验第14、21和28天从每个重复随机选取接近平均体重的2只鸡,用抗凝的真空采血管[抗凝剂:乙二胺四乙酸(EDTA)和肝素钠]翅下静脉采血5 mL,采血后颈动脉放血致死。将血液常温送至实验室,4 ℃条件下3 500 r/min离心10 min,取上清分装于干净的EP管中,置于-80 ℃冰箱冷冻储存;使用剪刀和镊子打开腹腔进行屠宰取样,解剖分离出肝脏、脾脏、十二指肠、空肠、回肠、胸腺和法氏囊,将肝脏、脾脏、胸腺和法氏囊剔除脂肪后进行称重;再取十二指肠、空肠、回肠中段1 cm的肠段置于4%的多聚甲醛液中进行固定,然后将样品送至武汉博士德生物工程有限公司进行组织石蜡包埋,制成苏木精-伊红(HE)染色切片;将剩余的十二指肠、空肠、回肠和肝脏样品剪碎,用灭菌锡箔纸包好,标记后放入液氮速冻,之后取出保存于实验室-80 ℃冰箱备用。

1.4 检测指标和方法

1.4.1 生长性能

试验期间每日以重复为单位记录采食量和死亡情况,分别于14、21和28日龄以重复为单位称取空腹状态下肉鸡体重,计算各重复的平均体重(ABW)、平均日采食量(ADFI)、平均日增重(ADG)和料重比(F/G)。计算公式如下:
ABW=每阶段肉鸡总末重/鸡数;
ADFI=总采食量/试验天数;
ADG=总增重/试验天数;
F/G=ADFI/ADG。

1.4.2 器官指数

分别于14、21和28日龄屠宰肉鸡,分离肝脏、脾脏、胸腺和法氏囊,剔除周边组织和脂肪,用滤纸擦干血水进行称重,并计算器官指数,计算公式为:
器官指数(%)=[器官重量(g)/鸡体重(g)]×100。

1.4.3 血清生化指标

使用日立7100全自动生化分析仪检测血清中总蛋白(total protein,TP)、白蛋白(albumin,ALB)、总胆固醇(total cholesterol,TC)、甘油三酯(triglycerides,TG)、葡萄糖(glucose,GLU)、高密度脂蛋白(high-density lipoprotein,HDL)、低密度脂蛋白(low-density lipoprotein,LDL)、钙、磷、尿酸(uric acid,UA)含量以及γ-谷氨酰转移酶(γ-glutamyl transferase,GGT)、乳酸脱氢酶(lactate dehydrogenase,LDH)活性。

1.4.4 血清和肝脏抗氧化指标

采用南京建成生物工程研究所生产的试剂盒使用多功能酶标仪(Spectra Max M5,Molecular Devices,美国)测定血清和肝脏中谷胱甘肽过氧化物酶(glutathione peroxidase,GSH-Px)、过氧化氢酶(hydrogen peroxidase,CAT)、总超氧化物歧化酶(total superoxide dismutase,T-SOD)活性和总抗氧化力(total antioxidant capacity,T-AOC)以及丙二醛(malondialdehyde,MDA)和过氧化氢(hydrogen peroxide,H2O2)含量。

1.4.5 肠道形态结构

使用OLYMPSBX-41TF型光学显微镜对肠道组织切片进行观察,应用HPISA-1000高清彩色病理图文报告系统分析。每张肠道组织切片选取8~10个不同走向且相对完整的绒毛,测量该绒毛高度(VH)及其隐窝深度(CD),取平均值作为最终测量值,并计算绒毛高度/隐窝深度(V/C)。

1.5 数据统计与分析

所有数据均使用SPSS 25.0软件进行单因素方差分析,当组间差异显著时,采用Duncan氏多重比较法进行组间差异显著性分析。试验结果以平均值±标准差表示,P<0.05表示差异显著,0.05≤P<0.10表示差异有显著的趋势。

2 结果与分析

2.1 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡生长性能的影响

由表2可知,与CON组相比,球虫和产气荚膜梭菌混合感染显著降低了肉鸡14、21和28日龄的ABW以及1~14日龄、15~21日龄和1~28日龄的ADG和ADFI(P<0.05),显著提高了1~14日龄、15~21日龄和1~28日龄的F/G(P<0.05)。与CCP组相比,饲粮中添加1 000 mg/kg单宁酸对球虫和产气荚膜梭菌混合感染造成的肉鸡各阶段生长性能下降无显著改善作用(P>0.05)。
表2 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡生长性能的影响

Table 2 Effects of tannic acid on growth performance of broilers co-infected with coccidia and Clostridium perfringens

项目
Items		 CON组
CON group		 CCP组
CCP group		 CTA组
CTA group		 P值
P-value
平均体重ABW/g
1日龄1 day of age 46.30±0.40 46.54±0.42 46.43±0.40 0.549
14日龄14 days of age 339.57±17.14a 281.71±10.89b 282.00±12.32b <0.001
21日龄21 days of age 686.59±10.01a 577.41±14.72b 583.06±12.98b <0.001
28日龄28 days of age 1 184.39±22.98a 1 031.87±59.39b 1 040.79±22.04b <0.001
1~14日龄1 to 14 days of age
平均日增重ADG/g 20.94±1.12a 16.80±0.77b 16.79±0.82b <0.001
平均日采食量ADFI/g 28.23±0.95a 25.46±1.19b 25.57±4.49b 0.001
料重比F/G 1.35±0.07b 1.52±0.06a 1.52±0.04a <0.001
15~21日龄15 to 21 days of age
平均日增重ADG/g 49.60±2.10a 42.26±1.37b 43.02±1.24b <0.001
平均日采食量ADFI/g 71.15±2.72a 63.21±3.37b 63.98±0.89b <0.001
料重比F/G 1.44±0.03b 1.50±0.05a 1.49±0.04a 0.016
22~28日龄22 to 28 days of age
平均日增重ADG/g 71.12±4.15 64.92±7.18 65.39±2.39 0.058
平均日采食量ADFI/g 105.82±2.79a 102.94±4.99ab 99.34±2.26b 0.011
料重比F/G 1.49±0.06 1.60±0.11 1.52±0.05 0.067
1~28日龄1 to 28 days of age
平均日增重ADG/g 40.65±0.82a 35.19±2.12b 35.49±0.77b <0.001
平均日采食量ADFI/g 58.36±1.10a 54.27±2.19b 53.61±1.23b <0.001
料重比F/G 1.44±0.04b 1.54±0.06a 1.51±0.03a 0.001

同行数据肩标无字母或相同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)。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 small letter superscripts mean significant difference (P<0.05). The same as below.

2.2 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡器官指数的影响

由表3可知,14日龄时,与CON组相比,CCP组肉鸡肝脏指数显著提高(P<0.05),胸腺指数和法氏囊指数显著降低(P<0.05);CTA组肉鸡各器官指数与CCP组差异不显著(P>0.05)。21日龄时,CCP组肉鸡胸腺指数显著高于CON组和CTA组(P<0.05)。28日龄时,CCP组和CTA组肉鸡脾脏指数显著高于CON组(P<0.05);与CON组和CCP组相比,CTA组肉鸡肝脏指数显著提高(P<0.05)。
表3 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡器官指数的影响

Table 3 Effects of tannic acid on organ indices of broilers co-infected with coccidia and Clostridium perfringens %

项目
Items		 CON组
CON group		 CCP组
CCP group		 CTA组
CTA group		 P值
P-value
14日龄14 days of age
肝脏Liver 2.83±0.24b 3.21±0.15a 3.14±0.23a <0.001
脾脏Spleen 0.09±0.02b 0.10±0.02ab 0.11±0.03a 0.035
胸腺Thymus 0.17±0.04a 0.13±0.03b 0.14±0.03b 0.012
法氏囊Bursa of Fabricius 0.25±0.07a 0.20±0.03b 0.24±0.04ab 0.044
21日龄21 days of age
肝脏Liver 2.65±0.41 2.87±0.16 2.79±0.27 0.150
脾脏Spleen 0.09±0.05 0.10±0.02 0.10±0.02 0.933
胸腺Thymus 0.18±0.04b 0.21±0.04a 0.17±0.03b 0.017
法氏囊Bursa of Fabricius 0.23±0.07 0.24±0.05 0.22±0.05 0.683
28日龄28 days of age
肝脏Liver 2.02±0.16b 2.08±0.15b 2.23±0.21a 0.009
脾脏Spleen 0.06±0.02b 0.08±0.02a 0.08±0.02a 0.030
胸腺Thymus 0.16±0.04 0.17±0.05 0.18±0.04 0.586
法氏囊Bursa of Fabricius 0.21±0.04 0.24±0.06 0.23±0.04 0.294

2.3 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡血清生化指标的影响

由表4可知,与CON组相比,CCP组肉鸡14日龄血清ALB、TC和HDL含量显著降低(P<0.05),21日龄血清GLU、HDL和Ca含量以及28日龄血清HDL含量显著降低(P<0.05),21日龄血清GGT和LDH活性与28日龄血清磷(P)含量显著升高(P<0.05)。CTA组对肉鸡各日龄血清生化指标与CCP组相比均无显著差异(P>0.05)。
表4 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡血清生化指标的影响

Table 4 Effects of tannic acid on serum biochemical indices of broilers co-infected with coccidia and Clostridium perfringens

项目
Items		 CON组
CON group		 CCP组
CCP group		 CTA组
CTA group		 P值
P-value
14日龄14 days of age
总蛋白TP/(g/L) 2.74±0.28 2.69±0.25 2.73±0.33 0.873
白蛋白ALB/(g/L) 1.46±0.14a 1.34±0.14b 1.33±0.17b 0.042
总胆固醇TC/(mg/dL) 142.84±17.50a 127.90±17.50b 125.90±15.92b 0.024
甘油三酯TG/(mg/dL) 21.16±6.20 19.34±4.74 21.20±4.71 0.588
葡萄糖GLU/(mg/dL) 207.64±8.63 202.08±12.73 211.14±8.68 0.077
钙Ca/(mg/dL) 11.80±0.99 12.00±0.95 11.78±0.61 0.766
磷P/(mg/dL) 7.13±0.68 7.24±0.84 7.17±0.55 0.911
高密度脂蛋白HDL/(mg/dL) 133.91±13.47a 108.54±12.90b 105.98±12.20b <0.001
尿酸UA/(mg/dL) 4.17±1.24 4.03±2.07 4.07±1.53 0.975
γ-谷氨酰转移酶GGT/(U/L) 13.79±3.02 15.46±4.98 15.29±4.97 0.552
乳酸脱氢酶LDH/(U/L) 698.60±52.88 666.33±92.55 688.37±89.59 0.842
21日龄21 days of age
总蛋白TP/(g/L) 3.19±0.37 3.20±0.31 3.07±0.25 0.444
白蛋白ALB/(g/L) 1.63±0.19 1.54±0.16 1.49±0.15 0.083
总胆固醇TC/(mg/dL) 124.70±20.86 108.29±15.95 115.44±17.99 0.073
甘油三酯TG/(mg/dL) 22.76±9.12 28.92±9.76 24.61±5.04 0.141
葡萄糖GLU/(mg/dL) 223.58±11.07a 208.48±10.89b 212.61±11.49b 0.003
钙Ca/(mg/dL) 11.67±2.23a 10.30±0.55b 10.82±0.82ab 0.045
磷P/(mg/dL) 7.09±0.43 7.26±0.40 7.52±0.53 0.059
高密度脂蛋白HDL/(mg/dL) 114.86±21.01a 96.03±13.06b 102.66±13.46ab 0.016
尿酸UA/(mg/dL) 4.72±2.34 6.00±2.24 5.97±2.33 0.259
γ-谷氨酰转移酶GGT/(U/L) 16.36±3.08b 21.36±5.67a 22.14±7.06a 0.017
乳酸脱氢酶LDH/(U/L) 684.48±134.19b 808.70±108.27a 812.32±74.15a 0.019
28日龄28 days of age
总蛋白TP/(g/L) 2.69±0.24 2.73±0.29 2.78±0.28 0.680
白蛋白ALB/(g/L) 1.67±0.14 1.63±0.19 1.60±0.12 0.522
总胆固醇TC/(mg/dL) 136.30±12.27 125.33±14.51 126.77±14.54 0.086
甘油三酯TG/(mg/dL) 20.45±6.27 24.83±6.54 25.73±5.52 0.063
葡萄糖GLU/(mg/dL) 220.87±20.42 215.49±10.41 210.19±13.07 0.192
钙Ca/(mg/dL) 9.52±0.83 9.60±0.86 9.48±0.74 0.920
磷P/(mg/dL) 6.38±0.62b 7.53±0.68a 7.21±0.60a <0.001
高密度脂蛋白HDL/(mg/dL) 128.42±14.62a 116.82±15.13b 115.53±13.44b 0.044
尿酸UA/(mg/dL) 4.61±2.53 4.09±1.21 4.51±1.58 0.732
γ-谷氨酰转移酶GGT/(U/L) 16.43±3.25 18.93±3.87 18.43±4.05 0.187
乳酸脱氢酶LDH/(U/L) 776.30±146.52 808.88±130.21 746.71±177.66 0.579

2.4 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡血清和肝脏抗氧化指标的影响

由表5可知,CCP组肉鸡14日龄血清GSH-Px、CAT和T-SOD活性显著低于CON组和CTA组(P<0.05)。与CON组相比,CCP组肉鸡21日龄血清GSH-Px和CAT活性显著降低(P<0.05);与CCP组相比,CTA组肉鸡21日龄血清GSH-Px、CAT和T-SOD活性显著升高(P<0.05)。CCP组肉鸡28日龄血清CAT活性显著低于CON组和CTA组(P<0.05)。CCP组肉鸡14和28日龄血清H2O2含量显著高于CON组和CTA组(P<0.05)。
表5 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡血清抗氧化指标的影响

Table 5 Effects of tannic acid on serum antioxidant indices of broilers co-infected with coccidia and Clostridium perfringens

项目
Items		 CON组
Control group		 CCP组
CCP group		 CTA组
CTA group		 P值
P-value
14日龄14 days of age
谷胱甘肽过氧化物酶GSH-Px/(U/mL) 1 737.87±111.56a 1 473.71±121.28c 1 622.66±65.99b <0.001
过氧化氢酶CAT/(U/mL) 6.12±1.23a 4.24±1.34b 5.98±0.77a <0.001
总超氧化物歧化酶T-SOD/(U/mL) 112.76±2.57b 107.04±4.41c 117.80±3.77a <0.001
丙二醛MDA/(nmol/mL) 3.08±0.28 3.25±0.26 3.04±0.26 0.110
过氧化氢H2O2/(mmol/L) 29.24±2.78b 43.96±5.61a 30.57±6.24b <0.001
总抗氧化能力T-AOC/(mmol/L) 0.56±0.13 0.45±0.06 0.52±0.07 0.206
21日龄21 days of age
谷胱甘肽过氧化物酶GSH-Px/(U/mL) 1 746.92±60.66b 1 514.97±106.24c 2 099.93±171.7a <0.001
过氧化氢酶CAT/(U/mL) 8.08±0.62b 6.34±0.52c 8.85±0.65a <0.001
总超氧化物歧化酶T-SOD/(U/mL) 110.81±4.64ab 109.31±3.51b 113.60±2.71a 0.026
丙二醛MDA/(nmol/mL) 2.78±0.90 3.11±0.92 2.84±1.01 0.659
过氧化氢H2O2/(mmol/L) 27.94±5.38 28.68±3.60 28.56±3.69 0.906
总抗氧化能力T-AOC/(mmol/L) 0.49±0.09 0.48±0.07 0.53±0.15 0.575
28日龄28 days of age
谷胱甘肽过氧化物酶GSH-Px/(U/mL) 1 401.51±184.53 1 260.88±182.3 1 374.81±167.67 0.127
过氧化氢酶CAT/(U/mL) 6.40±0.57a 5.83±0.36b 6.34±0.22a 0.003
总超氧化物歧化酶T-SOD/(U/mL) 110.59±3.96 104.63±10.49 108.48±4.43 0.096
丙二醛MDA/(nmol/mL) 3.28±0.32 3.04±0.31 2.90±0.52 0.057
过氧化氢H2O2/(mmol/L) 25.50±3.46b 31.47±3.05a 24.47±4.93b <0.001
总抗氧化能力T-AOC/(mmol/L) 0.26±0.19 0.21±0.08 0.28±0.16 0.498
由表6可知,CCP组肉鸡14日龄肝脏CAT活性显著低于CON组和CTA组(P<0.05),同时肝脏MDA含量显著高于CON组和CTA组(P<0.05)。CCP肉鸡组21日龄肝脏CAT和T-SOD活性显著低于CON组和CTA组(P<0.05)。CCP组肉鸡28日龄肝脏T-SOD活性显著低于CON组和CTA组(P<0.05)。CCP组肉鸡各日龄肝脏H2O2含量均显著高于CON组和CTA组(P<0.05)。
表6 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡肝脏抗氧化指标的影响

Table 6 Effects of tannic acid on liver antioxidant indices of broilers co-infected with coccidia and Clostridium perfringens

项目
Items		 CON组
CON group		 CCP组
CCP group		 CTA组
CTA group		 P值
P-value
14日龄14 days of age
谷胱甘肽过氧化物酶GSH-Px/(U/mg prot) 75.07±12.83 67.91±6.26 73.31±11.93 0.198
过氧化氢酶CAT/(U/mg prot) 14.34±2.12a 12.01±1.51b 14.58±1.22a <0.001
总超氧化物歧化酶T-SOD/(U/mg prot) 795.94±79.91 770.69±58.03 816.53±53.00 0.185
丙二醛MDA/(nmol/mg prot) 0.63±0.09c 0.97±0.09a 0.76±0.11b <0.001
过氧化氢H2O2/(mmol/g prot) 9.61±0.51b 11.05±0.76a 8.31±0.63c <0.001
总抗氧化能力T-AOC/(mmol/g prot) 0.06±0.01 0.06±0.01 0.06±0.01 0.993
21日龄21 days of age
谷胱甘肽过氧化物酶GSH-Px/(U/mg prot) 58.49±4.66 56.31±16.35 63.22±13.54 0.339
过氧化氢酶CAT/(U/mg prot) 16.30±2.39a 14.90±1.74b 16.49±0.87a 0.047
总超氧化物歧化酶T-SOD/(U/mg prot) 501.44±32.06a 442.28±86.98b 513.07±88.84a 0.035
丙二醛MDA/(nmol/mg prot) 1.40±0.55 1.21±0.52 1.67±0.85 0.195
过氧化氢H2O2/(mmol/g prot) 11.36±0.86b 13.68±0.81a 10.30±1.58b <0.001
总抗氧化能力T-AOC/(mmol/g prot) 0.08±0.02 0.09±0.03 0.09±0.03 0.227
28日龄28 days of age
谷胱甘肽过氧化物酶GSH-Px/(U/mg prot) 74.07±23.05 69.95±13.27 65.74±6.60 0.508
过氧化氢酶CAT/(U/mg prot) 23.80±2.70 22.90±1.89 24.45±1.24 0.252
总超氧化物歧化酶T-SOD/(U/mg prot) 763.56±30.22a 729.82±48.41b 787.63±18.76a 0.004
丙二醛MDA/(nmol/mg prot) 1.60±0.20b 1.80±0.15a 1.32±0.27c <0.001
过氧化氢H2O2/(mmol/g prot) 11.33±0.79b 12.80±2.01a 9.82±0.95c <0.001
总抗氧化能力T-AOC/(mmol/g prot) 0.09±0.01 0.08±0.01 0.09±0.01 0.373

2.5 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡肠道形态结构的影响

由表7可知,CTA组肉鸡14日龄十二指肠VH和V/C显著高于CON组和CCP组(P<0.05),同时十二指肠和空肠CD显著低于CON组和CCP组(P<0.05)。与CON组,CCP组肉鸡21和28日龄十二指肠、空肠、回肠VH和V/C显著降低(P<0.05),同时十二指肠和空肠CD显著增加(P<0.05);与CCP组相比,CTA组肉鸡肠道形态结构得到改善。
表7 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡肠道形态结构的影响

Table 7 Effects of tannic acid on intestinal morphology of broilers co-infected with coccidia and Clostridium perfringens

项目
Items		 CON组
CON group		 CCP组
CCP group		 CTA组
CTA group		 P值
P-value
14日龄14 days of age
十二指肠Duodenum
绒毛高度VH/μm 1 125.62±108.73b 1 069.09±129.34b 1 256.58±117.18a <0.001
隐窝深度CD/μm 103.29±6.66a 98.65±7.66a 85.01±11.82b <0.001
绒毛高度/隐窝深度V/C 10.63±0.91b 10.62±1.27b 13.99±1.61a <0.001
空肠Jejunum
绒毛高度VH/μm 868.85±73.41 814.37±77.30 847.52±85.73 0.063
隐窝深度CD/μm 104.29±9.22a 107.55±2.64a 96.81±10.16b <0.001
绒毛高度/隐窝深度V/C 8.17±0.69a 7.57±0.71b 8.42±0.98a <0.001
回肠Ileum
绒毛高度VH/μm 653.40±56.70 652.03±62.58 672.78±50.44 0.408
隐窝深度CD/μm 81.74±11.47 82.47±15.55 83.85±8.66 0.839
绒毛高度/隐窝深度V/C 7.80±0.88 7.93±1.10 8.14±1.28 0.535
21日龄21 days of age
十二指肠Duodenum
绒毛高度VH/μm 1 321.99±152.20a 1 183.74±166.46b 1 387.52±193.06a <0.001
隐窝深度CD/μm 86.12±28.23c 132.83±38.40a 106.03±18.00b <0.001
绒毛高度/隐窝深度V/C 18.39±2.42a 10.39±4.05c 13.48±2.20b <0.001
空肠Jejunum
绒毛高度VH/μm 877.73±114.77a 791.10±76.87b 800.04±43.46b 0.001
隐窝深度CD/μm 106.73±26.84b 152.54±27.10a 118.43±29.60b <0.001
绒毛高度/隐窝深度V/C 8.38±2.02a 5.40±0.98c 6.53±1.22b <0.001
回肠Ileum
绒毛高度VH/μm 649.71±73.22a 607.38±9.80b 613.27±27.04b 0.002
隐窝深度CD/μm 74.90±19.80b 86.95±22.77a 87.07±16.89a 0.020
绒毛高度/隐窝深度V/C 9.32±2.76a 7.40±1.78b 7.29±1.58b 0.001
28日龄28 days of age
十二指肠Duodenum
绒毛高度VH/μm 1 301.12±168.08a 1 149.72±92.28b 1 164.52±60.95b <0.001
隐窝深度CD/μm 98.14±12.16b 144.22±16.18a 140.33±13.26a <0.001
绒毛高度/隐窝深度V/C 13.38±1.80a 8.05±0.94b 8.39±1.07b <0.001
空肠Jejunum
绒毛高度VH/μm 665.63±75.14a 608.85±104.24b 703.46±76.99a <0.001
隐窝深度CD/μm 73.18±16.35c 115.58±18.63a 102.59±16.76b <0.001
绒毛高度/隐窝深度V/C 9.41±1.81a 5.41±1.31c 7.10±1.61b <0.001
回肠Ileum
绒毛高度VH/μm 475.41±53.24a 416.24±100.09b 455.22±60.69a 0.003
隐窝深度CD/μm 67.96±20.06b 89.90±15.98a 78.62±7.49b <0.001
绒毛高度/隐窝深度V/C 7.43±2.32a 4.77±1.49b 5.68±1.10b <0.001

3 讨论

3.1 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡生长性能的影响

球虫感染可导致肉鸡肠道黏膜损伤,破坏肠道稳态,易继发感染产气荚膜梭菌[2,10-11]。产气荚膜梭菌可产生多种毒素,最终引起鸡坏死性肠炎,导致营养物质消化利用率下降,饲料转化率和体重降低[12-13]。本研究结果表明,混合感染球虫和产气荚膜梭菌后,肉鸡生长性能下降,说明肠道损伤模型构建成功[14-15]。研究表明,饲粮中添加10~300 mg/kg原花青素、葡萄籽提取物和五倍子单宁酸能显著改善肉鸡的生长性能[16⇓-18]。但也有研究表明1 000 ~2 000 mg/kg单宁酸会显著降低肉鸡的日增重和饲料转化效率[19-20]。本研究发现,1 000 mg/kg单宁酸不能改善球虫和产气荚膜梭菌混合感染引起的肉鸡生长性能下降,这与Choi等[21]和Xu等[22]的报道结果不一致。这些结果表明单宁酸的生物学效价可能呈剂量依赖效应,和单宁酸种类、提取工艺和饲粮结构密切相关。

3.2 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡器官指数的影响

胸腺、脾脏和法氏囊是家禽的主要免疫器官,肝脏是机体脂肪代谢的重要场所。研究表明,球虫感染和坏死性肠炎会导致肉鸡肠黏膜损伤,引起肉鸡肠道功能紊乱,使肠道细菌及其代谢产物易位进入肝脏[23-24]。Daneshmand等[25]研究发现,产气荚膜梭菌会刺激脾细胞导致T细胞繁殖发育。本试验表明,球虫感染后肉鸡肝脏指数提高,法氏囊指数和胸腺指数降低,可能导致肉鸡免疫力下降。本结果与童玉鑫等[7]的研究结果一致。而产气荚膜梭菌感染显著提高了肉鸡胸腺指数和脾脏指数,这与张元可[26]和陈锁[27]的研究结果不一致。其原因可能是产气荚膜梭菌刺激了胸腺和脾脏淋巴细胞繁殖发育,引起了肉鸡的代偿性调节。

3.3 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡血清生化指标的影响

血清TC、TG、LDL和HDL含量可以反映机体脂质代谢情况,过高或过低均会引起血脂异常,导致疾病发生[28]。本试验中,混合感染球虫和产气荚膜梭菌显著降低了肉鸡血清TC和HDL含量,表明球虫和产气荚膜梭菌混合感染肉鸡后可能导致脂质代谢紊乱。LDH与细胞能量代谢和ATP的产生有关,细胞受损会使LDH释放到细胞外,降低能量利用率[29]。本研究结果表明,球虫和产气荚膜梭菌混合感染引起肉鸡肠道炎症,可能导致肠上皮细胞和免疫细胞损伤,从而导致LDH释放增加。血清GGT活性能一定程度反映肝脏健康状况,肝脏受损导致肝细胞细胞膜通透性增加,GGT活性升高[30-31]。本试验结果表明,球虫和产气荚膜梭菌混合感染可能引起肉鸡肝功能紊乱,影响肝脏代谢和物质转运,从而导致生长性能下降。此外,球虫和产气荚膜梭菌混合感染降低了肉鸡血清GLU和Ca含量,导致机体糖代谢紊乱,可能是肝脏功能、肾脏功能紊乱和坏死性肠炎引起的[32]。

3.4 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡抗氧化能力的影响

动物体内抗氧化酶活性和MDA含量可反映机体抗氧化能力强弱。已有研究证明,球虫和产气荚膜梭菌混合感染可增加肉鸡体内活性氧的产生,引起机体氧化应激[22]。Li等[33]和Zhao等[34]报道,球虫和产荚膜梭菌感染肉鸡血清和肝脏中CAT、SOD和GSH-Px等酶活性降低。与前人报道一致,本试验结果表明,球虫和产荚膜梭菌混合感染显著降低了肉鸡血清和肝脏GSH、CAT和T-SOD活性,提高了血清和肝脏MDA和H2O2含量。Zhang等[35]研究表明,250和500 mg/kg五倍子单宁酸改善了黄曲霉毒素B1感染肉鸡的抗氧化能力。Xi等[5]研究发现,250 mg/kg单宁酸可以降低黄曲霉毒素B1感染肉鸡血清MDA含量,提高血清CAT和GSH-Px活性。结合以上研究结果可知,饲粮中添加1 000 mg/kg单宁酸可以改善球虫和产气荚膜梭菌混合感染引起的肉鸡抗氧化能力下降。

3.5 单宁酸对球虫和产气荚膜梭菌混合感染肉鸡肠道形态结构的影响

研究表明,球虫和产气荚膜梭菌混合感染会造成肉鸡小肠形态结构损伤,引起营养物质的消化吸收率下降[22,35⇓-37]。李军辉等[6]报道,饲粮中添加水解单宁酸显著提高了肉鸡十二指肠和空肠VH和V/C,降低了CD。Yang等[17]研究发现,饲粮中添加17 mg/kg葡萄原花青素显著改善了肉仔鸡空肠形态结构。与前人报道一致,本研究发现球虫和产气荚膜梭菌混合感染造成肉鸡小肠形态结构受损,并且饲粮中添加1 000 mg/kg单宁酸能明显改善球虫和产气荚膜梭菌混合感染肉鸡小肠形态结构。

4 结论

球虫和产气荚膜梭菌混合感染会造成肉鸡生长性能下降、抗氧化能力降低和肠道形态结构损坏,尽管饲粮中添加1 000 mg/kg单宁酸不能改善球虫和产气荚膜梭菌混合感染造成的肉鸡生长性能下降,但是可以提高球虫和产气荚膜梭菌混合感染肉鸡的抗氧化能力,修复肠道形态结构损伤。

References

Publishing order | Descend order by publishing year | Descend order by cited within
[1]
GU C Q, LILLEHOJ H S, SUN Z F, et al. Characterization of virulent netB+/tpeL+Clostridium perfringens strains from necrotic enteritis-affected broiler chicken farms[J]. Avian Diseases, 2019, 63(3):461-467.

DOI

[2]
PRESCOTT J F, SMYTH J A, SHOJADOOST B, et al. Experimental reproduction of necrotic enteritis in chickens:a review[J]. Avian Pathology, 2016, 45(3):317-322.

DOI

[3]
JOHNSON C N, HASHIM M M, BAILEY C A, et al. Feeding of yeast cell wall extracts during a necrotic enteritis challenge enhances cell growth,survival and immune signaling in the jejunum of broiler chickens[J]. Poultry Science, 2020, 99(6):2955-2966.

DOI

[4]
王俊锋, 连慧香, 付春胜, 等. 水解单宁酸的生物学功能及其在畜牧生产中的应用[J]. 饲料研究, 2022, 45(19):145-148.

WANG J F, LIAN H X, FU C S, et al. Biological function of tannic acid and its application in animal production[J]. Feed Research, 2022, 45(19):145-148. (in Chinese)

[5]
XI Y, CHEN J, GUO S S, et al. Effects of tannic acid on growth performance,relative organ weight,antioxidative status,and intestinal histomorphology in broilers exposed to aflatoxin B1[J]. Frontiers in Veterinary Science, 2022, 9:1037046.

DOI

[6]
李军辉, 解玉怀, 张少涛, 等. 饲粮中添加水解单宁酸对肉鸡生长性能及肠道健康的影响[J]. 动物营养学报, 2021, 33(5):2642-2651.

DOI

LI J H, XIE Y H, ZHANG S T, et al. Effects of dietary hydrolyzed tannic acid on growth performance and intestinal health of broilers[J]. Chinese Journal of Animal Nutrition, 2021, 33(5):2642-2651. (in Chinese)

[7]
童玉鑫, 吴淑琴, 李顺路, 等. 五倍子单宁酸对1-21日龄黄羽肉鸡生长性能、免疫及抗氧化功能的影响[J]. 中国畜牧杂志, 2022, 58(5):251-255.

TONG Y X, WU S Q, LI S L, et al. Effect of pentosidine tannic acid on growth performance,immunity and antioxidant function of yellow-finned broiler chickens from 1 to 21 days of age[J]. Chinese Journal of Animal Science, 2022, 58(5):251-255. (in Chinese)

[8]
李军, 汤莉, 黄立, 等. 单宁酸和牛至油组合对肉仔鸡生长性能、屠宰性能、肉品质和抗氧化指标的影响[J]. 饲料研究, 2022, 45(18):51-55.

LI J, TANG L, HUANG L, et al. Effect of oregano oil and tannin combination on growth performance,slaughter performance,meat quality and antioxidant index of broilers[J]. Feed Research, 2022, 45(18):51-55. (in Chinese)

[9]
苏琪, 陆肇海, 段玉琴. 植物饲料中植酸磷的含量及测定[J]. 饲料研究, 1983(4):11-13.

SU Q, LU Z H, DUAN Y Q. Content and determination of phytate phosphorus in plant feed[J]. Feed Research, 1983(4):11-13. (in Chinese)

[10]
LEUNG H, YITBAREK A, SNYDER R, et al. Responses of broiler chickens to Eimeria challenge when fed a nucleotide-rich yeast extract[J]. Poultry Science, 2019, 98(4):1622-1633.

DOI

[11]
QUIROZ-CASTAÑEDA R E, DANTÁN-GONZÁLEZ E. Control of avian coccidiosis:future and present natural alternatives[J]. BioMed Research International, 2015, 2015:430610.

[12]
常磊, 安侠. 肉鸡坏死性肠炎的发病机制、诱发因素和防治措施[J]. 家禽科学, 2022(8):39-40.

CHANG L, AN X. Pathogenesis of necroticenteritis in broiler chickens,the predisposing factors and control measures[J]. Poultry Science, 2022(8):39-40. (in Chinese)

[13]
宋瑞艳, 姜玉财, 邬方基. 探讨鸡坏死性肠炎病的防治[J]. 吉林畜牧兽医, 2020, 41(11):43.

SONG R Y, JIANG Y C, WU F J. Exploring the control of necroticenteritis disease in chickens[J]. Jilin Animal Husbandry and Veterinary Medicine, 2020, 41(11):43. (in Chinese)

[14]
PARK I, OH S, NAM H, et al. Antimicrobial activity of sophorolipids against Eimeria maxima and Clostridium perfringens,and their effect on growth performance and gut health in necrotic enteritis[J]. Poultry Science, 2022, 101(4):101731.

DOI

[15]
IBRAHIM D, ISMAIL T A, KHALIFA E, et al. Supplementing garlic nanohydrogel optimized growth,gastrointestinal integrity and economics and ameliorated necrotic enteritis in broiler chickens using a Clostridium perfringens challenge model[J]. Animals, 2021, 11(7):2027.

DOI

[16]
NIU J X, WANG Q J, JING C W, et al. Dietary galla chinensis tannic acid supplementation in the diets improves growth performance,immune function and liver health status of broiler chicken[J]. Frontiers in Veterinary Science, 2022, 9:1024430.

DOI

[17]
YANG J Y, ZHANG H J, WANG J, et al. Effects of dietary grape proanthocyanidins on the growth performance,jejunum morphology and plasma biochemical indices of broiler chicks[J]. Animal, 2017, 11(5):762-770.

DOI

[18]
WANG M L, SUO X, GU J H, et al. Influence of grape seed proanthocyanidin extract in broiler chickens:effect on chicken coccidiosis and antioxidant status[J]. Poultry Science, 2008, 87(11):2273-2280.

DOI

[19]
MANSOORI B, NODEH H, MODIRSANEI M, et al. Influence of dietary tannic acid and polyethylene glycol on growth and intestinal D-xylose absorption of broiler cockerels and activity of serum enzymes[J]. British Poultry Science, 2007, 48(4):489-495.

DOI

[20]
CENGIZ Ö, KÖKSAL B H, TATLI O, et al. Effect of dietary tannic acid supplementation in corn- or barley-based diets on growth performance,intestinal viscosity,litter quality,and incidence and severity of footpad dermatitis in broiler chickens[J]. Livestock Science, 2017, 202:52-57.

DOI

[21]
CHOI J, TOMPKINS Y H, TENG P Y, et al. Effects of tannic acid supplementation on growth performance,oocyst shedding,and gut health of in broilers infected with Eimeria maxima[J]. Animals, 2022, 12(11):1378.

DOI

[22]
XU H P, FU J Y, LUO Y M, et al. Effects of tannic acid on the immunity and intestinal health of broiler chickens with necrotic enteritis infection[J]. Journal of Animal Science and Biotechnology, 2023, 14(1):72.

DOI PMID

[23]
洪玉梅. 鸡球虫病合理防治分析[J]. 农村实用技术, 2023(2):111-112.

HONG Y M. Analysis of rational control of chicken coccidiosis[J]. Applicable Technologies for Rural Areas, 2023(2):111-112. (in Chinese)

[24]
王磊熙, 候静, 张德凯. 肠道稳态失调与肝脏疾病的关联[J]. 医学综述, 2018, 24(7):1383-1387,1392.

WANG L X, HOU J, ZHANG D K. Relationship between intestinal dysregulation and liver disease[J]. Medical Recapitulate, 2018, 24(7):1383-1387,1392. (in Chinese)

[25]
DANESHMAND A, KERMANSHAHI H, MOHAMMED J, et al. Intestinal changes and immune responses during Clostridium perfringens-induced necrotic enteritis in broiler chickens[J]. Poultry Science, 2022, 101(3):101652.

DOI

[26]
张元可. 维生素A对球虫和产气荚膜梭菌混合感染肉鸡肠道屏障和免疫功能的影响[D]. 硕士学位论文. 武汉: 武汉轻工大学, 2020.

ZHANG Y K. Effect of vitamin A on intestinal barrier and immune function in broilers co-infected with coccidia and Clostridium perfringens[D]. Master's Thesis. Wuhan: Wuhan Polytechnic University, 2020. (in Chinese)

[27]
陈锁. 枯草芽孢杆菌制剂对产气荚膜梭菌和球虫引起的肉鸡坏死性肠炎治疗效果研究[D]. 硕士学位论文. 泰安: 山东农业大学, 2021.

CHEN S. Effect of Bacillus subtilis preparation on broiler necrotizing enteritis caused by Clostridium perfringens and coccidia[D]. Master's Thesis. Tai’an: Shandong Agricultural University, 2021. (in Chinese)

[28]
王琢. 牛樟芝水提物降血脂、保肝护肝功效及相关基因表达的研究[D]. 硕士学位论文. 武汉: 华中农业大学, 2019.

WANG Z. Antihyperlipidemic and liver protecting effects of water extract from antrodia cinnamomea and study on related geen expressions[D]. Master's Thesis. Wuhan: Huazhong Agricultural University, 2019. (in Chinese)

[29]
陈军校, 梁松, 赵叶. 血清乳酸脱氢酶、转化生长因子-β1在急性淋巴细胞白血病患儿中的表达及临床意义[J]. 癌症进展, 2023, 21(5):546-548,552.

CHEN J J, LIANG S, ZHAO Y. Expression of serum lactate dehydrogenase and transforming growth factor-β1 in children with acute lymphoblastic leukemia and their clinical significance[J]. Oncology Progress, 2023, 21(5):546-548,552. (in Chinese)

[30]
陈曦, 冯杰, 程正江, 等. 血清白蛋白、血浆纤维蛋白原和血小板的检测在评估肝癌进展及预后中的价值[J]. 标记免疫分析与临床, 2022, 29(12):1981-1985.

CHEN X, FENG J, CHENG Z J, et al. The value of serum albumin,plasma fibrinogen and platelet detection in evaluating the progression and prognosis of liver cancer[J]. Labeled Immunoassays and Clinical Medicine, 2022, 29(12):1981-1985. (in Chinese)

[31]
习羽. 单宁酸和没食子酸对饲喂含黄曲霉毒素B1日粮肉鸡生长性能和抗氧化功能的影响及机制研究[D]. 硕士学位论文. 武汉: 武汉轻工大学, 2022.

XI Y. Effects and mechanism of tannins and gallic acid on growth performance and antioxidant function of broilers fed diets containing aflatoxin B1[D]. Master's Thesis. Wuhan: Wuhan Polytechnic University, 2022. (in Chinese)

[32]
朱荷云, 赵威. 血液透析对慢性肾小球肾炎导致终末期肾病患者血清钙、磷水平的影响[J]. 中国现代药物应用, 2021, 15(9):60-63.

ZHU H Y, ZHAO W. Effect of hemodialysis on serum calcium and phosphorus levels in patients with end-stage renal disease caused by chronic glomerulonephritis[J]. Chinese Journal of Modern Drug Application, 2021, 15(9):60-63. (in Chinese)

[33]
LI P, LIU C G, NIU J L, et al. Effects of dietary supplementation with vitamin A on antioxidant and intestinal barrier function of broilers co-infected with coccidia and Clostridium perfringens[J]. Animals, 2022, 12(23):3431.

DOI

[34]
ZHAO Y, ZENG D, WANG H S, et al. Dietary probiotic Bacillus licheniformis H2 enhanced growth performance,morphology of small intestine and liver,and antioxidant capacity of broiler chickens against Clostridium perfringens-induced subclinical necrotic enteritis[J]. Probiotics and Antimicrobial Proteins, 2020, 12(3):883-895.

DOI

[35]
ZHANG Z F, XI Y, WANG S T, et al. Effects of Chinese gallnut tannic acid on growth performance,blood parameters,antioxidative status,intestinal histomorphology,and cecal microbial shedding in broilers challenged with aflatoxin B1[J]. Journal of Animal Science, 2022, 100(4):skac099.

DOI

[36]
邓沛杰, 宋泽和, 罗国升, 等. 枯草芽孢杆菌对球虫和产气荚膜梭菌混合攻毒肉鸡生长性能及肠道健康的影响[J]. 动物营养学报, 2022, 34(11):7082-7093.

DOI

DENG P J, SONG Z H, LUO G S, et al. Effects of Bacillus subtilis on growth performance and intestinal health of broilers attacked by coccidia and Clostridium perfringens[J]. Chinese Journal of Animal Nutrition, 2022, 34(11):7082-7093. (in Chinese)

[37]
许笑. 丁酸梭菌改善坏死性肠炎患鸡肠黏膜屏障机制的初步研究[D]. 博士学位论文. 杨凌: 西北农林科技大学, 2022.

XU X. Preliminary studies on the roles of Clostridium butyricum for ameliorating gut mucosal barrier of broiler chickens with necrotic enteritis[D]. Ph.D.Thesis. Yangling: Northwest A&F University, 2022. (in Chinese)

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