Chinese Journal of Animal Nutrition >

2025 , Vol. 37 >Issue 9: 5897 - 5910

DOI: https://doi.org/10.12418/CJAN2025.480

RESEARCH PAPER

Effects of Dietary Schizochytrium Powder on Growth Performance, Meat Quality, Organ Development, Serum Biochemical Indexes, Oxidative Stress and Inflammatory Response of Yellow-Feathered Broilers under Heat Stress

  • GUO Xuming , 1, 2 ,
  • CHEN Jinglong 1 ,
  • LEI Chuangchuang 1 ,
  • SHAO Dan 1 ,
  • TAO Shiyu 2 ,
  • SHI Shourong , 1, *
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  • 1 Jiangsu Institute of Poultry Sciences, Yangzhou 225125, China
  • 2 College of Animal Science and Technology, Huazhong Agricultural University, Wuhan 430070, China
* professor, E-mail:

Received date: 2025-01-10

  Online published: 2025-09-12

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Abstract

This experiment was conducted to investigate the effects of dietary Schizochytrium powder on growth performance, meat quality, organ development, serum biochemical indexes, oxidative stress and inflammatory response of yellow-feathered broilers under heat stress. A total of 144 male fast yellow-feathered broilers aged at 35 days were randomly divided into 3 groups with 6 replicates in each group and 8 broilers in each replicate. Broilers in the control group (CON group) and heat stress group (HS group) were fed a basal diet, and others in the Schizochytrium powder group (SP group) were fed the basal diet supplemented with 20 g/kg Schizochytrium powder. The pre-experimental period lasted for 1 week, and the experimental period lasted for 2 weeks. After the pre-experimental period, the CON group maintained normal temperature, and HS group and SP group were treated with cyclic heat stress. The results showed that compared with the CON group, the final body weight, average daily gain, average daily feed intake, breast muscle water-holding capacity, liver index and spleen index of HS group were significantly decreased (P<0.05), the feed to gain ratio was significantly increased (P<0.05), the serum aspartate aminotransferase (AST) activity and glucose (GLU), high density lipoprotein cholesterol (HDL-C) and low density lipoprotein cholesterol (LDL-C) contents were significantly increased (P<0.05), the serum and liver superoxide dismutase (SOD) activity was significantly increased (P<0.05), the jejunum villus height/crypt depth was significantly increased (P<0.05), and the mRNA relative expression levels of NOD-like receptor thermal protein domain associated protein 3 (NLRP3) and interleukin-6 (IL-6) in liver were significantly increased (P<0.05). Compared with the HS group, the breast muscle water-holding capacity, liver index and serum, liver and jejunum malondialdehyde (MDA) content of SP group were significantly increased (P<0.05), the bursa of Fabricius index was significantly decreased (P<0.05), the serum total cholesterol (TC) and HDL-C contents and catalase (CAT) activity were significantly decreased (P<0.05), and the mRNA relative expression level of NLRP3 in liver was significantly decreased (P<0.05). In conclusion, dietary Schizochytrium powder can improve the meat quality of yellow-feathered broilers, alleviate the liver damage and inflammatory reaction caused by heat stress, improve the lipid metabolism ability, and aggravate the oxidative damage of serum, liver and jejunum under heat stress.

Key words： yellow-feathered broilers; heat stress; Schizochytrium powder; growth performance; meat quality

Cite this article

GUO Xuming , CHEN Jinglong , LEI Chuangchuang , SHAO Dan , TAO Shiyu , SHI Shourong . Effects of Dietary Schizochytrium Powder on Growth Performance, Meat Quality, Organ Development, Serum Biochemical Indexes, Oxidative Stress and Inflammatory Response of Yellow-Feathered Broilers under Heat Stress[J]. Chinese Journal of Animal Nutrition, 2025 , 37(9) : 5897 -5910 . DOI: 10.12418/CJAN2025.480

随着全球温室效应逐年增强,家禽集约化养殖所面临的热应激问题越来越严峻[1]。高温环境下动物无法有效散热,尤其家禽对热应激更为敏感[2-3]。家禽适宜的生长温度在21~26 ℃,当饲养环境温度超过32 ℃时,会出现高温应激现象,影响其组织器官的生长和发育[4]。热应激对动物生长性能和产品质量均会产生负面影响。研究表明,高温会导致家禽体内活性氧(ROS)含量增加,氧化还原反应失衡,从而导致机体的氧化损伤,诱发肠道炎症,严重影响家禽消化能力和营养吸收[5]。热应激还会导致家禽体重、采食量、产蛋率和饲料利用率的下降,从而对行业造成巨大的经济损失[6]。因此,通过调控饲粮营养来缓解热应激的不良影响对家禽养殖具有重要意义。
二十二碳六烯酸(docosahexaenoic acid,DHA)是一种机体必需的多不饱和脂肪酸,其有益作用已得到饲料营养行业的广泛关注。据报道,DHA在缓解氧化应激、抗炎、抑癌、提高免疫力等方面发挥着积极作用[7-8]。但人和动物自身无法合成DHA,只能通过鱼油或海洋微藻获得。裂殖壶菌(Schizochytrium limacinum)又名裂殖壶藻,是破囊壶菌科的一类海洋真菌,其中DHA作为主要的脂肪酸之一,占菌体油脂含量30%以上,是工业生产DHA的重要来源[9-10]。同时,裂殖壶藻本身具有较强的抗氧化活性,能防止油脂氧化[11]。研究表明,裂殖壶藻能够增强细胞抗氧化和抗炎能力,并缓解过氧化氢(H2O2)引起的氧化应激[12]。李浩洋等[13]在蛋鸡饲粮中添加1%、2%、3%的裂殖壶藻粉后,发现鸡蛋中DHA含量增加,蛋黄胆固醇含量减少。Ribeiro等[14]在肉鸡饲粮中添加74 g/kg裂殖壶藻后,发现肉鸡的生长性能显著提高,鸡肉中脂肪酸营养水平有所提高。因此,裂殖壶藻作为一种重要的DHA资源,对于鸡的生长发育起着积极的作用。本试验在黄羽肉鸡基础饲粮中添加裂殖壶藻粉,并通过建立循环热应激模型,研究其对热应激黄羽肉鸡生长性能、肉品质、器官发育、血清生化指标、氧化应激及炎症反应的影响,为其缓解家禽热应激损伤提供理论依据。

1 材料与方法

1.1 试验设计

本试验所有程序均经中国江苏省家禽科学研究所动物伦理委员会批准(编号20230109)。
选择体重相近的144只35日龄雄性快速型黄羽肉鸡(购自江苏立华牧业股份有限公司),随机分为3组,每组6个重复,每个重复8只。对照组(CON组)和热应激组(HS组)饲喂基础饲粮,裂殖壶藻粉组(SP组)在基础饲粮中添加20 g/kg裂殖壶藻粉。预试期1周,正试期2周。预试期饲粮中按正试期的比例添加裂殖壶藻粉,裂殖壶藻粉中DHA含量为20%。预试期结束后,CON组维持常温[(26±1) ℃];HS组和SP组进行循环热应激处理,设置程序为:00:00—06:00和22:00—00:00,(30±1) ℃,共8 h;06:00—10:00和18:00—22:00,(32±1) ℃,共8 h;10:00—18:00,(34±1) ℃,共8 h,循环热应激程序设定见图1。
图1 循环热应激程序设定

Fig.1 Cyclic heat stress program setting

1.2 饲养管理

试验地点为江苏省家禽科学研究所仪征基地,在动物营养代谢环控仓(北京库蓝科技有限公司)中进行,采用3层笼养,鸡笼规格为100 cm×80 cm×45 cm,保证饲养密度在0.1 m2/只左右,期间自由采食和饮水,相对湿度维持在(60±5)%,定期清理粪便,24 h光照。试验期间定期记录体重、采食量和直肠温度等。饲粮参照《黄羽肉鸡营养需要量》(NY/T 3645—2020)配制并制粒,其组成及营养水平见表1。
表1 饲粮组成及营养水平(风干基础)

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

项目
Items		 对照组
CON
group		 裂殖壶
藻粉组
SP group
原料Ingredients
玉米Corn 69.37 68.80
豆粕Soybean meal 20.00 20.00
玉米蛋白粉Corn gluten meal 5.00 4.57
大豆油Soybean oil 3.03 2.03
裂殖壶藻粉
Schizochytrium powder		 2.00
石粉Limestone 0.96 0.96
磷酸氢钙CaHPO4 0.52 0.52
微量元素预混料
Trace mineral premix1)		 0.20 0.20
DL-蛋氨酸DL-Met 0.15 0.15
L-赖氨酸L-Lys 0.29 0.29
苏氨酸Thr 0.02 0.02
精氨酸Arg 0.01 0.01
植酸酶Phytase 0.02 0.02
氯化胆碱Choline chloride 0.10 0.10
维生素预混料Vitamin premix2) 0.03 0.03
食盐NaCl 0.30 0.30
合计Total 100.00 100.00
营养水平Nutrient levels3)
粗蛋白质CP 17.00 17.00
代谢能ME/(MJ/kg) 13.18 13.18
钙Ca 0.55 0.55
总磷TP 0.42 0.42
有效磷AP 0.22 0.22

1)微量元素预混料为每千克饲粮提供 Trace mineral premix provided the following per kg of diets:Mn 60 mg,I 0.35 mg,Fe 25 mg,Cu 8 mg,Zn 50 mg。

2)维生素预混料为每千克饲粮提供 Vitamin premix provided the following per kg of diets:VA 4 000 IU,VD3 1 600 IU,VK3 1.5 mg,VB1 1.0 mg,VB2 3.0 mg,VB6 3.0 mg,VB12 0.005 mg,泛酸 pantothenic acid 8.0 mg,烟酸 nicotinic acid 20 mg,叶酸 folic acid 20 mg。

3)代谢能和有效磷为计算值,参照NY/T 3645—2020计算;粗蛋白质、钙、总磷为实测值,分别参照GB/T 6432—2018、GB/T 6436—2018、GB/T 6437—2018测定。ME and AP were calculated values, referred to NY/T 3645—2020; CP, Ca and TP were measured values, referred to GB/T 6432—2018, GB/T 6436—2018, GB/T 6437—2018, respectively.

1.3 样品采集及处理

试验结束时,各重复按平均体重选取试验鸡各1只,翅下静脉采集血液于促凝管中静置2 h,2 060×g离心10 min收集血清,用于检测血清生化及抗氧化指标;肉鸡处死后采集肝脏、脾脏、法氏囊等器官进行称重,用以计算器官指数;采集肝脏和空肠黏膜样品,置于液氮保存,用于检测空肠和肝脏抗氧化指标、空肠形态及肝脏炎症相关基因表达。

1.4 指标检测

1.4.1 生长性能

于入舍前(35日龄)、正试期前(42日龄)和热应激结束后(56日龄),定时称量试验鸡体重。同时,每日定时投喂饲粮并记录每日采食量和剩料量,计算试验期的平均日增重(ADG)、平均日采食量(ADFI)、料重比(F/G)和死淘率。

1.4.2 直肠温度

在正试期第1、4、7和14天10:00,从每个重复中随机选取1只鸡,使用兽用电子体温计(32~44 ℃,河北易牧宝科技有限公司)测定直肠温度。

1.4.3 肉品质

肉鸡屠宰后剖取左侧胸肌,在4 ℃下保存,测定屠宰后45 min和2 h胸肌的pH、系水力、嫩度、肉色[亮度(L*)、红度(a*)、黄度(b*)值]等指标。
肉色:将胸肌样品摆放平整,使用全自动色差仪贴紧胸肌表面,在相同的位置连续测量3次,结果取平均值。
pH:使用德图半固体pH计(205-pH2,德国Testo公司)分别对屠宰后45 min和24 h的胸肌样品进行pH检测,每个样品测定3次,结果取平均值。
系水力:采用滤纸挤压法测定。从每个样品中剪取5 g左右的胸肌样品,称重即为压前肉样重(m1),随后用滤纸将胸肌样品包裹好,使用压力机(YYW-2,南京土壤仪器厂有限公司)以35 kg压力持续挤压5 min,取出样品并称重,即为压后肉样重(m2)。按如下公式计算系水力:
系水力(%)=100×(m1-m2)/m1。
嫩度:取出屠宰后的胸肌样品,用塑料袋包装后放置于80 ℃恒温水浴锅进行加热,当肉品中心温度达到75 ℃时取出,冷却至室温。然后沿肌纤维方向修成长5.0 cm、宽1.0 cm、高0.5 cm的长条,使用嫩度仪进行测定,每个样品测定3次,结果取平均值。

1.4.4 器官指数

按如下公式计算器官指数:
器官指数(g/kg)=器官重(g)/活鸡重(kg)。

1.4.5 血清生化指标

使用全自动血液生化分析仪(BS280,深圳迈瑞生物医疗电子股份有限公司)测定血清谷丙转氨酶(ALT)、谷草转氨酶(AST)活性及葡萄糖(GLU)、总胆固醇(TC)、甘油三酯(TG)、高密度脂蛋白胆固醇(HDL-C)、低密度脂蛋白胆固醇(LDL-C)含量。

1.4.6 血清、肝脏和空肠抗氧化指标

使用试剂盒(南京建成生物工程研究所)测定血清、肝脏和空肠丙二醛(MDA)含量及过氧化氢酶(CAT)和超氧化物歧化酶(SOD)活性。

1.4.7 空肠形态

空肠组织经4%多聚甲醛固定后,制备成石蜡切片并进行苏木精-伊红(HE)染色,在光学显微镜(DM-1000,德国Leica Microsystems Inc公司)下测量空肠绒毛高度、隐窝深度,计算绒毛高度/隐窝深度(V/C)。

1.4.8 肝脏RNA提取及荧光定量PCR

按照RNA-easy Isolation Reagent细胞/组织总RNA提取试剂盒(货号:R701-02-AA,南京诺唯赞生物科技股份有限公司)步骤提取肝脏RNA。使用实时荧光定量PCR(RT-qPCR)试剂盒(货号:E301-01A,近岸蛋白质科技有限公司)进行RT-qPCR测定,基因引物由苏州金唯智生物科技有限公司合成,引物信息见表2。试验通过荧光定量PCR仪(美国Applied Biosystems公司)进行,以甘油醛-3-磷酸脱氢酶(GAPDH)为内参基因,使用2-△△Ct法计算肝脏热休克蛋白和炎症相关基因[热休克蛋白40(HSP40)、热休克蛋白60(HSP60)、热休克蛋白70(HSP70)、热休克蛋白90(HSP90)、Toll样受体4(TLR4)、白细胞介素-1β(IL-1β)、肿瘤坏死因子-α(TNF-α)、干扰素-γ(IFN-γ)、白细胞介素-6(IL-6)、NOD样受体热蛋白结构域相关蛋白3(NLRP3)]mRNA相对表达水平。
表2 引物信息

Table 2 Primer information

基因
Genes		 引物序列
Primer sequences (5'—3')		 产物长度
Product
length/bp		 退火温度
Annealing
Temperature/℃		 GenBank序列号
GenBank serial
number
甘油醛-3-磷酸脱氢酶
GAPDH		 F:GCCCAGAACATCATCCCA
R:CGGCAGGTCAGGTCAACA		 137 60 NM_204305.2
热休克蛋白40
HSP40		 F:CCACCAGTTATCCGTAAGTT
R:CACCACGACCTTCACATT		 101 55 XM_046935213.1
热休克蛋白60
HSP60		 F:CTGTAGAGGAAGGCATTGT
R:CAAGCATCGCATCATAGC		 231 54 NM_001012916.3
热休克蛋白70
HSP70		 F:GTGTCCATCCTTACCATTGA
R:TGCTTACGCTTGAACTCTT		 128 55 NM_001006685.2
热休克蛋白90
HSP90		 F:CACAGTCCAAGTCCATAGG
R:CATCTCTTGAGTAACGAACAC		 110 54 XM_040672816.2
Toll样受体4
TLR4		 F:GAATGACACGGACACTCTT
R:TGGTAATACGAAGCACTCTC		 197 55 NM_001030693.2
白细胞介素-1β
IL-1β		 F:AGTGAGGCTCAACATTGC
R:GTCCAGGCGGTAGAAGAT		 214 55 XM_046931582.1
肿瘤坏死因子-α
TNF-α		 F:GACAGCCTATGCCAACAA
R:TCAACGCTCCTGACTCAT		 153 55 XM_046927265.1
干扰素-γ
IFN-γ		 F:CCTTCAGCACCTCTTCAC
R:CTGTAATCGTTGTCTTGGAG		 228 54 XM_046936227.1
白细胞介素-6
IL-6		 F:CCTCCTCGCCAATCTGAA
R:CCTCACGGTCTTCTCCATA		 100 56 NM_204628.2
NOD样受体热蛋白结构域
相关蛋白3
NLRP3		 F:CACCAACCTGACCATAGC
R:ACTCCATCATCACCTTCCT		 191 55 XM_046918112.1

1.5 数据统计与分析

数据经Excel 2013进行处理后,使用SPSS 20.0的t检验进行分析(CON组vs HS组和HS组vs SP组),结果以平均值±标准误表示,P<0.05为显著差异。

2 结果

2.1 裂殖壶藻粉对热应激黄羽肉鸡生长性能的影响

如表3所示,与CON组相比,HS组肉鸡末重、平均日增重和平均日采食量均显著降低(P<0.05),料重比显著增加(P<0.05);与HS组相比,SP组肉鸡末重、平均日增重、平均日采食量和料重比均无显著差异(P>0.05)。
表3 裂殖壶藻粉对热应激黄羽肉鸡生长性能影响

Table 3 Effects of Schizochytrium powder on growth performance of yellow-feathered broilers under heat stress

项目
Items		 组别Groups P值P-value
CON HS SP CON组vs HS组
CON group vs
HS group		 HS组vs SP组
HS group vs
SP group
初重IBW/g 1 525.74±10.21 1 432.38±19.44 1 482.50±31.28 0.423 0.195
末重FBW/g 2 873.33±21.26 2 042.71±17.79# 2 141.75±49.55 <0.001 0.094
平均日增重ADG/g 67.14±0.74 41.96±2.53# 47.09±3.11 <0.001 0.221
平均日采食量ADFI/g 165.36±0.65 120.30±2.73# 124.04±4.69 <0.001 0.505
料重比F/G 2.46±0.03 2.92±0.13# 2.67±0.10 <0.001 0.158
死淘率Mortality/% 0 5.56 0

#表示CON组与HS组之间差异显著(P<0.05),*表示HS组与SP组之间差异显著(P<0.05)。下表同。

# represented significant difference between CON group and HS group (P<0.05), and * represented significant difference between HS group and SP group (P<0.05). The same as below.

2.2 裂殖壶藻粉对热应激黄羽肉鸡直肠温度的影响

如表4所示,在热应激第4、7、14天,与CON组相比,HS组肉鸡直肠温度均显著升高(P<0.05);与HS组相比,SP组肉鸡直肠温度均无显著差异(P>0.05)。
表4 裂殖壶藻粉对热应激黄羽肉鸡直肠温度的影响

Table 4 Effects of Schizochytrium powder on rectal temperature of yellow-feathered broilers under heat stress

项目
Items		 组别Groups P值P-value
CON HS SP CON组vs HS组
CON group vs
HS group		 HS组vs SP组
HS group vs
SP group
第1天Day 1 41.14±0.08 40.79±0.05# 40.76±0.07 <0.001 0.774
第4天Day 4 41.80±0.30 42.73±0.27# 42.70±0.08 0.038 0.931
第7天Day 7 42.35±0.23 43.48±0.23# 43.18±0.23 <0.001 0.378
第14天Day 14 41.81±0.07 43.71±0.19# 43.65±0.24 <0.001 0.840

2.3 裂殖壶藻粉对热应激黄羽肉鸡肉品质的影响

如表5所示,与CON组相比,HS组胸肌系水力显著降低(P<0.05);与HS组相比,SP组胸肌系水力显著升高(P<0.05)。
表5 裂殖壶藻粉对热应激黄羽肉鸡肉品质的影响

Table 5 Effects of Schizochytrium powder on meat quality of yellow-feathered broilers under heat stress

项目
Items		 组别Groups P值P-value
CON HS SP CON组vs HS组
CON group vs
HS group		 HS组vs SP组
HS group vs
SP group
系水力Water-holding capacity/% 52.13±1.12 46.68±0.83# 51.20±0.78* <0.001 <0.001
嫩度Tenderness 17.79±0.60 17.94±0.37 18.17±0.35 0.833 0.660
亮度L* 50.81±0.67 52.67±0.68 51.23±1.33 0.072 0.352
红度a* 3.14±0.63 2.52±0.46 1.36±0.29 0.439 0.061
黄度b* 8.46±0.68 7.87±0.62 8.43±0.55 0.531 0.507
45 min pH 6.03±0.09 6.08±0.12 6.18±0.15 0.750 0.623
24 h pH 5.58±0.03 5.63±0.04 5.62±0.04 0.337 0.873

2.4 裂殖壶藻粉对热应激黄羽肉鸡器官指数的影响

如表6所示,与CON组相比,HS组肝脏指数和脾脏指数显著降低(P<0.05);与HS组相比,SP组肝脏指数显著升高(P<0.05),法氏囊指数显著降低(P<0.05)。
表6 裂殖壶藻粉对热应激黄羽肉鸡器官指数的影响

Table 6 Effects of Schizochytrium powder on organ indexes of yellow-feathered broilers under heat stress

项目
Items		 组别Groups P值P-value
CON HS SP CON组vs HS组
CON group vs
HS group		 HS组vs SP组
HS group vs
SP group
肝脏Liver 23.43±0.90 19.66±0.92# 23.31±1.14* 0.011 0.025
腹脂Abdominal fat 14.03±2.73 12.58±1.26 15.40±0.43 0.637 0.064
脾脏Spleen 4.25±0.66 1.65±0.35# 1.38±0.18 <0.001 0.502
胸肌Breast muscle 38.19±1.39 39.80±1.91 43.41±0.99 0.507 0.123
法氏囊Bursa of Fabricius 1.39±0.49 0.81±0.12 0.30±0.04* 0.285 <0.001

2.5 裂殖壶藻粉对热应激黄羽肉鸡血清生化指标的影响

如表7所示,与CON组相比,HS组血清AST活性及GLU、HDL-C和LDL-C含量显著增加(P<0.05);与HS组相比,SP组血清TC和HDL-C含量显著降低(P<0.05)。
表7 裂殖壶藻粉对热应激黄羽肉鸡血清生化指标的影响

Table 7 Effects of Schizochytrium powder on serum biochemical indexes of yellow-feathered broilers under heat stress

项目
Items		 组别Groups P值P-value
CON HS SP CON组vs HS组
CON group vs
HS group		 HS组vs SP组
HS group vs
SP group
谷丙转氨酶ALT/(U/L) 1.50±0.27 1.56±0.29 1.63±0.18 0.876 0.858
谷草转氨酶AST/(U/L) 211.63±11.88 252.29±9.99# 224.75±12.83 0.023 0.121
葡萄糖GLU/(mmol/L) 12.46±0.33 14.67±0.44# 15.21±0.37 <0.001 0.361
总胆固醇TC/(mmol/L) 2.61±0.21 3.25±0.24 2.66±0.12* 0.061 0.047
甘油三酯TG/(mmol/L) 1.31±0.16 0.91±0.18 1.00±0.09 0.114 0.661
高密度脂蛋白胆固醇
HDL-C/(mmol/L)		 1.50±0.12 1.90±0.13# 1.41±0.09* 0.037 <0.001
低密度脂蛋白胆固醇
LDL-C/(mmol/L)		 0.89±0.09 1.22±0.11# 1.05±0.08 0.040 0.238

2.6 裂殖壶藻粉对热应激黄羽肉鸡血清、肝脏和空肠抗氧化指标的影响

如表8所示,与CON组相比,HS组血清和肝脏SOD活性显著升高(P<0.05);与HS组相比,SP组血清CAT活性显著降低(P<0.05),血清、肝脏和空肠MDA含量显著升高(P<0.05)。
表8 裂殖壶藻粉对热应激黄羽肉鸡血清、肝脏和空肠抗氧化指标的影响

Table 8 Effects of Schizochytrium powder on serum, liver and jejunum antioxidant indexes of yellow-feathered broilers under heat stress

项目
Items		 组别Groups P值P-value
CON HS SP CON组vs HS组
CON group vs
HS group		 HS组vs SP组
HS group vs
SP group


超氧化物
歧化酶
SOD		 血清Serum/(U/μL) 60.108±2.957 70.042±3.340# 74.572±3.509 0.044 0.368
肝脏Liver/(U/mg prot) 0.422±0.024 0.501±0.026# 0.540±0.029 0.043 0.348
空肠Jejunum/(U/mg prot) 2.244±0.062 3.017±0.636 1.450±0.166 0.292 0.068


过氧化氢酶
CAT		 血清Serum/(U/μL) 3.251±0.336 3.130±0.295 2.326±0.216* 0.793 0.046
肝脏Liver/(U/mg prot) 0.030±0.001 0.035±0.002 0.038±0.003 0.184 0.343
空肠Jejunum/(U/mg prot) 0.051±0.010 0.047±0.009 0.039±0.008 0.772 0.558


丙二醛
MDA		 血清Serum/(nmol/μL) 0.832±0.272 0.987±0.231 2.421±0.116* 0.723 <0.001
肝脏Liver/(nmol/mg prot) 0.007±0.001 0.009±0.001 0.014±0.001* 0.076 <0.001
空肠Jejunum/(nmol/mg prot) 0.003±0.001 0.004±0.001 0.011±0.002* 0.437 0.021

2.7 裂殖壶藻粉对热应激黄羽肉鸡肠道形态的影响

如表9所示,与CON组相比,HS组空肠绒毛高度/隐窝深度显著升高(P<0.05),空肠绒毛高度和隐窝深度无显著差异(P>0.05);与HS组相比,SP组空肠绒毛高度、隐窝深度和绒毛高度/隐窝深度均无显著差异(P>0.05)。
表9 裂殖壶藻粉对热应激黄羽肉鸡肠道形态的影响

Table 9 Effects of Schizochytrium powder on intestinal morphology of yellow-feathered broilers under heat stress

项目
Items		 组别Groups P值P-value
CON HS SP CON组vs HS组
CON group vs
HS group		 HS组vs SP组
HS group vs
SP group
绒毛高度VH/μm 1 533.54±63.99 1 675.45±140.37 1 443.58±81.71 0.385 0.191
隐窝深度CD/μm 288.49±6.29 250.40±20.17 225.91±12.43 0.135 0.332
绒毛高度/隐窝深度V/C 5.33±0.41 6.70±0.32# 6.64±0.18 0.030 0.867

2.8 裂殖壶藻粉对热应激黄羽肉鸡肝脏热休克蛋白相关基因表达的影响

如图2所示,与CON组相比,HS组肝脏HSP40、HSP60、HSP70、HSP90的mRNA相对表达水平无显著差异(P>0.05);与HS组相比,SP组肝脏HSP40、HSP60、HSP70、HSP90的mRNA相对表达水平无显著差异(P>0.05)。
图2 裂殖壶藻粉对热应激黄羽肉鸡肝脏热休克蛋白相关基因表达的影响

HSP40:热休克蛋白40;HSP60:热休克蛋白60;HSP70:热休克蛋白70;HSP90:热休克蛋白90。

数据柱形标注*表示差异显著(P<0.05)。下图同。

Fig.2 Effects of Schizochytrium powder on expression of heat shock protein related genes in liver of yellow-feathered broilers under heat stress

HSP40: heat shock protein 40; HSP60: heat shock protein 60; HSP70: heat shock protein 70; HSP90: heat shock protein 90.

Value columns with * mean significant difference (P<0.05). The same as below.

2.9 裂殖壶藻粉对热应激黄羽肉鸡肝脏炎症相关基因表达的影响

如图3所示,与CON组相比,HS组肝脏NLRP3、IL-6的mRNA相对表达水平显著升高(P<0.05);与HS组相比,SP组肝脏NLRP3的mRNA相对表达水平显著下降(P<0.05)。
图3 裂殖壶藻粉对热应激黄羽肉鸡肝脏炎症相关基因表达的影响

TLR4:Toll样受体4;IL-1β:白细胞介素-1β;TNF-α:肿瘤坏死因子-α;IFN-γ:干扰素-γ;IL-6:白细胞介素-6;NLRP3:NOD样受体热蛋白结构域相关蛋白3。

Fig.3 Effects of Schizochytrium powder on expression of inflammation related genes in liver of yellow-feathered broilers under heat stress

TLR4: Toll-like receptor 4; IL-1β: interleukin-1β; TNF-α: tumour necrosis factor-α; IFN-γ: interferon-γ; IL-6: interleukin-6; NLRP3: NOD-like receptor thermal protein domain associated protein 3.

3 讨论

3.1 裂殖壶藻粉对热应激黄羽肉鸡生长性能和器官发育的影响

生长性能作为肉鸡养殖中一项重要的指标,直接决定着肉鸡的价值。热应激是近些年来家禽生产中影响最严重的环境因素之一,会很大程度地降低家禽的增重和采食量,导致生长性能下降[15]。相关研究发现,28日龄白羽肉鸡在热应激条件下饲喂2周后,试验末体重、平均日增重以及平均日采食量均显著降低[16]。Kikusato等[17]在热中性与热应激条件下饲养罗斯308肉鸡,结果显示,热应激组的平均日增重和平均日采食量显著低于对照组,但饲料转化率增加。郑雨萱等[18]研究表明,与常温对照组相比,热应激组白羽肉鸡平均日增重和平均日采食量显著降低,料重比则显著提高。在将21日龄的罗斯308肉鸡和科宝肉鸡暴露于高温环境下14 d之后,其生长性能受到显著的负面影响,并且直肠温度显著升高[19]。Li等[20]研究显示,经热应激暴露后,爱拔益加肉鸡的直肠温度显著升高。在本研究中,与对照组相比,HS组体重、平均日增重和平均日采食量均显著降低,料重比及第4、7、14天直肠温度显著升高,与以上的研究结果一致;在饲喂了添加裂殖壶藻粉的饲粮后,肉鸡体重有所增加,其他生长性能和直肠温度无显著差异。Jeon等[21]研究发现,在肉鸡饲粮中添加2%的裂殖壶藻粉后,肉鸡体重相比于对照组显著增加,同时鸡肉品质也有所上升。而Yan等[22]在基础饲粮中分别加入0.1%和0.2%的裂殖壶藻粉后,罗斯308肉鸡的体重增加,采食量和饲料转化率等均未受到显著影响。Rymer等[23]研究表明,饲粮中添加裂殖壶藻并未显著影响罗斯308肉鸡生长性能。这与本试验结果基本一致。
热应激也会对肉鸡的器官发育造成不良影响。朱春梅等[24]对肉鸡进行为期14 d的热应激处理后,鸡只的脾脏、胸腺、法氏囊等器官重量减少,生长发育受限,器官指数明显下降。Ding等[25]研究表明,7 d的高温应激降低了白羽肉鸡的肝脏重量和指数,造成肝脏损伤。本研究结果显示,HS组肉鸡的肝脏指数和脾脏指数相比于CON组显著降低,腹脂和法氏囊等器官指数未受到显著影响,这与上述研究结果存在差异,可能是由于不同肉鸡品种的生理差异造成的。Long等[26]在饲喂爱拔益加肉鸡添加了不同比例裂殖壶藻粉的饲粮后,与对照组相比,1%裂殖壶藻粉组的肝脏指数显著升高,腹脂指数显著降低;2%裂殖壶藻粉组的脾脏指数显著升高。Gatrell等[27]研究显示,在罗斯308肉鸡的饲粮中添加不同浓度富含DHA的脱脂微藻,6周后只有16%浓度组的肝脏、肠道等器官指数显著增加,胸肌、肌胃等器官指数无显著影响。本试验饲喂了添加裂殖壶藻粉的饲粮后,与HS组相比,SP组肉鸡肝脏器官指数显著增加。综上所述,饲粮中添加裂殖壶藻粉改善肉鸡的器官特别是肝脏的生长发育。

3.2 裂殖壶藻粉对热应激黄羽肉鸡血清生化指标的影响

高温导致的机体应激反应常常伴随着血清中相关蛋白质等代谢指标的变化,血清AST、ALT、乳酸脱氢酶等活性的变化常标志着肝脏的损伤[28]。研究表明,热应激会降低肉鸡代谢相关酶的活性,进一步影响糖、脂代谢速率,从而增加血清中胆固醇含量,导致肉鸡血清生化指标的异常变化[29]。Wang等[30]在研究热应激对黄羽肉鸡的影响时发现,14 d的循环热应激处理显著增加了肉鸡的血清ALT、AST活性及TC、LDL-C含量,显著降低了血清GLU含量。金永燕等[31]在热应激条件下饲养了科宝肉鸡7 d后,肉鸡的血清GLU、TC、LDL-C和HDL-C含量均显著增加;而饲养了14 d后,仅血清GLU含量显著增加。胆固醇、LDL-C、HDL-C与血清中的脂质代谢密切相关。本研究结果发现,热应激显著增加了肉鸡血清AST活性及GLU、HDL-C和LDL-C含量,血清TC含量趋于上升,与上述研究结果一致,表明黄羽肉鸡受热应激影响肝功能受损,机体能量代谢特别是脂质代谢受到干扰。本试验中,在饲喂了裂殖壶藻粉饲粮后,SP组血清TC和HDL-C含量显著降低。Wahid等[32]在罗斯308肉鸡饲粮中添加富含DHA的鱼油后,经过为期35 d的饲养试验,血清TC、HDL-C、LDL-C含量均显著降低。饲粮中的裂殖壶藻粉对肉鸡脂质代谢能力的调节很可能是通过抑制羟甲基戊二酰辅酶A(HMG-CoA)还原酶和角鲨烯环氧化物酶等关键酶的活性降低血清的胆固醇含量,从而使HDL-C含量降低[33]。

3.3 裂殖壶藻粉对热应激黄羽肉鸡肉品质的影响

热应激会在肉鸡生长发育阶段影响其肌肉的生长,导致肉品质的下降,同时一定程度上影响其肉色、水分含量、嫩度和营养成分[34]。Dai等[35]在循环热应激下分别观察了爱拨益加肉鸡28、35和42日龄胸肌颜色、pH、成分以及持水特性,发现相比于对照组,热应激组3个时间点的胸肌亮度值显著增加,水分、粗蛋白质、粗脂肪含量显著减少。Chen等[36]研究发现,热应激导致鸡肉的红度值和pH显著降低,亮度值和滴水损失显著增加。系水力是指保持肌肉内水分的能力,作为一项评估肉品质的重要指标,受到机体自身遗传特性、屠宰以及环境等多种因素的影响,不同品种不同日龄之间也有差异[37]。本研究结果显示,与CON组相比,HS组胸肌系水力显著降低。裂殖壶藻粉中DHA等多不饱和脂肪酸的含量丰富,对改善家禽肉品质和健康有着积极作用。本研究中,热应激造成了肉鸡胸肌系水力下降,在饲粮中添加了裂殖壶藻粉后,肉鸡胸肌系水力显著升高,表明肌肉的持水能力相比HS组得到了改善。有报道称,饲粮中添加不同比例的裂殖壶藻粉对肉鸡的胸肌系水力、pH及亮度、红度值等肉品质指标均无显著影响[26]。在饲粮中添加3%和6%的小球藻粉,罗斯308肉鸡的胸肌黄度和红度值显著升高,而亮度值显著降低[38]。这与上述研究结果不一致,产生不同试验结果的原因可能是由于肉鸡品种、添加剂适应性以及饲料加工各有差异造成的。

3.4 裂殖壶藻粉对热应激黄羽肉鸡氧化应激的影响

氧化应激在肉鸡养殖中普遍存在,当机体抗氧化能力失调,体内氧化还原反应失衡,会导致细胞受到多种氧化损伤,严重影响肉鸡生产,造成经济损失[39]。热应激在引起机体热休克反应的同时,会导致活性氧和细胞中抗氧化剂含量的大量增加,造成组织细胞的损伤[40-41]。陈乐乐等[42]研究结果显示,21 d的热应激处理会使肉鸡血清SOD活性和MDA含量显著提高。大量研究表明,热应激的强度与持续时间会造成抗氧化酶活性的差异变化,急性热应激可能增加肉鸡血清和肝脏中SOD、CAT等抗氧化酶的活性,而长期热应激会降低这些酶活性[43-44]。Madkour等[45]在对印第安河(Indian river,IR)雏鸡进行热应激处理后,肉鸡肝脏中HSP70和HSP90的mRNA相对表达水平显著上调。本研究结果显示,与CON组相比,HS组血清和肝脏SOD活性显著升高,肝脏MDA含量有所增加,肉鸡肝脏中热休克蛋白相关基因的mRNA相对表达水平无显著差异,这可能是由于热应激引发的氧化还原失衡导致的。裂殖壶藻粉本身富含DHA等优质抗氧化剂,可以通过氧化还原反应清除自由基,调节机体内活性氧的水平,从而提高机体抗氧化能力[46]。相关研究表明,饲粮中添加1%和2%的裂殖壶藻粉均可显著增加肉鸡肌肉SOD活性,降低MDA含量,提升总抗氧化能力[26]。Mouradian等[47]通过DHA处理人乳腺癌细胞以及在小鼠饲粮中补充DHA添加剂后,都观察到HSP90的mRNA相对表达水平显著降低。而本研究在饲粮中添加了藻粉后,血清CAT活性显著降低,血清、肝脏和空肠MDA含量显著升高,HSP70的mRNA相对表达水平呈下降趋势,肉鸡在热应激下的氧化损伤加剧,与上述研究结果并不一致。DHA本身含有多个不饱和键,导致其易在贮存过程中被氧化,从而影响抗氧化的功能,甚至损害动物的抗氧化能力。谭露霖等[48]研究表明,富含DHA的鱼油被氧化后,爱拔益加肉鸡的生长性能和肉品质受到显著负面影响。Huang等[49]在饲粮中添加了氧化鱼油后,仔猪空肠中MDA含量显著提高,引起仔猪肠道发生氧化应激。因此,笔者推测这可能是由于热应激的强度过高、持续的时间过长以及饲粮被氧化导致的。

3.5 裂殖壶藻粉对热应激黄羽肉鸡炎症反应的影响

炎症反应是机体在保护自身的免疫反应中重要的一环,但是炎症反应的紊乱同样会造成机体组织损伤,甚至严重威胁个体的健康。炎症反应在组织中与氧化应激息息相关,共同维持动物机体稳态,这一过程由多因子共同介导。热应激导致的活性氧水平上升,会激活NLRP3炎症小体和Toll样受体(Toll-like receptors,TLRs)从而促进TNF-α、IFN-γ、IL-6等促炎因子的表达,也会促进相关热应激蛋白的表达,调节机体的免疫和炎症反应;而炎症反应也会反过来促进活性氧的产生,降低细胞的抗氧化能力,从而导致机体氧化应激的加剧[50-52]。Liu等[53]研究发现,1和2周的热应激处理均会显著上调肉鸡肝脏TLR4、NLRP3、IL-6、TNF-α等的mRNA相对表达水平。Ding等[54]研究结果显示,28日龄的肉鸡在经过4周的慢性热应激处理后,其血清和脾脏中的IL-6、TNF-α、IL-1β等的mRNA相对表达水平显著增加。本研究中,热应激肉鸡肝脏中炎症相关基因NLRP3和IL-6的mRNA相对表达水平显著增加;在饲喂了裂殖壶藻粉饲粮后,肝脏中NLRP3的mRNA相对表达水平显著下降。Wang等[55]研究显示,在饲粮中添加裂殖壶藻后,葡聚糖硫酸钠(DSS)诱导的小鼠结肠炎症状得到缓解,TNF-α、IL-1β等的mRNA相对表达水平显著降低。大量研究表明,在体外细胞试验中,DHA处理均能显著降低细胞内TNF-α、IL-1β等炎症细胞因子的分泌与基因表达[12,56]。结合本试验结果,笔者推测饲粮中添加裂殖壶藻粉很有可能通过炎症小体调控肉鸡机体内的免疫反应,从而缓解热应激导致的炎症失调。

4 结论

在热应激条件下,肉鸡的体重和采食量减少,体温升高,生长性能和肉品质下降,器官发育受到影响,机体代谢紊乱,抗氧化能力下降。在基础饲粮中添加20 g/kg裂殖壶藻粉后,肉鸡的肝脏指数和肉品质上升,热应激导致的脂质代谢和炎症反应紊乱得到改善,代谢能力增强,但血清、肝脏和空肠的氧化应激加剧。

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