Effects of Combination of Curcumin and Vitamin E on NutrientApparent Digestibility, Serum Biochemical Indices and Lipid Metabolism of Beagle Dogs

LUO Youwen; YUAN Huagen; MENG Ting; CAO Yun; WU Haitao; SHI Wujie

doi:10.12418/CJAN2024.681

2024 , Vol. 36 >Issue 12: 7986 - 7994

DOI: https://doi.org/10.12418/CJAN2024.681

RESEARCH PAPER

Effects of Combination of Curcumin and Vitamin E on NutrientApparent Digestibility, Serum Biochemical Indices and Lipid Metabolism of Beagle Dogs

LUO Youwen ,
YUAN Huagen ,
MENG Ting ,
CAO Yun ,
WU Haitao ,
SHI Wujie

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Jiangsu Animal Husbandry and Veterinary College, Taizhou 225300, China

Received date: 2024-06-24

Online published: 2024-12-12

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Abstract

The aim of this study was to investigate the effects of combination of curcumin and vitamin E on the apparent digestibility of nutrients, serum biochemical indices and lipid metabolism of Beagle dogs. Eighteen Beagle dogs about 12 months old were randomly divided into three groups (n=6), and they were fed basal diet (control group), basal diet+50 mg/kg curcumin+100 mg/kg vitamin E (Cur-50 group), basal diet+100 mg/kg curcumin+100 mg/kg vitamin E (Cur-100 group), respectively. After 30 days, the apparent digestibility of nutrients, serum biochemical and lipid metabolism indices were determined, and fecal scores were performed. The results showed that, compared with the control group, the apparent digestibility of ether extract in Cur-100 group was significantly increased (P<0.05), serum total protein (TP) content and fecal secretory immunoglobulin A (sIgA) contents were significantly increased (P<0.05), and serum urea nitrogen (UN) content and fecal scores on days 15 and 30 were significantly decreased (P<0.05); fecal sIgA content in Cur-50 group was significantly increased (P<0.05). In terms of lipid metabolism, the contents of serum total cholesterol (TC), triglyceride (TG) and low-density lipoprotein (LDL-C) in Cur-100 group were significantly decreased (P<0.05), while the activity of serum lipoprotein lipase (LPL) was significantly increased compared with the control group (P<0.05); serum TC content in Cur-50 group was significantly decreased (P<0.05), and the activity of serum LPL was significantly increased compared with the control group (P<0.05). In summary, curcumin combined with vitamin E can improve the apparent digestibility of ether extract, promote nitrogen metabolism, improve fecal status, improve the body’s immunity, promote lipid metabolism and reduce the level of blood lipids in Beagle dogs.

Key words： curcumin; vitamin E; serum biochemical indices; lipid metabolism; Beagle dogs

Cite this article

LUO Youwen , YUAN Huagen , MENG Ting , CAO Yun , WU Haitao , SHI Wujie . Effects of Combination of Curcumin and Vitamin E on NutrientApparent Digestibility, Serum Biochemical Indices and Lipid Metabolism of Beagle Dogs[J]. Chinese Journal of Animal Nutrition, 2024 , 36(12) : 7986 -7994 . DOI: 10.12418/CJAN2024.681

近年来,随着经济的发展,宠物犬饲养量日益增加。犬作为人们主要的伴侣动物之一,其健康程度日益受到重视。在饲养过程中,越来越多的犬受饲粮、品种、生活方式等因素的影响导致肥胖和氧化应激。肥胖不仅影响犬的生活质量,还易引起代谢性疾病、高脂血症、骨科疾病、繁殖障碍等^[1],慢性病发病率也较高^[2]。

植物提取物在犬粮中的应用日益受到人们的欢迎,研究人员对植物中的活性物质对机体脂质代谢等健康方面的作用日益感兴趣。姜黄素是一种从姜科植物姜黄的根茎中提取而得的天然多酚类植物提取物,是赋予姜黄特殊功能的生物活性因子,具有抗氧化、抗炎、抑制肥胖等多种作用。核因子E2相关因子2(Nrf2)是体内脂质代谢稳态和氧化应激的重要调节剂^[3]。研究证实,姜黄素能通过对Kelch样ECH关联蛋白1(Keap1)-Nrf2通路的调控^[4]缓解大鼠肝组织的氧化损伤^[5];姜黄素还可以有效激活Nrf2,预防和治疗非酒精性脂肪肝^[6]。研究发现,饲粮中添加姜黄素可以提高肉鸡的肌肉品质和胸肌抗氧化酶活性^[7],通过调节肝脏相关信号通路的基因表达,降低肝脏脂肪水平,并提高宫内生长迟缓(IUGR)仔猪肝脏抗氧化酶活性,促进脂质分解代谢,降低背最长肌氧化应激和脂肪沉积^[8]。但姜黄素对犬脂质代谢和营养物质消化率的影响暂未见报道。

维生素E是一类化学结构相似的酚类化合物,具有很强的抗氧化活性,是犬粮中最常用的抗氧化剂之一。此外,维生素E在调控脂质代谢方面也发挥着重要作用。研究发现,维生素E以细胞信号转导因子的形式影响脂肪代谢相关基因的表达。Li等^[9]报道,维生素E可以通过调控北京油鸡心型脂肪酸结合蛋白(H-FABP)基因的表达降低肌内脂肪含量,而H-FABP基因的mRNA表达水平与肌内脂肪含量呈显著的负相关。维生素E也能够通过调控脂肪酸结合蛋白(FABPs)相关基因的表达促进细胞内脂肪酸的摄取和运输^[10]。维生素E在调节肝脂、血脂代谢上亦有重要作用^[11-12],在畜牧生产领域得到了广泛应用。然而,维生素E和姜黄素对犬脂质代谢的影响却鲜见报道。本研究以比格犬为试验对象,探讨姜黄素和维生素E联用对其营养物质表观消化率、脂质代谢和血液生化指标的影响,为姜黄素和维生素E在犬功能性食品和处方粮上的应用提供参考。

1 材料与方法

1.1 试验材料

试验所用姜黄素纯度为98%,维生素E纯度为98%。

1.2 试验设计

选取约12月龄的健康比格犬18只,体重为(16.73±1.84) kg,随机分成3组,每组6只,公母各占1/2。对照组饲喂基础饲粮,Cur-50组饲喂基础饲粮+50 mg/kg姜黄素+100 mg/kg维生素E,Cur-100组饲喂基础饲粮+100 mg/kg姜黄素+100 mg/kg维生素E。动物试验由江苏农牧科技职业学院实验动物伦理委员会批准(批准号:CWKJ2023-05),试验过程善待动物,遵循动物伦理及相关法规。

1.3 饲养管理

所有供试犬只单笼饲养于试验房内,按照常规免疫程序进行疫苗接种和驱虫。基础饲粮参照AAFCO(2016)犬营养需要进行配制,其组成及营养水平见表1。每天09:00和16:00各饲喂1次,每次每只给料约180 g,日均采食量290 g/只,自由饮水;每天户外自由活动约1 h,记录犬只采食量,观察其精神状态和健康状况。饲养期共计37 d,包含7 d的预试期和30 d的正试期。

表1 基础饲粮组成及营养水平(风干基础)

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

原料 Ingredients		营养水平 Nutrient levels²⁾
鲜鸡肉 Fresh chicken	29.0	粗蛋白质 Crude protein	25.01
鸡肉粉 Chicken-meat powder	10.0	粗脂肪 Ether extract	10.54
燕麦 Oat	13.5	粗灰分 Ash	6.43
大米 Rice	19.1	粗纤维 Crude fiber	3.82
鸭骨架 Duck skeleton	15.0	代谢能 ME/(MJ/kg)	16.73
动物脂肪Animal grease	7.3	钙 Calcium	1.25
鱼粉 Fish meal	4.7	总磷 Total phosphorus	1.10
风味剂 Flavor	0.3	水溶性氯化物 Water-soluble chloride	0.44
磷酸氢钙 CaHPO₄	0.1	赖氨酸 Lys	1.20
预混料Premix¹⁾	1.0	蛋氨酸+胱氨酸 Met+Cys	0.63
合计 Total	100.0

1)预混料为每千克饲粮提供The premix provided the following per kg of the diet:VA 15 000 IU,VD₃ 2 500 IU,VE 60 IU,VB₁ 2.2 mg,VB₂ 5.5 mg,VB₆ 1.5 mg,叶酸 folic acid 0.22 mg,胆碱 choline 1 000 mg,Fe 80 mg,Cu 12 mg,Mn 7 mg,I 1.1 mg,Se 0.35 mg。

2)代谢能和氨基酸为计算值,其余为测定值。代谢能参考AAFCO(2016)计算,氨基酸根据原料中相应氨基酸含量计算。ME and amino acids were calculated values, while the others were measured values. ME was calculated by reference to AAFCO(2016), and amino acids were calculated according to the corresponding amino acid contents in the materials.

1.4 指标测定

1.4.1 营养物质表观消化率

采用全收粪法测定各营养物质表观消化率。在正试期最后3 d,连续(72 h)收集所有受试犬的粪便,-20 ℃保存。试验结束后将每只犬3 d收集的所有粪便解冻并充分混合,称取200 g左右的粪样,于65 ℃烘至恒重,粉碎过40目筛,4 ℃保存待测。饲粮和粪样中干物质(DM)(GB/T 6435—2014)、粗蛋白质(CP)(GB/T 6432—2018)、粗脂肪(EE)(GB/T 6433—2006)、粗灰分(Ash)(GB/T 6438—2007)和粗纤维(CF)(GB/T 6434—2022)含量均按照对应的国标方法进行测定,总能(GE)、粪能(FE)采用氧弹式热量计进行测定。饲粮中粗纤维含量参照GB/T 6434—2022进行测定,钙含量采用乙二胺四乙酸二钠络合滴定法(GB/T 6436—2018)测定,总磷含量采用分光光度法(GB/T 6437—2018)测定。

营养物质表观消化率计算公式如下:

某营养物质表观消化率(%)=[(该营养物质摄入量-粪中该营养物质排出量)/该营养物质摄入量]×100。

1.4.2 粪便评分

于正试期的第1、15和30天,参考威豪粪便评分系统(The Waltham^® Faeces Scoring System,WFS)和Cavett等^[13]报道的评分标准,对每只犬的鲜粪便进行现场评分(1~5分),分数越高,粪便含水量越高。粪便评分标准见表2。

表2 粪便评分标准

Table 2 Fecal scoring criteria

评分 Scores/分	外观 Appearance	形态 Form
1	干、硬、易碎,子弹状	成形
2	成形良好,捡拾起来不留印记	成形
3	含水量较多,捡拾后地面留下明显印记	部分成形
4	黏稠,缺乏一致性,基本不成形	不成形
5	水样液态	不成形

1.4.3 血液样本采集和指标测定

正试期第30天,饲养试验结束时对供试犬只(空腹状态)前肢静脉采血约8 mL,4 ℃下1 360×g离心10 min,分离血清并置于-20 ℃保存待测。

血清总蛋白(TP)、白蛋白(ALB)、球蛋白(GLB)、尿素氮(UN)、肌酐(CREA)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)、葡萄糖(GLU)含量及谷丙转氨酶(ALT)、碱性磷酸酶(AKP)活性使用全自动生化分析仪(MindaryBS-280)测定;血清游离脂肪酸(FFA)含量使用酶联免疫吸附测定(ELISA)法进行测定,试剂盒购于南京建成生物工程研究所;血清脂蛋白脂酶(LPL)活性、饥饿素(GHRL)含量参考Yamka等^[14]的方法使用试剂盒进行测定,试剂盒购于南京建成生物工程研究所。

1.4.4 粪便样本采集和指标测定

于正试期第30天采集新鲜粪便2~3 g于无菌粪便采集管中,-20 ℃保存待测。测定时称取1.0 g粪便于离心管中,加入9 mL无菌生理盐水并振荡混匀,4 ℃下999×g离心20 min后分离上清液,采用ELISA法检测粪便中分泌型免疫球蛋白A(sIgA)含量,试剂盒购于南京建成生物工程研究所。

1.5 数据统计与分析

使用SPSS 20.0软件对试验数据进行单因素方差分析,差异显著时采用Duncan氏法进行组间多重比较,差异显著水平为P<0.05。试验结果以平均值±标准差(mean±SD)表示。

2 结果与分析

2.1 姜黄素和维生素E联用对比格犬营养物质表观消化率的影响

由表3可知,各组的DM、CP、Ash、GE表观消化率无显著差异(P>0.05);Cur-100组EE表观消化率显著高于对照组(P<0.05),Cur-50组EE表观消化率与对照组相比无显著差异(P>0.05)。

表3 姜黄素和维生素E联用对比格犬营养物质表观消化率的影响

Table 3 Effects of combination of curcumin and vitamin E on nutrient apparent digestibility of Beagle dogs

项目 Items	组别 Groups
项目 Items	对照 CON	Cur-50	Cur-100
干物质 DM	86.90±4.47	85.01±3.51	85.19±3.46
粗蛋白质 CP	81.04±2.08	82.45±2.15	85.46±3.13
粗脂肪 EE	87.52±4.42^a	90.43±5.44^ab	93.29±5.59^b
粗灰分 Ash	37.24±1.38	36.96±2.45	38.90±1.59
总能 GE	82.25±4.56	83.89±3.69	83.07±3.88

	同行数据肩标相同字母或无字母表示差异不显著(P>0.05),不同字母表示差异显著(P<0.05)。下表同。
	In the same row, values with the same letter or no letter superscripts mean no significant difference (P>0.05), while with the different letter superscripts mean significant difference (P<0.05). The same as below.

2.2 姜黄素和维生素E联用对比格犬粪便评分的影响

由表4可知,第15天时,Cur-100组粪便评分显著低于对照组和Cur-50组(P<0.05);第60天时,Cur-100组粪便评分显著低于对照组(P<0.05)。

表4 姜黄素和维生素E联用对比格犬粪便评分的影响

Table 4 Effects of combination of curcumin and vitamin E on fecal scoring of Beagle dogs

时间 Time	组别 Groups
时间 Time	对照 CON	Cur-50	Cur-100
第1天 Day 1	2.82±0.20	3.00±0.00	2.97±0.08
第15天 Day 15	2.87±0.18^a	2.81±0.24^a	2.59±0.20^b
第30天 Day 30	3.00±0.00^a	2.71±0.17^ab	2.54±0.12^b

2.3 姜黄素和维生素E联用对比格犬血清生化指标的影响

由表5可知,Cur-100组血清TP、UN含量显著高于对照组(P<0.05);各组血清ALB、GLB、CREA含量与AKP、ALT活性无显著差异(P>0.05)。

表5 姜黄素和维生素E联用对比格犬血清生化指标的影响

Table 5 Effects of combination of curcumin and vitamin E on serum biochemical indices of Beagle dogs

项目 Items	组别 Groups
项目 Items	CON	Cur-50	Cur-100
总蛋白 TP/(g/L)	40.05±3.52^a	44.34±3.78^ab	48.17±4.36^b
白蛋白 ALB/(g/L)	23.03±2.95	25.14±2.50	27.03±2.38
球蛋白 GLB/(g/L)	17.01±1.06	18.49±1.64	19.85±2.02
碱性磷酸酶 AKP/(U/L)	32.34±2.07	35.10±3.51	31.27±1.66
尿素氮 UN/(mmol/L)	6.69±0.85^a	5.17±0.46^ab	4.96±0.59^b
肌酐 GREA/(μmol/L)	56.88±3.09	52.39±4.52	59.06±3.64
谷丙转氨酶 ALT/(U/L)	15.11±1.04	16.89±1.39	14.30±0.84

2.4 姜黄素和维生素E联用对比格犬粪便中sIgA含量的影响

由图1可知,Cur-50组和Cur-100组粪便中sIgA含量均显著高于对照组(P<0.05)。

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图1 姜黄素和维生素E联用对比格犬粪便中分泌型免疫球蛋白A含量的影响

数据柱标注相同字母或无字母表示差异不显著(P>0.05),不同字母表示差异显著(P<0.05)。下图同。

Fig.1 Effects of combination of curcumin and vitamin E on fecal sIgA content of Beagle dogs

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

2.5 姜黄素和维生素E联用对犬脂质代谢指标的影响

由表6可知,Cur-50组和Cur-100组血清TC含量显著低于对照组(P<0.05);Cur-100组血清TG和LDL-C含量显著低于对照组(P<0.05);各组血清HDL-C和FFA含量无显著差异(P>0.05)。

表6 姜黄素和维生素E联用对比格犬血清脂质代谢指标的影响

Table 6 Effects of combination of curcumin and vitamin E on serum lipid metabolism indices of Beagle dogs

项目 Items	组别 Groups
项目 Items	对照 CON	Cur-50	Cur-100
总胆固醇 TC(mmol/mL)	4.52±0.50^a	3.53±0.63^b	3.61±0.47^b
甘油三酯 TG(mmol/mL)	1.21±0.17^a	1.39±0.13^ab	1.48±0.14^b
高密度脂蛋白胆固醇 HDL-C/(mmol/mL)	2.59±0.31	2.71±0.29	2.44±0.25
低密度脂蛋白胆固醇 LDL-C/(mmol/mL)	1.96±0.19^a	1.79±0.13^ab	1.61±0.15^b
游离脂肪酸 FFA/(μmol/L)	1 012.34±76.30	962.17±55.21	981.43±62.73

由图2可知,Cur-50组和Cur-100组血清LPL活性显著高于对照组(P<0.05);各组血清GHRL含量无显著差异(P>0.05)。

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图2 姜黄素和维生素E联用对比格犬血清脂蛋白脂酶活性和饥饿素含量的影响

Fig.2 Effects of combination of curcumin and vitamin E on LPL activity and GHRL content in serum of Beagle dogs

3 讨论

3.1 姜黄素和维生素E联用对比格犬营养物质表观消化率和粪便评分的影响

姜黄素作为天然植物源活性提取物,具有绿色安全的特点。近年来,不少研究发现姜黄素能提高动物生长性能和营养物质的消化率。例如,芦娜等^[15]研究发现,饲粮中添加200或400 mg/kg姜黄素能提高断奶仔猪对CP等营养物质的表观消化率;田光元等^[16]研究显示,饲粮中添加300 mg/kg姜黄素可以提高舍饲羔羊对中性洗涤纤维的表观消化率;Niu等^[17]报道,饲粮中添加400 mg/kg姜黄素可以显著提高断奶仔猪的日增重,降低料重比。上述报道提示,姜黄素有提高营养物质消化率和动物生长性能的作用。本研究发现,100 mg/kg姜黄素+100 mg/kg维生素E可以提高比格犬对饲粮中EE的表观消化率,这跟芦娜等^[15]在断奶仔猪上所得试验结果类似。还有研究还发现,姜黄素可以改善生长期肉兔空肠黏膜形态,增加绒毛长度^[18],这可能是姜黄素可以提高营养物质消化率的原因。

粪便评分系统中,2~3分是较理想的粪便评分范围,2.5分为最理想状态^[19]。本研究发现,添加100 mg/kg姜黄素+100 mg/kg维生素E组比格犬在第15和30天的粪便评分显著低于对照组,且接近2.5分,与对照组相比粪便硬度增加,且更接近理想状态,提示姜黄素和维生素E可以改善比格犬的粪便状态。类似研究也发现,姜黄素对小鼠腹泻具有良好的干预效果^[20];姜黄素可以抑制断奶仔猪肠道致病菌的增殖,提高益生菌的相

对丰度^[21];姜黄素可以提高肉鸡盲肠菌群丰度,增加肠道菌群的多样性^[22]。肠道中有益菌的相对丰度和肠道菌群多样性的增加可以提高肠道微生态平衡,促进肠道健康,从而改善粪便状态。而姜黄素对肠道菌群的有益性亦可能是上述营养物质消化率提高的原因之一。

3.2 姜黄素和维生素E联用对比格犬血清生化指标和粪便sIgA含量的影响

在犬血清生化指标中,Cur-100组血清UN含量显著低于对照组,提示一定量的姜黄素和维生素E可以促进比格犬体内氮代谢,Cur-100组的CP表观消化率比对照组提高了5.45%同样能提示

这一作用。田光园等^[16]报道,饲粮中添加姜黄素可以提高羔羊的氮代谢水平。Vorlaphim等^[23]研究表明,饲粮中添加姜黄素显著降低了肉牛瘤胃氨态氮(NH₃-N)含量,显著促进氮沉积,提高了氮利用水平,与本研究结果类似。

已有研究表明姜黄素通过抗炎、抗癌和抗氧化对犬的健康起到改善作用^[24]。本试验发现,与对照组相比,Cur-100组比格犬血清中TP含量显著提高,Cur-50组、Cur-100组粪便中sIgA含量显著提高,这提示姜黄素和维生素E联用可以在一定程度上提高比格犬的免疫功能。研究发现,姜黄素通过Toll样受体4(TRL4)/核因子-κB(NF-κB)通路提升小鼠机体的抗氧化应激能力,抑制促炎因子白细胞介素-1β(IL-1β)、肿瘤坏死因子-α(TNF-α)、白细胞介素-6(IL-6)释放,并促进抗炎因子白细胞介素-10(IL-10)释放^[20]。维生素E是目前常用的抗氧化剂,可清除过量的活性氧(ROS)和活性氮(RON),提高超氧化物歧化酶(SOD)的活性,增强机体抗氧化能力^[25]。由此可知,在抗氧化和抗炎的共同作用下,姜黄素和维生素E共同维持机体免疫屏障,改善比格犬的免疫功能。

3.3 姜黄素和维生素E联用对比格犬脂质代谢的影响

姜黄素可以调节肉鸡脂质代谢,显著降低肉鸡血清和肝脏中TC含量,显著降低血清中LDL-C含量^[26]。研究报道,受试者口服500 mg/d姜黄素7 d后,血清TC含量显著降低,血清HDL-C含量显著升高^[27]。本试验发现,与对照组相比,Cur-100组比格犬血清中TC、TG和LDL-C含量显著降低。在断奶仔猪上的试验发现,饲粮中添加200或300 mg/kg姜黄素能降低仔猪血清TC、TG和LDL-C含量^[28],与本试验结果类似。

尽管研究报道姜黄素能够降低血脂水平,但其机制尚未明确。LPL是血液中一种关键的脂质代谢酶,主要分解TG以产生脂肪酸和甘油^[29]。本试验发现,Cur-50、Cur-100组血清中LPL活性均显著提高,推测添加姜黄素和维生素E后血清LPL活性的提高促进了血液中脂质的分解代谢。崔艳峰^[30]研究发现,姜黄素能提高高温环境下蛋鸡肝脏LPL活性,减少肝脏TG存储,与本试验结果类似。Seo等^[29]报道,姜黄素能使糖尿病小鼠血浆中TC和TG含量显著降低,并使LPL活性显著升高。姜黄素提高LPL活性,进而促进TG、TC的代谢,可能是姜黄素降低血脂水平的机理之一。此外,本试验还发现,饲粮中添加姜黄素和维生素E有降低比格犬血清中FFA含量的趋势,提示姜黄素和维生素E联用可以降低比格犬血脂水平,影响脂质代谢,且其效果可能与剂量有关。

4 结论

综上所述,饲粮中同时添加姜黄素和维生素E可以提高比格犬对EE的表观消化率和氮利用率,改善粪便状态,增强机体免疫力,并能促进血液中脂质代谢,降低血脂水平。

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