2. 岭南现代农业科学与技术广东省实验室茂名分中心, 茂名 525000
2. Maoming Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Maoming 525000, China
随着动物对蛋白质需求的增加，饲料短缺、人畜争粮的矛盾将不断扩大。我国玉米和豆粕长期依赖于进口，养殖成本高。为保障饲料原料有效供给、降低养殖成本，将非常规饲料纳入动物生产是可行的策略。潜在的饲料资源可以部分替代玉米和豆粕等传统饲料原料，有助于缓解饲料短缺、降低饲养成本、减少人畜争粮矛盾。
桑叶资源丰富，富含粗蛋白质(14.0%~34.2%)、氨基酸、微量元素，是重要的非常规饲料[1-2]。桑叶中丰富的活性物质(多酚、多糖、生物碱等)具有抗氧化、免疫调节、抗应激、降脂等多种生物学功能[2-4]。研究表明，桑叶可以改善动物生长性能、抗氧化能力、免疫功能[5-8]。但是，抗营养因子单宁的存在降低了桑叶的消化吸收，桑叶在肥育猪生产中的添加量较低。对桑叶进行微生物发酵，可减少单宁含量，同时提高粗蛋白质含量。目前，发酵桑叶(fermented mulberry leaves，FML)在肥育猪生产中的应用较少。因此，本试验旨在探讨饲粮中添加发酵桑叶对肥育猪生长性能以及血液、尿液代谢物的影响，以期为发酵桑叶在猪生产中的应用提供依据。
1 材料与方法 1.1 试验材料发酵桑叶制备：将鲜桑叶切短(1~2 cm)，桑叶与麸皮(质量比9 ∶ 1)混合均匀，加入酒窖片球菌(Pediococcus cellicola)和地衣芽孢杆菌(Bacillus licheniformis)，搅拌均匀，pH自然，密封发酵。发酵桑叶含水量68%，营养水平(干物质基础)如下：粗蛋白质含量26.88%，粗脂肪含量2.14%，粗纤维含量14.65%，中性洗涤纤维含量31.43%，酸性洗涤纤维含量14.95%，粗灰分含量12.87%，钙含量2.67%，磷含量0.61%。
1.2 试验设计和试验饲粮选取18头132日龄杜×长×大阉公猪，体重(78.19±2.05) kg，按体重随机分为2组，每组9个重复，每个重复1头猪。对照组饲喂基础饲粮，发酵桑叶组在基础饲粮中添加10%发酵桑叶。试验期69 d。试验饲粮组成及营养水平见表 1。
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表 1 试验饲粮组成及营养水平(风干基础) Table 1 Composition and nutrient levels of experimental diets (air-dry basis) |
试验在广东省农业科学院动物科学研究所猪场进行，按照猪场常规程序管理。试验期间，记录试验猪的初重、末重和每天耗料量。试验结束时，每组选取接近平均体重的6头试验猪进行耳静脉采血，肝素钠抗凝管收集血液，3 500 r/min、4 ℃离心10 min后收集血浆，-80 ℃保存。试验猪屠宰后分离出膀胱，混匀膀胱中尿液，收集尿液，-80 ℃保存。
1.4 指标测定 1.4.1 生长性能指标根据试验猪的初重、末重和每天耗料量，计算平均日采食量(ADFI)、平均日增重(ADG)、料重比(F/G)。
1.4.2 血浆和尿液生化指标血浆总蛋白、白蛋白、肌酐、尿素、尿酸、葡萄糖、甘油三酯、总胆固醇、高密度脂蛋白胆固醇、低密度脂蛋白胆固醇含量和谷丙转氨酶、谷草转氨酶、乳酸脱氢酶、碱性磷酸酶活，以及尿液肌酐、尿素、尿酸含量和乳酸脱氢酶、碱性磷酸酶活性均采用中生北控生物科技股份有限公司的试剂盒，并通过Selectra Pro XL全自动生化仪(VITAL，荷兰)进行测定。
1.4.3 血浆抗氧化指标血浆丙二醛(MDA)、谷胱甘肽(GSH)含量和总超氧化物歧化酶(T-SOD)、过氧化氢酶(CAT)、谷胱甘肽过氧化物酶(GSH-Px)活性以及总抗氧化能力(T-AOC)均采用南京建成生物工程研究所的试剂盒进行测定。
1.4.4 血浆免疫指标血浆白细胞介素(IL)-2、IL-6、IL-8、IL-10、IL-22、IL-1β、肿瘤坏死因子-α(TNF-α)、干扰素-γ(IFN-γ)以及免疫球蛋白(Ig)A、IgG、IgM含量均采用上海酶联生物科技有限公司的试剂盒进行测定。
1.5 数据统计分析试验数据采用SPSS 25.0软件进行独立样品t检验(independent samples t-test)，结果用平均值±标准误(SE)表示，P < 0.05为差异显著，0.05≤P < 0.10为有趋势。
2 结果 2.1 发酵桑叶对肥育猪生长性能的影响由表 2可知，与对照组相比，饲粮中添加发酵桑叶对肥育猪生长性能无显著影响(P>0.05)。
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表 2 发酵桑叶对肥育猪生长性能的影响 Table 2 Effects of fermented mulberry leaves on growth performance of finishing pigs |
由表 3可知，与对照组相比，发酵桑叶组血浆肌酐、尿酸、甘油三酯含量和乳酸脱氢酶活性显著降低(P < 0.05)，血浆谷草转氨酶活性有降低趋势(P=0.079)。2组之间其他血浆生化指标差异不显著(P>0.05)。
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表 3 发酵桑叶对肥育猪血浆生化指标的影响 Table 3 Effects of fermented mulberry leaves on plasma biochemical indexes of finishing pigs |
由表 4可知，与对照组相比，发酵桑叶组尿液肌酐含量显著提高(P < 0.05)，尿液尿酸含量和乳酸脱氢酶活性显著降低(P < 0.05)。2组之间尿液尿素含量和碱性磷酸酶活性差异不显著(P>0.05)。
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表 4 发酵桑叶对肥育猪尿液生化指标的影响 Table 4 Effects of fermented mulberry leaves on urine biochemical indexes of finishing pigs |
由表 5可知，与对照组相比，发酵桑叶组血浆GSH含量显著提高(P < 0.05)。2组之间其他血浆抗氧化指标差异不显著(P>0.05)。
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表 5 发酵桑叶对肥育猪血浆抗氧化指标的影响 Table 5 Effects of fermented mulberry leaves on plasma antioxidant indexes of finishing pigs |
由表 6可知，与对照组相比，发酵桑叶组血浆IL-2、IL-6、IL-8、IL-22、TNF-α、IFN-γ、IgA含量显著提高(P < 0.05)，血浆IgG和IgM含量有提高趋势(P=0.084和P=0.068)。2组之间血浆IL-10和IL-1β含量差异不显著(P>0.05)。
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表 6 发酵桑叶对肥育猪血浆免疫指标的影响 Table 6 Effects of fermented mulberry leaves on plasma immune indexes of finishing pigs |
桑叶(发酵/青贮)对动物生长性能的影响与动物品种有关。研究发现，饲粮中高达9%的桑叶添加量不影响湘村黑猪生长性能[5]，而4%和5%的桑叶添加量降低了商品猪饲料转化率[7, 9]；饲粮中添加桑叶和青贮桑叶不影响牛和羊的ADG、F/G、末重[10-12]。由此可见，草食动物和本地猪种(黑猪)耐受较高添加量的桑叶。另外，桑叶对动物生长性能的影响也和桑叶添加量、动物生理阶段有关。饲粮中添加45%~60%桑叶粉会增加精料中膳食纤维的含量，降低湖羊的末重、干物质采食量、ADG[13]。饲粮中添加25.5%发酵桑叶可以提高母猪泌乳期采食量，缓解体重下降，并增加21日龄仔猪的断奶体重[14]。饲粮中添加0.03%~0.09%桑叶多糖对仔猪生长性能无显著影响[15]。饲粮中桑叶添加量达12%和15%时显著降低了肥育猪饲料转化率[5-6]，而桑叶添加量达6%时可提高肥育猪末重和ADG[16]。本研究中，饲粮中添加10%发酵桑叶未对商品肥育猪的生长性能产生不利影响。这从侧面反映出发酵改善了桑叶的适口性。发酵后桑叶的单宁含量降低了56.40%，有助于桑叶适口性的提高。发酵桑叶粗蛋白质含量较高，饲喂发酵桑叶替代部分玉米和豆粕后，保持了肥育猪的生长性能。饲喂湿发酵桑叶(长度1~2 cm)与饲喂桑叶干粉不同，大粒径饲料需要动物咀嚼，能量损耗可能是发酵桑叶未能提高肥育猪生长性能的一个原因。研究表明，饲粮中添加3%桑叶粉和3%发酵桑叶粉(含乳酸杆菌、酵母菌和枯草芽孢杆菌)提高了肉鸡ADG和ADFI，3%发酵桑叶粉组的F/G显著低于基础饲粮组和3%桑叶粉组[17]。发酵桑叶粉效果优于桑叶粉，与饲粮中抗营养因子含量的减少、大分子有机物通过发酵降解成小分子易吸收利用以及益生菌的存在有关。根据上述试验可以推测，饲粮中添加10%发酵桑叶饲喂肥育猪效果优于添加10%桑叶。饲粮中添加芽孢杆菌[18-20]、酵母[21]、乳酸菌[22]可以提高动物生长性能。但是，饲粮中添加含有乳酸菌、地衣芽孢杆菌、酵母的发酵桑叶未能改善猪生长性能，这可能与饲料配方、发酵桑叶添加量、肥育猪日龄或环境特征有关。
3.2 发酵桑叶对肥育猪血浆和尿液生化指标的影响大量研究证明了桑叶具有降血脂作用[2, 23-24]。饲粮中添加5%桑叶粉显著降低了猪血清甘油三酯和游离胆固醇含量，不影响总胆固醇含量[25]。Zeng等[6]也报道，饲粮中添加15%桑叶粉降低了猪血清甘油三酯含量，提高了血清高密度脂蛋白胆固醇含量。本试验中，与对照组相比，发酵桑叶组血浆甘油三酯含量显著降低，而血浆总胆固醇含量无显著差异。桑叶中具有降脂功能的1-脱氧野尻霉素、多糖、酚类物质[2]是发酵桑叶降脂的原因之一。此外，膳食纤维能通过抑制胆固醇吸收、增加胆汁酸排泄以及改变肠道微生态来改善血液脂质分布[26]。发酵桑叶组血脂的降低可能是摄入较多纤维引起的，发酵桑叶组饲粮的粗纤维水平高于对照组。另外，IL-6和TNF-α促进脂肪分解并抑制脂质合成，能降低血液甘油三酯和总胆固醇含量[27]。这与发酵桑叶组血浆TNF-α和IL-6含量提高和甘油三酯含量降低是相符的。
血浆肌酐、尿酸、尿素是肾功能的标志物[28-29]。研究发现，饲喂9%桑叶粉的猪血浆尿酸和尿素含量较低[30]。本试验中，饲粮中添加发酵桑叶减少了猪血浆尿酸和肌酐含量，未改变血浆尿素含量。为了解发酵桑叶是否通过增加氮代谢物排泄来减少血浆中肌酐和尿酸含量，本试验测定了尿液中的这些物质含量，发现与对照组相比，发酵桑叶组尿液肌酐含量显著增加，尿液尿酸含量显著降低。这说明发酵桑叶通过增加尿液肌酐的排泄来减少血液肌酐含量。饲粮中添加发酵桑叶降低了血浆和尿液尿酸含量，意味着机体产生的尿酸更少。尿酸由内源性嘌呤代谢产生[31]。大豆属于高嘌呤食物[32]，发酵桑叶组的猪摄入的嘌呤减少，从源头上减少了尿酸的产生。此外，发酵桑叶的活性成分如芦丁、槲皮素、桑黄素、桑椹苷A、多糖、维生素C等均具有保护肾脏作用，可减少氮代谢物的产生[15, 33-36]。此外，膳食纤维可以通过减弱膳食腺嘌呤的吸收来降低血清尿酸和尿素氮含量[37-38]。益生菌可以减少动物血液中肌酐含量[39]。发酵桑叶中纤维和益生菌也许对机体中这些含氮代谢物产生了积极影响。血浆总蛋白和白蛋白含量反映了蛋白质合成分解的状态[30]。青贮桑叶不影响动物血液总蛋白、白蛋白、球蛋白含量[10-12]。本试验中，饲粮粗蛋白质水平一致，发酵桑叶组血浆总蛋白和白蛋白含量与对照组相似，但是发酵桑叶组的血浆氮代谢物含量低于对照组，这从侧面反映出发酵桑叶提高了氮的利用率，促进了蛋白质合成代谢或减少蛋白质分解代谢，有利于猪体内蛋白质的沉积。
本试验中，饲粮中添加发酵桑叶有降低谷草转氨酶活性的趋势。红曲菌发酵桑椹糟可降低糖尿病小鼠血液转氨酶活性，还可以降低尿素氮和肌酐含量，改善肾小球体积，减少肾脏肿胀和炎症[24]。同样地，虫草发酵桑叶提取物饲喂小鼠12周对肝脏和肾脏没有产生毒性[23]。发酵桑叶组尿液乳酸脱氢酶活性的减少表明肾功能改善，血浆肌酐和尿酸含量的减少也证实了这点。这与Ullah等[40]研究结果相似，桑果提取物减少了尿液乳酸脱氢酶活性。饲粮中添加桑叶(提取物)降低了动物血清和组织乳酸脱氢酶活性[41-42]。由此可见，饲粮中添加10%发酵桑叶改善了肥育猪的肝脏和肾脏功能，有益于动物健康。
3.3 发酵桑叶对肥育猪血浆抗氧化指标的影响抗氧化酶可作为抗氧化反应的标志物，谷胱甘肽是重要的内源性小分子抗氧化剂，可保护细胞免受化学诱导的细胞毒性[43]。桑叶含有大量具有抗氧化和抗炎作用的类黄酮、多酚及其他活性物质，能缓解动物生产中的氧化应激[1, 44-45]。本试验中，饲粮中添加发酵桑叶未提高猪血浆抗氧化酶活性的结果与以往研究不符。以往研究认为，饲粮中添加桑叶粉可提高猪血清GSH含量和GPX-Px、SOD活性以及T-AOC[5-6, 9]。饲粮中添加桑叶(青贮)可提高羔羊和鸡血清CAT、GPX-Px、SOD活性以及T-AOC，降低血清MDA含量[11, 44]。本试验中，发酵桑叶组血浆GSH含量显著高于对照组，这表明发酵桑叶可能通过增加非酶促抗氧化剂含量来改善机体抗氧化能力，而不是通过增加抗氧化酶活性来提高机体抗氧化能力。
3.4 发酵桑叶对肥育猪血浆免疫指标的影响免疫反应与动物的健康密切相关。TNF-α在宿主防御中起重要作用，协同INF-γ激活巨噬细胞，增强免疫作用[27]。本试验中，发酵桑叶组血浆TNF-α和INF-γ含量的提高有助于机体免疫力的改善。TNF-α可以刺激IL-6和IL-8产生，IL-6对于B细胞分化和抗体产生至关重要[27]。IL-8有助于适应性免疫反应的泛化和强化[46]。这与发酵桑叶组血浆中这三者含量的提高是一致的。IL-22促进上皮稳态并抑制炎症，维持机体的防御屏障[47]。本试验中，饲粮中添加发酵桑叶提高了肥育猪血浆细胞因子(IL-2、IL-6、IL-8、IL-22、TNF-α、IFN-γ)含量，与以往研究结果[8, 48-49]相似。饲粮中添加桑叶多糖可提高仔猪血清IL-1β、IL-2、IL-6、IL-8、IFN-γ含量，改善仔猪免疫力[8]。桑叶提取物诱导细胞因子(TNF-α、IFN-γ、IL-1β、IL-6、IL-10)分泌，调节机体免疫活性[48-49]。IgG、IgA、IgM是体液免疫的主要参与者，在免疫系统中发挥重要作用[50]。饲粮中添加桑叶多糖能提高仔猪血清IgG和IgM含量[8]。本试验中，发酵桑叶组血浆免疫球蛋白含量均高于对照组，表明发酵桑叶改善了肥育猪的免疫功能。植物化学物质是机体免疫的潜在调节剂。发酵桑叶富含的多酚和多糖等活性物质可通过提高血清细胞因子含量或影响微生物群来抑制炎症过程[11, 51-52]。发酵桑叶中的益生菌与肠道微生物、上皮细胞、免疫细胞相互作用以刺激免疫功能[53]。
3.5 发酵桑叶的益处在本试验条件下观察到的发酵桑叶益处可能是因为发酵桑叶富含抗氧化和免疫调节等特性的活性成分和益生菌，这些物质改善了肥育猪生理代谢，促进了机体健康。天然物质的生物利用度在微生物发酵后通常会增加[54]。乳酸菌发酵桑叶提取物的总多酚、总黄酮、绿原酸含量高于桑叶提取物[55]。发酵可提高桑叶多酚(36.15%)[9]和1-脱氧野尻霉素(77%~190%)产量[56]。蛹虫草发酵桑叶具有抗炎和抗自噬活性[57]。发酵桑叶的有益成分综合作用改善机体代谢、抗氧化能力、免疫功能，降低血脂和含氮代谢物含量，保护动物机体健康。另外，饲粮中添加10%发酵桑叶对肥育猪生长性能无负面影响。因此，发酵桑叶可作为肥育猪的饲料资源，采用发酵桑叶喂猪是一种绿色健康的饲喂策略。
4 结论饲粮中添加10%发酵桑叶对肥育猪生长性能无负面影响，改善了血浆和尿液代谢物含量，提高了机体抗氧化能力和免疫功能。
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