低聚木糖是通过β-1, 4糖苷键将2~8个木糖分子连接起来的寡糖[1],主要有效成分包括木二糖、木三糖和木四糖,其来源广泛,由甘蔗渣、玉米芯、稻壳、秸秆等富含半纤维素的农作物副产品水解而得[2]。低聚木糖在pH 2.5~8.0稳定性高,并具有耐高温的特点[3]。动物体内缺乏水解β-1, 4糖苷键的消化酶,因此低聚木糖可直接经过胃和小肠,进入消化道后段,经肠道微生物发酵产生的短链脂肪酸(SCFAs),如乙酸盐、丙酸盐、丁酸盐降低肠道pH,抑制有害菌生长繁殖,促进双歧杆菌、乳酸杆菌的定植,选择性刺激与健康和福利相关的肠道微生物群的生长和活性的变化[4]。低聚木糖具有增强先天免疫[5]、调节血脂水平[6]、提高抗氧化功能[7]和改善肠道形态结构的特点[8]。影响低聚木糖使用效果的因素有很多,包括其结构组成、添加剂量、饲粮种类、饲养环境以及动物个体之间的差异,因而在畜禽应用上的研究结论并不一致。本文综述了低聚木糖对肉鸡生长性能、肉品质、氮代谢及粪便氨气释放、血清生化指标、抗氧化功能、肠道组织形态、免疫功能和采食行为的影响,为进一步研究和应用低聚木糖提供参考。
1 低聚木糖对肉鸡生长性能和肉品质的影响 1.1 低聚木糖对肉鸡生长性能的影响低聚木糖对肉鸡生长性能的影响报道并不一致。有学者认为添加适宜水平的低聚糖对禽类生长性能、屠宰性能以及健康状况有明显的改善。由于机体健康状况得到改善,用于抵御、排除病原微生物消耗的能量支出转化到生产中,使饲料转化率也有明显提高[9]。Craig等[10]在小麦型饲粮中添加0.25和1.00 g/kg低聚木糖均降低了28日龄肉鸡采食量和饲料转化率。冷智贤等[11]研究发现,豆粕型基础饲粮中添加100 mg/kg的低聚木糖可显著提高肉鸡21和42日龄平均体重及1~21日龄平均日增重。Courtin等[12]报道,小麦型基础饲粮中添加0.5%或玉米型基础饲粮中添加0.25%的麦麸源阿拉伯低聚木糖均可提高肉鸡饲料转化率。De Maesschalck等[13]试验结果也表明,小麦型基础饲粮添加0.2%和0.5%的低聚木糖可显著提高肉仔鸡初期和生长期饲料转化率,整个试验期间的饲料转化率也显著提高,但0.5%的低聚木糖对不同时期平均体重均没有显著影响。综上所述,低聚木糖通过提高肠道消化酶活性,促进与生长相关的激素分泌,增加肠道SCFAs含量[14],从而将饲料中难以分解的大分子营养物质转变为易被消化吸收的小分子营养物质。同时,低聚木糖经有益菌代谢产生的SCFAs为肠上皮细胞(IEC)吸收营养物质提供能量[4],因此,低聚木糖可在一定程度上改善肉鸡生长性能。然而,Luo等[15]试验发现,玉米-豆粕型基础饲粮中添加150 mg/kg低聚木糖对肉仔鸡体增重、采食量、饲料转化率均无显著影响。Ribeiro等[16]研究表明,玉米型基础饲粮中添加0.1 g/kg低聚木糖组与未添加组相比虽然肉鸡体重较高,但是随着添加水平的提高,高剂量组(10.0 g/kg)与未添加组的体重类似。索海青等[17]报道,玉米-豆粕型基础饲粮中低聚木糖添加水平在160~1 600 mg/kg时,对1~21日龄和22~42日龄肉仔鸡生长性能和死亡率的影响均不显著。关于低聚木糖对肉鸡生长性能影响的报道不一致的原因可能是肉鸡存在一个适应期,低聚木糖使食糜通过消化道的速度加快,导致营养物质来不及吸收,或与添加剂量和产品形式的差异有关。
1.2 低聚木糖对肉鸡肉品质的影响肉色、肌肉pH、嫩度和系水力是综合反映肉品质的指标,肌肉pH反映屠宰后体内糖原酵解的速度,与其他肉品质指标密切相关。据报道,青脚麻鸡饲粮中添加低聚木糖合生元有利于改善肉品质,降低了屠宰后胸肌蒸煮损失和24 h滴水损失[18]。Suo等[19]试验结果表明,肉鸡腿肌滴水损失随着低聚木糖添加水平的提高呈线性下降,当添加量为100 mg/kg时腿肌滴水损失最低,但对胸肌肉品质没有显著影响。研究表明,肉鸭肌肉较高的抗氧化酶活性使pH、系水力提高,肉色也更加稳定,可抑制脂质氧化并参与肉质的调节[20],因此,肌肉系水力的提高可能与低聚木糖的抗氧化性有关。陈倩妮[21]试验发现,低聚木糖能降低肉鸡腹脂率,而对胸肌率和腿肌率没有显著影响,0.3%添加水平有利于提高肌肉粗蛋白质和粗脂肪含量,这可能是由于含有大量消化酶的有益菌在肠道中增殖,促使一些不能被自身内源酶降解的大分子营养物质得到吸收利用,降低了血氨浓度,使体内蛋白质的蓄积增加所致。邓文等[22]报道,单独添加丁酸梭菌和低聚木糖以及同时添加两者能显著降低肉鸡的腹脂率。综上所述, 丁酸梭菌和低聚木糖可互作改善肉鸡生长性能、屠宰性能和肉品质。
2 低聚木糖对肉鸡氮代谢及粪便氨气释放的影响血清总蛋白(TP)及白蛋白(ALB)的含量能准确反映机体蛋白质吸收状况,血清尿素氮(UN)和尿酸(UA)是家禽利用蛋白质的产物,可直接反映氨基酸和蛋白质的代谢情况,蛋白质代谢良好时,血清UN含量降低。肉鸡饲粮中有约2/3的氮沉积到肌肉中或被组织吸收,剩下约1/3的氮不能被利用而排出体外[23]。据Hou等[24]报道,低聚木糖可以降低血清UN含量,而对血清TP、ALB含量影响的报道结果不一致。王鹏[25]在玉米-豆粕型饲粮中添加300 g/t(即300 mg/kg)低聚木糖可显著提高肉仔鸡血清TP、ALB含量。陈雁南等[26]则报道,添加150 mg/kg低聚木糖显著降低肉鸡血清TP和ALB含量。氮代谢报道不一致的原因可能与饲粮氨基酸水平、肉鸡生长阶段的代谢水平不同以及肠道微生物区系有关。
氨气是鸡舍中危害最大的有害气体之一,主要来源于含氮有机物如粪便的分解。当有害菌在肠道中的活动增强时,蛋白质更多地转化成胺、氨以及其他腐败物质[27]。Kajihara等[28]研究表明,低聚木糖可以通过抑制产氨厌氧菌(如拟杆菌)的肠道定植来发挥作用,粪便恶臭物质生成量减少可能是因为分解氨基酸产生氨气的细菌主要是革兰氏阴性菌。Christophersen等[29]在人类结肠模拟器中,通过混合粪便微生物群向发酵大豆蛋白添加低聚木糖或菊粉,发现低聚木糖可通过特定的菌群和SCFAs调节蛋白质诱导的结肠环境的遗传毒性。这是由于大多数结肠蛋白酶在中性条件下发挥最佳作用,SCFAs的产生导致结肠pH降低,从而抑制了蛋白酶活性[30],SCFAs含量增加时也可以抑制蛋白质的降解(抑制脱氨基作用)[31]。
3 低聚木糖对肉鸡血清生化指标的影响血清生化指标的变化可反映机体的代谢状况,Samanta等[32]报道,玉米壳来源的低聚木糖显著降低了肉鸡血清胆固醇(CHOL)、葡萄糖(GLU)、极低密度脂蛋白(VLDL)、低密度脂蛋白(LDL)和甘油三酯(TG)的含量。低聚木糖对脂代谢的调控可能是通过有益菌发酵产生的SCFAs介导的[33]。研究发现,饲粮中添加菊粉可显著降低仓鼠血浆中TG、VLDL和总胆固醇的含量,刺激胆汁酸的合成[34]。为了维持肠肝循环所需的结合胆汁酸水平,排泄的胆汁酸被体内胆固醇合成新的胆汁酸所替代,从而发挥降低体内CHOL的潜力[35],结肠发酵产物丙酸盐也能抑制肝脏脂肪的形成[36]。也有研究发现,SCFAs通过降低过氧化物酶体增殖物激活受体γ(PPARγ)及靶基因Cd36、Lpl、Fabp4和Pltp在肝脏和脂肪组织中的表达来调节脂质代谢[37]。甲状腺激素(TH)可调节多种生理过程,包括细胞生长、分化、代谢和增殖[38],在刺激垂体生长激素(GH)合成和分泌中起关键作用[39]。范艳平[40]在肉鸡饲粮中添加棉籽壳源低聚木糖菌糠显著提高了血清三碘甲状腺原氨酸(T3)、甲状腺素(T4)、GH和胰岛素(Ins)含量。李淑珍等[14]研究也发现,饲粮添加低聚木糖可显著增加肉鸡血清GH和T3的含量,并显著降低血清T4含量,可能是在低聚木糖的作用下,一部分T4转化成T3,使总体上T3所占比例显著增加,正向调控肉鸡生长速率,与Sun等[41]、Iqbal等[42]发现低聚糖能显著增加血清T3含量的报道一致。
4 低聚木糖对肉鸡抗氧化功能的影响氧化应激是一种不平衡的状态,产生的一系列活性氧(ROS),如超氧阴离子(O2-)、过氧化氢(H2O2)和羟自由基(·OH)的含量超过正常细胞功能所需的水平时,将压倒内源性抗氧化能力和修复能力[43]。氧化应激通过破坏蛋白质和核酸、诱导脂质过氧化产生大量丙二醛(MDA)等方式对细胞造成损伤,导致内环境失衡并引发疾病[44]。肉鸡生长中后期随着机体的衰老,自由基产生和脂质过氧化作用加剧,生理机能减退。超氧化物歧化酶(SOD)、过氧化氢酶(CAT)、谷胱甘肽还原酶(GR)、谷胱甘肽过氧化物酶(GSH-Px)和黄嘌呤氧化还原酶(XOR)负责维持自由基形成和清除之间的平衡[45]。Boonchuay等[46]报道,玉米芯来源的低聚木糖具有良好的2, 2′-二苯-1-吡啶肼(DPPH)和2, 2′-叠氮-双(3-乙基苯并噻唑啉-6-磺酸)(ABTS)自由基清除活性和铁还原抗氧化能力(FRAP),总酚类化合物含量显著提高。研究表明,低聚木糖可增强动物的抗氧化能力[47-48]。赵颖[49]也报道,低聚木糖添加组肉鸡21日龄血清MDA含量降低,血清总抗氧化能力(T-AOC)提高,尤其是75 mg/kg超微低聚木糖组其血清T-AOC显著高于常规低聚木糖组。杨卫兵[50]试验结果表明,饲粮添加100 mg/kg的低聚木糖可提高肉鸡血清SOD和CAT活性,降低血清MDA含量。Chen等[51]在肉鸡饲粮中添加1.5 g/kg合生元(1.5 g合生元含有150 mg低聚木糖、3×109 CFU丁酸梭菌和4.5×1010 CFU枯草芽孢杆菌等),降低42日龄肉鸡回肠MDA含量。抗氧化能力的提高可能是因为低聚木糖促进了肉鸡肠道乳酸杆菌属的生长,乙酸盐和丙酸盐浓度增加[52],低聚木糖使受试黄鸡体内SOD活性,与对照组比较显著提高[53]。
5 低聚木糖对肉鸡肠道组织形态的影响小肠是消化吸收的主要场所和关键器官,肠壁厚度、绒毛高度和隐窝深度可作为衡量肠道形态的指标。绒隐比(VH/CD)通常用作评估肠道绒毛吸收营养物质能力的标准,其数值的增加意味着小肠吸收能力更强。杯状细胞的数量常用于评估肠道完整性,有研究发现,150 mg/kg低聚木糖添加水平使肉鸡十二指肠和空肠杯状细胞数量增加,有利于保护肠黏膜屏障[15]。赵颖[49]研究发现,玉米-豆粕型饲粮添加75 mg/kg超微粉碎低聚木糖虽然对十二指肠肠道形态无显著影响,但可显著增加回肠绒毛高度,降低空肠隐窝深度,提高空肠VH/CD值,说明超微粉碎低聚木糖可在一定程度上改善肉鸡肠道黏膜结构。Suo等[19]在玉米-豆粕型饲粮中添加75 mg/kg低聚木糖,对肉鸡十二指肠绒毛高度和宽度均无显著影响,但显著降低了十二指肠隐窝深度。Wang等[54]也报道,玉米-豆粕型饲粮中添加100 mg/kg低聚木糖对肉鸡十二指肠的长度及相对重量产生有利影响,显著提高肉鸡所有肠段绒毛高度和VH/CD。不一致的是,吴媛媛等[9]在玉米-豆粕型饲粮中分别添加1、2和4 g/kg低聚木糖,发现对肉鸡空肠绒毛高度和隐窝深度均无显著影响。研究表明,饲喂阿拉伯低聚木糖可以刺激或“启动”饲粮中阿拉伯木聚糖的消化,从而促进幼龄肉鸡肠道中纤维发酵微生物组的发育[55]。肠道形态的改变可能是因为益生菌通过与病原体竞争有限的营养,抑制病原体对肠上皮、黏膜的黏附和侵袭,产生抗菌物质或刺激了黏膜免疫[56],肠道细菌的多样性提高并改变了微生物的组成[57]。有益菌代谢产生的SCFAs是肠道微生物菌群和肠上皮细胞的重要能量来源[58],细胞增殖主要发生在隐窝的下半部分,有丝分裂产生的压力迫使细胞沿隐窝轴上升[59],促进隐窝分裂的细胞向脱落的肠绒毛上皮细胞方向移动,增加了绒毛高度,基部细胞生成速率缓慢从而降低了隐窝深度。当前,市场上用于生产低聚木糖的原料来源广泛,由于所含有效成分的不同导致在肉鸡饲粮中的添加剂量差异很大,因此,低聚木糖对肉鸡肠道组织形态的影响及其机理有待进一步研究。
6 低聚木糖对肉鸡免疫功能的影响低聚木糖本身具有免疫源性,可诱导免疫系统中的多种细胞因子,激活巨噬细胞和T、B淋巴细胞,发挥免疫调控作用。经抗原提呈细胞激活免疫应答,促进免疫细胞增殖分化[60]。微生物代谢产物SCFAs可通过激活G蛋白偶联受体(FFAR2、FFAR3、GPR109a和Olfr78)来调节IEC和白细胞的发育、存活及功能;调节酶和转录因子的活性,建立微生物群和免疫系统之间的联系[61];通过抑制组蛋白脱乙酰酶(HDAC)的活性促进T细胞分化为效应T细胞和调节T细胞[62]。肿瘤坏死因子-α(TNF-α)、白细胞介素-1(IL-1)、白细胞介素-1β(IL-1β)、白细胞介素-6(IL-6)、前列腺素E2(PGE2)、诱导型一氧化氮合酶(iNOS)及环氧合酶-2(COX-2)等促炎细胞因子和炎性介质触发炎症联动效应[63]。体外试验发现,低聚木糖在脂多糖(LPS)刺激的巨噬细胞RAW264.7中以剂量依赖性的方式抑制TNF-α、IL-1β、IL-6和一氧化氮(NO)的产生[64]。特定的肠道微生物可以通过连接到上皮细胞和免疫细胞上的Toll样受体和其他模式识别受体来刺激宿主免疫系统[65]。Yuan等[66]报道,添加2 mg/kg低聚木糖可显著增加肉鸡血浆免疫球蛋白G(IgG)含量,下调21和42日龄空肠干扰素-γ(IFN-γ)、LPS诱导的肿瘤坏死因子(LITAF)和Toll样受体5(TLR5)的mRNA表达水平。发酵产物乙酸盐、丙酸盐和丁酸盐是能力最强的SCFAs,可诱导钙动员,调节免疫系统中的白细胞功能[67]。Pourabedin等[68]发现,感染肠炎沙门氏菌的肉仔鸡饲粮中添加2 g/kg低聚木糖,肉仔鸡盲肠扁桃体中LITAF和IL-6的含量显著降低。而Singh等[69]试验结果表明,饲粮添加100 mg/kg的低聚木糖,肉鸡回肠中白细胞介素-4(IL-4)和白细胞介素-10(IL-10)含量显著提高。据Jazi等[70]报道,在感染鼠伤寒沙门氏菌的肉鸡饲粮中添加2 g/kg低聚木糖,可显著降低肝、脾脏和法氏囊等免疫器官的沙门氏菌数量,同时显著降低血清嗜异性粒细胞与淋巴细胞数量比(H/L),从而增强免疫应答。Sun等[41]通过检测肉鸡血清AI H5N1抗体滴度发现,饲粮添加5、10和20 g/kg低聚木糖,肉鸡24日龄血清抗体滴度均显著高于对照组,且10 g/kg添加水平在59日龄时的血清抗体滴度仍显著提高,因此,研究认为低聚木糖可以通过刺激抗体的产生来提高肉鸡体液免疫。袁缨等[71]研究也发现,果寡糖、甘露寡糖、低聚异麦芽糖、低聚木糖均可改善肉仔鸡免疫器官指数,其中低聚木糖提高胸腺、脾脏、法氏囊指数的效果优于其他低聚糖,与冷智贤等[11]、杨卫兵[50]使用低聚木糖提高肉鸡免疫器官指数的报道一致。综上所述,低聚木糖可以刺激机体细胞免疫和体液免疫,使免疫器官指数在正常范围内提高,可能是因为有益菌和代谢产物作为抗原物质间接促进了免疫器官的发育和成熟。
低聚木糖还可以提高肠黏膜局部免疫力。SCFAs诱导肠道巨噬细胞的抗微生物活性并增加对病原体的抵抗力[72],分泌型免疫球蛋白A(sIgA)是肠黏膜表面最突出的抗体,起着重要的防御作用。杨卫兵[50]报道,饲粮添加100 mg/kg低聚木糖能提高肉鸡空肠和回肠sIgA含量。Min等[73]通过添加低聚木糖、甘露低聚糖和枯草芽孢杆菌组成的合生元研究对肉仔鸡肠道形态和肠黏膜sIgA含量的影响,结果发现能显著提高sIgA含量,新增的抗体覆盖在肠黏膜表面来保护绒毛免受损伤。sIgA受到抗原刺激时分泌量增加,尤其是受到肠道微生物的刺激,可能是低聚木糖促进了sIgA的分泌来提高肠黏膜免疫力。
7 低聚木糖对肉鸡采食行为的影响行为评价指标是衡量动物健康和福利状况的可靠性指标,采食行为与动物生产性能的高低有直接关系。大量研究表明,饲粮味道[74]、粒度[75]、营养成分[76-77]等因素影响肉鸡的采食行为。韩淑云[78]报道,饲粮添加可溶性纤维可通过增加禽类的顿间间隔时间来提高饱腹感,进而影响采食行为。近年的研究发现,饲喂添加0.5%的阿拉伯低聚木糖的饲粮后,肉鸡回肠食糜黏度均高于对照组[55],因此,推测阿拉伯低聚木糖可能提高了小肠内容物的黏度,延长营养物质在消化道的运输和吸收从而增加了饱腹感。肠道菌群代谢产生的SCFAs可通过与G蛋白偶联受体(GPCRs),如GPR41和GPR43结合来调节基因表达,由GPR41和GPR43发出的信号会影响广泛的生物学功能,其中包括参与食欲控制的激素和Ins的分泌[79]。目前,国内外有关低聚木糖对肉鸡采食行为的影响至今尚未见报道,且低聚木糖略带特殊气味,是否会影响肉鸡对饲粮的采食偏好性进而影响采食行为有待研究。
8 小结低聚木糖在提高肉鸡抗氧化能力、免疫功能和改善肠道组织形态等方面发挥的积极作用,已被大量试验证实,但是对于生长性能的报道没有一致的结论。这是由于目前市场上生产低聚木糖的原料广泛,且有效成分(木二糖、木三糖和木四糖)的含量不同,导致在饲粮中的添加剂量差异很大。此外,低聚木糖的使用效果还与饲粮种类和试验动物的品种、日龄以及健康状况密切相关。因此,添加低聚木糖对生长性能并不一定产生积极的影响,具体因素和最适添加水平还需进行更多的研究加以论证。采食行为也是动物生产的一个重要方面,通过采食行为将机体所需的各种营养物质摄入体内,以满足生长发育的需要。研究低聚木糖对肉鸡采食行为的影响及其作用机制,有望进一步为低聚木糖在肉鸡生产中的合理应用提供参考依据。
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