通过在蛋鸡和肉鸡饲粮中合理添加氨基酸和酶制剂，并根据氨基酸平衡模式理论配制的低蛋白质饲粮，不仅可以高效利用其中的蛋白质，减少蛋白质饲料原料的使用量和养殖饲料成本，实现源头节粮；而且还可以降低排泄物中氮含量，有效改善养殖环境。《产蛋鸡和肉鸡配合饲料》(GB/T 5916—2020)[1]标准的实施有效地推进了低蛋白质饲粮在养殖生产中的应用。
动物的肠道是营养物质消化吸收的场所，其依赖于肠黏膜最外层的黏蛋白与底部细胞膜之间的相互作用形成一个屏障，从而对吸收过程中潜在的危害起到抵抗作用[2]。小肠中的黏蛋白会因饮食和肠道微生物群的变化而发生动态变化[3]。已有的研究表明，仔猪需要一定水平的肠内营养物质摄入量，用于维持肠黏膜的生长和黏膜蛋白的合成[4]。低蛋白质饲粮尽管补充了晶体必需氨基酸，但降低饲粮粗蛋白质水平会导致猪中后段肠道的蛋白质代谢改变，这可能会损害外周组织对氨基酸的利用，因此在补充晶体氨基酸的低蛋白质饲粮中，用于肠黏膜的氨基酸减少对肠道形态维持的长期影响值得进一步研究[5]。猪肠道对氨基酸的消化、吸收与其菌群构成[6]和黏膜功能[5]等有重要的相关性，而饲粮氮水平和氨基酸组成对肠道菌群结构、屏障功能及肠道健康等均有明显的影响[7-8]。家禽与猪等哺乳动物相比，在消化系统组成、肠道结构和消化时间等方面均存在明显的不同[9]。本文围绕低蛋白质饲粮对家禽肠道形态结构与屏障功能的作用和影响进行了综述，以期为肠道健康相关研究和低蛋白质饲粮在家禽生产中的应用提供参考。
1 低蛋白质饲粮与应用概况低蛋白质饲粮是在平衡氨基酸的基础上，通过降低饲粮粗蛋白质水平2~4个百分点，并保证动物维持正常的生产性能和健康状况。养殖生产中，低蛋白质饲粮下补充必需氨基酸，可以提高饲粮蛋白质的利用效率，减少氮排泄量，而对其生产性能没有影响[10-11]。但是，低蛋白质饲粮的应用对蛋鸡生产性能影响的研究结果不一致。Keshavarz等[12]报道，饲粮13.0%粗蛋白质水平并补充必需氨基酸条件下，蛋鸡的生产性能与饲粮16.0%~16.5%粗蛋白质水平条件下相当。而Shim等[13]研究表明，蛋鸡饲粮粗蛋白质水平降低4个百分点，即使补充必需氨基酸也会造成蛋鸡生产性能的下降。本实验室前期研究表明，低蛋白质饲粮(9.2%粗蛋白质)抑制了蛋鸡食欲和载脂蛋白合成，并与其生产性能的改变有关[14]。此外，低蛋白质饲粮条件下，蛋鸡适宜氨基酸的比例变化也可能是生产性能改变的原因。Parenteau等[15]研究表明，20~46周龄蛋鸡的饲粮粗蛋白质水平降低2个百分点，获得最佳生产性能的异亮氨酸∶赖氨酸从80%增加至82%~84%。本实验室最近的研究也表明，蛋鸡饲粮粗蛋白质水平从16%降至14%，精氨酸不足(0.80%)会导致肠黏膜氧化损伤加剧，33~40周龄海兰褐蛋鸡在饲粮14%粗蛋白质条件下获得最优生产性能的精氨酸水平为0.86%[16]。
2 低蛋白质饲粮对家禽肠道形态结构的影响肠道是家禽消化吸收营养物质的场所，在致病菌感染家禽或肠道内条件性致病菌大量增殖的情况下，肠道内微生物和抗原等容易突破肠道屏障，造成家禽肠道疾病、生产性能下降和经济效益损失。肠道健康的标准就是肠道结构和功能完整、能够快速消化和吸收营养物质以及肠道微生物菌群和免疫系统保持稳定[17]。所以，肠道既是病原微生物和毒素等入侵机体的主要部位，又是阻止肠道致病性微生物感染的重要屏障[18-20]。
肠道黏膜的完整性是确保营养物质消化吸收的生理基础，是影响畜禽的肠道健康和正常生长发育的保障。肠黏膜绒毛高度、隐窝深度是反映肠道形态、功能和健康的重要指标[21]。肠绒毛高度越高，肠道的吸收面积就越大，促进消化的营养物质吸收转运就更加充分；隐窝深度代表肠上皮细胞生成速率，肠道健康与隐窝深度呈负相关[22]。已有的研究表明，低蛋白质饲粮能够增加肠道黏膜绒毛高度，从而增加消化吸收的表面积；能够降低隐窝深度，从而提高肠道的消化吸收能力[23-25]。但是，低蛋白质饲粮在家禽上对肠道形态结构的改善作用与饲粮粗蛋白质水平的降低程度有关。Zaefarian等[26]研究表明，饲粮粗蛋白质水平降低1.5个百分点，并通过补充合成氨基酸并不影响小肠黏膜形态；但粗蛋白质水平降低3.0个百分点时，就会显著减少小肠吸收面积，改变小肠黏膜形态，不利于机体对营养物质的消化和吸收。
3 低蛋白质饲粮对家禽肠道屏障功能的影响动物肠道屏障功能主要依靠肠黏膜、肠道细胞和分泌物以及微生物等实现，且包括物理屏障、化学屏障、免疫屏障和生物屏障[27]。肠道屏障形成了动物机体内环境与外界环境之间连通的界面，肠道屏障功能的发挥保障了饲粮营养物质的正常吸收，同时也有效阻止了诸如内毒素、微生物等有害物质通过肠上皮进入机体内部组织[28]。
3.1 低蛋白质饲粮对家禽肠道物理屏障的影响将肠道外部的环境因子与内部宿主环境分隔开的物理屏障，是由肠黏膜表面的黏液层、肠上皮细胞、细胞间的紧密连接以及上皮下固有层共同组成。黏液层在肠上皮细胞表面形成了紧密的保护层，以保护上皮细胞免受有毒和有害物质的侵害[28-29]。肠上皮由几种不同类型细胞组成，包括上皮细胞、潘氏细胞和杯状细胞等。这些细胞及其不同的功能在肠腔内部形成了紧密的屏障[30]。肠上皮细胞间存在紧密连接(tight junction, TJ)、黏附连接(adherens junction, AJ)、缝隙连接(gap junction, GJ)和桥粒(desmosome)等多种连接形式，使得相邻的细胞能紧密结合，防止肠道内的物质从细胞间隙穿过膜上皮，对细胞旁路的通透性起决定作用[31]。紧密连接不仅可以有效阻止病原微生物的入侵，而且可以调节肠黏膜对离子和分子的通透性，通过调节紧密连接蛋白的表达能够增强肠黏膜物理屏障功能[32-34]。Azzam等[35]在产蛋高峰期蛋鸡上的研究表明，14.16%粗蛋白质水平饲粮条件下，随着可消化苏氨酸水平的提高，回肠黏膜紧密连接蛋白——闭合蛋白(occludin)的相对表达量显著增加，并以0.57%可消化苏氨酸条件下最高。Dong等[36]研究了在14%粗蛋白质水平饲粮中添加不同水平的异亮氨酸，但其对蛋鸡回肠紧密连接蛋白——封闭蛋白-1(claudin-1)和occludin均无显著的影响。
3.2 低蛋白质饲粮对家禽肠道化学屏障的影响肠黏膜化学屏障有杀灭进入机体的有害微生物、防止毒素被机体吸收等作用[37]，主要由肠上皮分泌的黏液、消化液、黏蛋白和溶菌酶等物质组成。黏蛋白主要是由肠上皮的杯状细胞分泌，其中黏蛋白2(MUC2)对维持肠腔表面黏液层至关重要[38]，饲粮的变化可能影响黏液层的表达和完整性。研究表明，蛋鸡饲粮粗蛋白质水平降低2.44个百分点，补充丝氨酸可以通过同时调节回肠中MUC2的转录和修饰来增强回肠黏膜免疫，改善生产性能[39]。低蛋白质饲粮条件下，补充苏氨酸显著升高蛋鸡回肠MUC2的相对表达量[35]，而补充异亮氨酸对其表达量没有显著影响[36]。由此提示，低蛋白质饲粮对肠道屏障功能的影响可能与所补充氨基酸的种类及数量有关。此外，肠黏膜化学屏障对于维持动物肠道适宜的pH环境有重要作用。正常状态下，家禽肠道pH维持在较低水平(酸性)，以保障消化酶的活性和有益微生物的生长，抑制有害微生物的增殖。有研究指出，家禽体内的有益菌和病原菌生长增值受pH的调节，pH呈酸性时，乳酸菌和链球菌等有益菌群是肠道内的优势菌群；肠道环境为弱碱性时，大肠杆菌的繁殖显著增加，进而改变肠道内菌群的比例[40]。孙小沛等[41]研究表明，肉鸡饲喂15.5%粗蛋白质水平饲粮与饲喂16.0%和16.5%粗蛋白质水平饲粮相比，其十二指肠与空肠pH显著降低，这有利于肠道组织的生长发育。
3.3 低蛋白质饲粮对家禽肠道生物屏障的影响肠道内大量的共生菌附着在宿主肠道表面的黏膜层上，形成了稳定的微生态环境，构成了肠道的生物屏障，且能与致病菌竞争定植，对肠道黏膜和免疫系统的发育有促进作用[42-43]。现代研究认为，动物肠道微生物群可被看作是一个内分泌器官，其产生和分泌的代谢产物能够与宿主相互作用并在局部和远端发挥相应的作用[44]。肠道菌群能够与机体的免疫系统间相互作用影响疾病的发展，在调节局部免疫功能和抵御有害菌入侵方面发挥重要的作用[45-46]。Zaefarian等[26]在肉鸡上的研究表明，饲喂低蛋白质饲粮能减少氮的摄入，增加粪便中乳酸菌的数量，进而减少有害菌群的增殖，从而促进肉鸡肠道健康和提高机体抗热应激的能力。De Cesare等[47]研究也证实，减少肉鸡饲粮粗蛋白质摄入量(每只鸡饲养全期为82 g)，随着饲喂时间的延长，肉鸡盲肠中乳酸杆菌的丰度增加，而且这可能与36~42日龄肉鸡饲料转化率提高相关。蛋鸡上的研究也表明，低蛋白质饲粮补充蛋氨酸改变了肠道菌群组成，使得盲肠乳杆菌属的丰度增加，而粪杆菌属的比例降低[48]。Dong等[49]研究表明，蛋鸡饲喂低蛋白质饲粮引起肠道菌群多样性降低，而补充苏氨酸使菌群多样性恢复，而且显著增加潜在的肠道有益菌。
3.4 低蛋白质饲粮对家禽肠道免疫屏障的影响肠道免疫屏障主要由肠相关淋巴组织(gut associated lymphoid tissue，GALT)和弥散免疫细胞构成。肠道GALT是机体最大的淋巴器官，包括肠上皮淋巴细胞、固有层淋巴细胞、微皱褶细胞和派伊氏淋巴结等相关淋巴组织[50-51]。这些组织能诱导产生全身或局部的免疫应答反应，对防御病原菌、毒素等入侵发挥重要作用。黏蛋白增强黏膜免疫系统的一个主要途径是通过积累分泌型免疫球蛋白A(sIgA)[49]。上皮细胞分泌的sIgA是肠黏液中的主要免疫球蛋白，是肠道免疫系统的关键指标[52]，可以与抗原特异性结合，阻止有害病原体与肠黏膜的接触[53]。研究表明，饲粮中添加苏氨酸可以提高蛋鸡回肠sIgA和MUC2的表达水平，并可降低回肠中促炎细胞因子干扰素-γ(IFN-γ)和白细胞介素-1(IL-1)的表达量[54-56]。Azzam等[35]在低蛋白质饲粮中补充不同梯度的苏氨酸，回肠黏膜sIgA的表达量在一定范围内随可消化苏氨酸水平的提高而显著升高，而炎性因子INF-γ、白细胞介素-2(IL-2)、白细胞介素-6(IL-6)和白细胞介素-1β(IL-1β)的表达量显著降低。Zhou等[39]研究表明，低蛋白质饲粮中添加0.498%丝氨酸可显著上调蛋鸡回肠黏膜sIgA表达，证明回肠黏膜免疫功能得到改善，进而增强了肠道对营养物质的吸收。而Dong等[36]在低蛋白质饲粮中添加异亮氨酸的研究结果表明，不同水平的异亮氨酸对蛋鸡回肠黏膜sIgA和IL-1β的表达量均无显著影响。
4 小结综上所述，适当降低饲粮粗蛋白质水平对改善家禽肠道屏障功能、维持肠道形态结构完整性以及促进其对营养物质的吸收具有有益作用。低蛋白质饲粮添加晶体氨基酸可减少豆粕等蛋白质原料的使用量，降低饲料成本和排泄物氮排放，对从源头上缓解饲料资源紧张和养殖环保压力具有重要意义。但是，饲粮粗蛋白质水平降低范围及补充氨基酸的种类和剂量是影响其维持和改善家禽肠道健康的关键因素；另外，低蛋白质饲粮条件下，除了补充必需氨基酸外，一些非必需氨基酸在低蛋白质饲粮中的应用也应得到重视。
| [1] |
国家市场监督管理总局, 国家标准化管理委员会. 产蛋鸡和肉鸡配合饲料: GB/T 5916—2020[S]. 北京: 中国标准出版社, 2020. State Administration for Market Regulation, Standardization Administration of the People's Republic of China. Formula feeds for layers and broilers: GB/T 5916—2020[S]. Beijing: Standards Press of China, 2020. (in Chinese) |
| [2] |
MORAN E T, J r. Nutrients central to maintaining intestinal absorptive efficiency and barrier integrity with fowl[J]. Poultry Science, 2017, 96(5): 1348-1363. DOI:10.3382/ps/pew337 |
| [3] |
GORK A S, USUI N, CERIATI E, et al. The effect of mucin on bacterial translocation in Ⅰ-407 fetal and Caco-2 adult enterocyte cultured cell lines[J]. Pediatric Surgery International, 1999, 15(3/4): 155-159. |
| [4] |
BURRIN D G, STOLL B, JIANG R, et al. Minimal enteral nutrient requirements for intestinal growth in neonatal piglets: how much is enough?[J]. The American Journal of Clinical Nutrition, 2000, 71(6): 1603-1610. DOI:10.1093/ajcn/71.6.1603 |
| [5] |
GUAY F, DONOVAN S M, TROTTIER N L. Biochemical and morphological developments are partially impaired in intestinal mucosa from growing pigs fed reduced-protein diets supplemented with crystalline amino acids[J]. Journal of Animal Science, 2006, 84(7): 1749-1760. DOI:10.2527/jas.2005-558 |
| [6] |
KAEWTAPEE C, BURBACH K, TOMFORDE G, et al. Effect of Bacillus subtilis and Bacillus licheniformis supplementation in diets with low- and high-protein content on ileal crude protein and amino acid digestibility and intestinal microbiota composition of growing pigs[J]. Journal of Animal Science and Biotechnology, 2017, 8: 37. DOI:10.1186/s40104-017-0168-2 |
| [7] |
LUO Z, LI C B, CHENG Y F, et al. Effects of low dietary protein on the metabolites and microbial communities in the caecal digesta of piglets[J]. Archives of Animal Nutrition, 2015, 69(3): 212-226. DOI:10.1080/1745039X.2015.1034521 |
| [8] |
ZHOU L P, FANG L D, SUN Y, et al. Effects of the dietary protein level on the microbial composition and metabolomic profile in the hindgut of the pig[J]. Anaerobe, 2016, 38: 61-69. DOI:10.1016/j.anaerobe.2015.12.009 |
| [9] |
MCWHORTER T J, CAVIEDES-VIDAL E, KARASOV W H. The integration of digestion and osmoregulation in the avian gut[J]. Biological Reviews of the Cambridge Philosophical Society, 2009, 84(4): 533-565. DOI:10.1111/j.1469-185X.2009.00086.x |
| [10] |
WANG W W, QIAO S Y, LI D F. Amino acids and gut function[J]. Amino Acids, 2009, 37(1): 105-110. DOI:10.1007/s00726-008-0152-4 |
| [11] |
LAUDADIO V, PASSANTINO L, PERILLO A, et al. Productive performance and histological features of intestinal mucosa of broiler chickens fed different dietary protein levels[J]. Poultry Science, 2012, 91(1): 265-270. DOI:10.3382/ps.2011-01675 |
| [12] |
KESHAVARZ K, AUSTIC R E. The use of low-protein, low-phosphorus, amino acid- and phytase-supplemented diets on laying hen performance and nitrogen and phosphorus excretion[J]. Poultry Science, 2004, 83(1): 75-83. DOI:10.1093/ps/83.1.75 |
| [13] |
SHIM M Y, SONG E, BILLARD L, et al. Effects of balanced dietary protein levels on egg production and egg quality parameters of individual commercial layers[J]. Poultry Science, 2013, 92(10): 2687-2696. DOI:10.3382/ps.2012-02569 |
| [14] |
WANG H, WANG X J, ZHAO J P, et al. Low protein diet supplemented with crystalline amino acids suppressing appetite and apo-lipoprotein synthesis in laying hens[J]. Animal Feed Science and Technology, 2020, 266: 114533. DOI:10.1016/j.anifeedsci.2020.114533 |
| [15] |
PARENTEAU I A, STEVENSON M, KIARIE E G. Egg production and quality responses to increasing isoleucine supplementation in Shaver White hens fed a low crude protein corn-soybean meal diet fortified with synthetic amino acids between 20 and 46 weeks of age[J]. Poultry Science, 2020, 99(3): 1444-1453. DOI:10.1016/j.psj.2019.10.064 |
| [16] |
SUN M F, MA N, LIU H, et al. The optimal dietary arginine level of laying hens fed with low-protein diets[J]. Journal of Animal Science and Biotechnology, 2022, 13(1): 63. DOI:10.1186/s40104-022-00719-x |
| [17] |
凌晓波. 家禽肠道健康及其营养调控措施探讨[J]. 吉林畜牧兽医, 2019, 40(6): 30-31. LING X B. Intestinal health of poultry and its nutritional control measures[J]. Jilin Animal Husbandry and Veterinary Medicine, 2019, 40(6): 30-31 (in Chinese). DOI:10.3969/j.issn.1672-2078.2019.06.016 |
| [18] |
BAUMGART D C, DIGNASS A U. Intestinal barrier function[J]. Current Opinion in Clinical Nutrition and Metabolic Care, 2002, 5(6): 685-694. DOI:10.1097/00075197-200211000-00012 |
| [19] |
ARRIETA M C, BISTRITZ L, MEDDINGS J B. Alterations in intestinal permeability[J]. Gut, 2006, 55(10): 1512-1520. DOI:10.1136/gut.2005.085373 |
| [20] |
LIBONI K C, LI N, SCUMPIA P O, et al. Glutamine modulates LPS-induced IL-8 production through IκB/NF-κB in human fetal and adult intestinal epithelium[J]. The Journal of Nutrition, 2005, 135(2): 245-251. DOI:10.1093/jn/135.2.245 |
| [21] |
HAMPSON D J. Alterations in piglet small intestinal structure at weaning[J]. Research in Veterinary Science, 1986, 40(1): 32-40. DOI:10.1016/S0034-5288(18)30482-X |
| [22] |
EGE G, BOZKURT M, KOÇER B, et al. Influence of feed particle size and feed form on productive performance, egg quality, gastrointestinal tract traits, digestive enzymes, intestinal morphology, and nutrient digestibility of laying hens reared in enriched cages[J]. Poultry Science, 2019, 98(9): 3787-3801. DOI:10.3382/ps/pez082 |
| [23] |
张丽明. 低蛋白日粮调整氨基酸平衡对肉鸡氮代谢及肠道氨基酸转运载体相关基因表达的影响[D]. 硕士学位论文. 长春: 吉林大学, 2017. ZHANG L M. Effects of amino acid balance in low protein diets on nitrogen metabolism and intestinal amino acid transporter related genes expression in broilers[D]. Master's Thesis. Changchun: Jilin University, 2017. (in Chinese) |
| [24] |
ALLAMEH S, TOGHYANI M. Effect of dietary valine supplementation to low protein diets on performance, intestinal morphology and immune responses in broiler chickens[J]. Livestock Science, 2019, 229: 137-144. DOI:10.1016/j.livsci.2019.09.025 |
| [25] |
陶红旭, 隋炳毅, 龙烁, 等. 低蛋白日粮对蛋鸡生产性能和蛋品质的影响[J]. 中国家禽, 2014, 36(24): 38-42. TAO H X, SUI B Y, LONG S, et al. Effect of low-protein diet on production performance and egg quality of laying hens[J]. China Poultry, 2014, 36(24): 38-42 (in Chinese). DOI:10.3969/j.issn.1004-6364.2014.24.010 |
| [26] |
ZAEFARIAN F, ZAGHARI M, SHIVAZAD M. The threonine requirements and its effect on growth performance and gut morphology of broiler chicken fed different levels of protein[J]. International Journal of Poultry Science, 2008, 7(12): 1207-1215. DOI:10.3923/ijps.2008.1207.1215 |
| [27] |
蔡元丽. 影响肠道屏障功能的因素及营养调控措施[J]. 齐鲁工业大学学报, 2019, 33(1): 41-47. CAI Y L. Factors influencing on intestinal barrier function and nutrient modulation[J]. Journal of Shandong Institute of Light Industry (Natural Science Edition), 2019, 33(1): 41-47 (in Chinese). DOI:10.16442/j.cnki.qlgydxxb.2019.01.007 |
| [28] |
FURNESS J B, KUNZE W A, CLERC N. Nutrient tasting and signaling mechanisms in the gut.Ⅱ.The intestine as a sensory organ: neural, endocrine, and immune responses[J]. The American Journal of Physiology, 1999, 277(5): G922-G928. |
| [29] |
MAJKA G, WIECEK G, ŚRÓTTEK M, et al. The impact of lactoferrin with different levels of metal saturation on the intestinal epithelial barrier function and mucosal inflammation[J]. BioMetals, 2016, 29(6): 1019-1033. DOI:10.1007/s10534-016-9973-x |
| [30] |
CHOI E Y, HWANG H J, KIM I H, et al. Protective effects of a polysaccharide from Hizikia fusiformis against ethanol toxicity in rats[J]. Food and Chemical Toxicology, 2009, 47(1): 134-139. DOI:10.1016/j.fct.2008.10.026 |
| [31] |
SCHOULTZ I, KEITA Å V. Cellular and molecular therapeutic targets in inflammatory bowel disease-focusing on intestinal barrier function[J]. Cells, 2019, 8(2): 193. DOI:10.3390/cells8020193 |
| [32] |
SUZUKI T. Regulation of intestinal epithelial permeability by tight junctions[J]. Cellular and Molecular Life Sciences, 2013, 70(4): 631-659. DOI:10.1007/s00018-012-1070-x |
| [33] |
VICENTE Y, DA ROCHA C, YU J K, et al. Architecture and function of the gastroesophageal barrier in the piglet[J]. Digestive Diseases and Sciences, 2001, 46(9): 1899-1908. DOI:10.1023/A:1010631030320 |
| [34] |
TSUKITA S, FURUSE M, ITOH M. Multifunctional strands in tight junctions[J]. Nature Reviews: Molecular Cell Biology, 2001, 2(4): 285-293. DOI:10.1038/35067088 |
| [35] |
AZZAM M M M, DONG X Y, ZOU X T. Effect of dietary threonine on laying performance and intestinal immunity of laying hens fed low-crude-protein diets during the peak production period[J]. Journal of Animal Physiology and Animal Nutrition, 2017, 101(5): e55-e66. DOI:10.1111/jpn.12559 |
| [36] |
DONG X Y, AZZAM M M M, ZOU X T. Effects of dietary L-isoleucine on laying performance and immunomodulation of laying hens[J]. Poultry Science, 2016, 95(10): 2297-2305. DOI:10.3382/ps/pew163 |
| [37] |
徐子伟. 仔猪肠道损伤修复营养调控及其机制和应用[J]. 动物营养学报, 2014, 26(10): 3033-3045. XU Z W. Mechanism and application for nutritional regulations of intestine damage repair in piglets[J]. Chinese Journal of Animal Nutrition, 2014, 26(10): 3033-3045 (in Chinese). DOI:10.3969/j.issn.1006-267x.2014.10.015 |
| [38] |
陈渝, 陈代文, 毛湘冰, 等. 精氨酸对免疫应激仔猪肠道组织Toll样受体基因表达的影响[C]//第五届中国畜牧科技论坛论文集. 重庆: 中国畜牧兽医学会, 2011. CHEN Y, CHEN D W, MAO X B, et al. Effect of arginine supplementation on expression of Toll-like receptors genes of gut in weaned piglets during immune challenge[C]//Proceedings of the 5th China Animal Husbandry Science and Technology Forum. Chongqing: Chinese Association of Animal Science and Veterinary Medicine, 2011. (in Chinese) |
| [39] |
ZHOU J M, QIU K, WANG J, et al. Effect of dietary serine supplementation on performance, egg quality, serum indices, and ileal mucosal immunity in laying hens fed a low crude protein diet[J]. Poultry Science, 2021, 100(12): 101465. DOI:10.1016/j.psj.2021.101465 |
| [40] |
张日俊, 潘淑媛, 白永义, 等. 微生物饲料添加剂益生康对肉仔鸡营养代谢与免疫功能的调控机理[J]. 中国农业大学学报, 2005, 10(3): 40-47. ZHANG R J, PAN S Y, BAI Y Y, et al. Modulating mechanism of Yishengkang as feed additives on nutrient metabolism and immune function in broiler chickens[J]. Journal of China Agricultural University, 2005, 10(3): 40-47 (in Chinese). DOI:10.3321/j.issn:1007-4333.2005.03.009 |
| [41] |
孙小沛, 杨在宾, 李兆勇, 等. 地衣芽孢杆菌与日粮蛋白水平对肉鸡生产性能、肠道环境及免疫器官指数的影响[J]. 饲料工业, 2013, 34(23): 40-46. SUN X P, YANG Z B, LI Z Y, et al. Effects of Bacillus licheniformis and dietary protein levels on growth performance, intestinal health and immune organ indexes of broilers[J]. Feed Industry, 2013, 34(23): 40-46 (in Chinese). |
| [42] |
NATIVIDAD J M M, VERDU E F. Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications[J]. Pharmacological Research, 2013, 69(1): 42-51. DOI:10.1016/j.phrs.2012.10.007 |
| [43] |
HAYES C L, DONG J, GALIPEAU H J, et al. Commensal microbiota induces colonic barrier structure and functions that contribute to homeostasis[J]. Scientific Reports, 2018, 8(1): 14184. DOI:10.1038/s41598-018-32366-6 |
| [44] |
SONNENBURG J L, BÄCKHED F. Diet-microbiota interactions as moderators of human metabolism[J]. Nature, 2016, 535(7610): 56-64. DOI:10.1038/nature18846 |
| [45] |
FENG Q Q, CHEN W D, WANG Y D. Gut microbiota: an integral moderator in health and disease[J]. Frontiers in Microbiology, 2018, 9: 151. DOI:10.3389/fmicb.2018.00151 |
| [46] |
BRESTOFF J R, ARTIS D. Commensal bacteria at the interface of host metabolism and the immune system[J]. Nature Immunology, 2013, 14(7): 676-684. DOI:10.1038/ni.2640 |
| [47] |
DE CESARE A, FARIA DO VALLE Ì, SALA C, et al. Effect of a low protein diet on chicken ceca microbiome and productive performances[J]. Poultry Science, 2019, 98(9): 3963-3976. DOI:10.3382/ps/pez132 |
| [48] |
MA M, GENG S J, LIU M L, et al. Effects of different methionine levels in low protein diets on production performance, reproductive system, metabolism, and gut microbiota in laying hens[J]. Frontiers in Nutrion, 2021, 8: 739676. DOI:10.3389/fnut.2021.739676 |
| [49] |
DONG X Y, AZZAM M M M, ZOU X T. Effects of dietary threonine supplementation on intestinal barrier function and gut microbiota of laying hens[J]. Poultry Science, 2017, 96(10): 3654-3663. DOI:10.3382/ps/pex185 |
| [50] |
PRIOULT G, FLISS I, PECQUET S. Effect of probiotic bacteria on induction and maintenance of oral tolerance to β-lactoglobulin in gnotobiotic mice[J]. Clinical and Diagnostic Laboratory Immunology, 2003, 10(5): 787-792. |
| [51] |
BEAGLEY K W, HUSBAND A J. Intraepithelial lymphocytes: origins, distribution, and function[J]. Critical Reviews in Immunology, 1998, 18(3): 237-254. DOI:10.1615/CritRevImmunol.v18.i3.40 |
| [52] |
ZHOU J M, ZHANG H J, WU S G, et al. Supplemental xylooligosaccharide modulates intestinal mucosal barrier and cecal microbiota in laying hens fed oxidized fish oil[J]. Frontiers in Microbiology, 2021, 12: 635333. DOI:10.3389/fmicb.2021.635333 |
| [53] |
KUMAR D, RAGINSKI C, SCHWEAN-LARDNER L K, et al. Assessing the response of hen weight, body composition, feather score, egg quality, and level of excreta nitrogen content to digestible balanced proteinintake of laying hens[J]. Canadian Journal of Animal Science, 2018, 98(4): 619-630. DOI:10.1139/cjas-2017-0134 |
| [54] |
LI J M, ZHANG X Y, YUAN C, et al. Effects of dietary L-thronine levels on antioxidant capacity digestive enzyme on antioxdant capacity, digestive enzyme activities, and antibody production of Xinyang green shell laying hens[J]. Journal of Applied Poultry Research, 2016, 25(3): 422-427. DOI:10.3382/japr/pfw028 |
| [55] |
VAN DER SLUIS M, SCHAART M W, DE KONING B A E, et al. Threonine metabolism in the intestine of mice: loss of mucin 2 induces the threonine catabolic pathway[J]. Journal of Pediatric Gastroenterology and Nutrition, 2009, 49(1): 99-107. DOI:10.1097/MPG.0b013e3181a23dbe |
| [56] |
AZZAM M M M, DONG X Y, XIE P, et al. Influence of L-threonine supplementation on goblet cell numbers, histological structure and antioxidant enzyme activities of laying hens reared in a hot and humid climate[J]. British Poultry Science, 2012, 53(5): 640-645. DOI:10.1080/00071668.2012.726707 |