2. 陕西片仔癀麝业有限责任公司, 宝鸡 721000
2. Shanxi Pien Tze Huang Musk Deer Industry Limited Liability Corporations, Baoji 721000, China
植物单宁(vegetable tannin)又称植物多酚(plant polyphenol)，广泛存在于众多植物种群，尤其是在豆科植物和木本植物的嫩枝芽部位。植物单宁与植食动物的采食防御机制密切相关，是植物进化过程中衍生出来的一种自身保护性的次生代谢物质，是动植物协同进化的产物[1, 2, 3]。根据单宁的化学结构和性能将其分为2大类：水解单宁(hydrolysable tannins，HT)和缩合单宁(condensed tannins，CT)。后者是最常见的单宁类型。高含量的单宁不利于单胃动物和反刍动物的消化和生理，通常会降低草食动物采食量、消化率、身体发育和产毛量等。
研究表明，植物缩合单宁对草食动物的胃肠道寄生虫(gastrointestinal parasites，GIP)具有抑制作用[4, 5, 6]。究其原因，胃肠道寄生虫是制约草食家畜生长发育及生产性能的重要因素，感染胃肠道寄生虫会严重影响动物的营养吸收，导致腹泻、食欲低下、贫血、体重下降甚至死亡[7, 8, 9]。传统上，家畜饲养业采用化学驱虫剂控制寄生虫感染，获得了显著的成效。然而，源于连续使用驱虫剂造成的抗药性[10, 11, 12, 13, 14]及公众对食品中药物残留的关注等原因，已有研究者着手探索控制家畜寄生虫的替代方法[15, 16, 17]。植物缩合单宁广泛存在于植物界，是动物与植物相互作用的重要环节。而且大量研究表明，缩合单宁可通过直接或间接作用抑制胃肠道寄生虫数量并提高动物的生产性能[6, 18, 19, 20, 21]。由此可见，缩合单宁有望成为草食家畜寄生虫防控的新途径[19, 20, 21, 22, 23]及动植物协同进化的新切入点[20, 21]。
1 植物缩合单宁的结构及存在方式植物缩合单宁是碳-碳键连接起来的黄烷酮寡聚体和多聚体[3, 22]，通常由10~12个低聚物组成，且相对分子质量是2 000~4 000[22]，它是以黄烷-3醇类(焦儿茶酸)或黄烷-3，4二醇类(表儿茶酸)的低聚物存在。缩合单宁的不同组成产生了多种多样的化学结构，也形成了物理和生物化学特性上的差异。
缩合单宁广泛存在于双子叶植物的细胞壁或茎杆、树皮、花和种子的胞液中，热带和亚热带乔灌木含量最高，豆科植物(如红豆草、百脉根和小冠花)、油菜籽及高梁含量次之，小麦、白苜蓿和黄苜蓿等含量较低，鲜见于禾本科植物[21]。研究表明，不同植物和部位中缩合单宁的类型和含量均有很大的差异，且其含量随生长环境和阶段不同而改变[22, 23, 24, 25]。普遍认为豆科植物和木本植物所含缩合单宁显著高于其他植物种群[25, 26]。
2 植物缩合单宁的抗寄生虫性及其作用机制 2.1 植物缩合单宁的抗寄生虫性研究者采用植物缩合单宁或其粗提取物，通过体内或体外试验方法，对植物缩合单宁进行虫卵孵化测试(egg hatch assay，EHA)、幼虫摄食抑制试验(larval feeding inhibition assay，LFIA)、幼虫发育试验(larval development assay，LDA)、Ⅲ期幼虫迁移抑制试验(larval migration inhibition assay，LMIA)或者成虫活力抑制试验(adult motility inhibition assay，AMIA)，结果证实了缩合单宁具有抗寄生虫的功效[4, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43]。
在动物体内试验中，富含单宁的白坚木(Aspidosperma quebracho)树皮提取物可以有效抑制Ⅲ期幼虫在寄主体内的定居[30, 44]，降低线虫的繁殖力和虫卵产量[30, 31, 32, 33]。莲花(Lotus spp.)和红豆草(Onobrychis viciifolia)的缩合单宁提取物对牛体内的线虫有显著的抑制作用[45]。Kabasa等[46]研究表明，缩合单宁对山羊体内的寄生虫具有显著的抑制作用，且山羊可以选择适宜含量或者类型的缩合单宁减缓寄生虫压力。聚乙二醇(polyethylene glycol，PEG)能有效地结合单宁并抑制其生物活性。Makkar等[34]的研究表明，在富含单宁的食物中添加适当剂量PEG可抑制单宁结合瘤胃中的蛋白质，增加瘤胃中蛋白质的发酵并生成大量气体。有试验表明，山羊饲喂添加PEG的饲料导致其粪便内虫产卵量增加，机体生长发育减缓[46]，从而可见单宁有抗寄生虫的功效。现有大量体外研究证明，PEG可使植物提取物的抗寄生虫性失效[36, 39, 40]。
在动物体外试验中，将白坚木[35]、管状岩黄芪[36]、菊苣[37, 38]或者其他木本植物[39]的提取物添加到培养基中，被测试的寄生虫受到明显抑制且抑制效果具有剂量依赖性。从菊苣[37]、豆科植物[40]或者绿茶[41]中提炼的缩合单宁对Ⅲ期幼虫的迁移产生了抑制作用，且具有剂量依赖性。豆科植物中提取的缩合单宁能影响蛇形毛圆线虫卵孵化和幼虫发育[4]。桑寄生(Viscum verrucosum)、槲寄生(Tapinanthus oleifolius)和扁担杆属椴树科(Grewia flava)所含缩合单宁能抑制虫卵孵化、幼虫发育和幼虫迁移[6]。绿茶[41]和红豆草[43]的缩合单宁提取物能抑制幼虫迁移。以黄烷-3-醇和没食子酸形式存在的缩合单宁提取物能抑制体外培养的蛇形毛圆线虫的卵孵化，加大剂量则能够显著影响其幼虫发育和Ⅲ期幼虫迁移[47]。
2.2 植物缩合单宁的抗寄生虫作用机制动物的体内外试验已经充分证明缩合单宁的抗寄生虫性，迄今有关缩合单宁的抗寄生虫机制仍缺乏深入的了解。总结迄今的研究结果，我们将现有的植物缩合单宁的抗寄生虫机制归纳为2种假说。
其一为营养免疫假说，即缩合单宁能结合并保护蛋白质在反刍动物的瘤胃内不被降解，使蛋白质流向小肠，促进氨基酸的吸收[20, 48]，提高了动物机体获取营养物质的能力[49]，增强了感染寄生虫个体的抵抗力及免疫力。因此，适量摄食缩合单宁可提高营养物质的利用率并增强机体的抵抗力，被认为是缩合单宁的间接抗寄生虫作用。Tibe等[50]通过体内试验证明，扁担杆属椴树科和桑寄生科的缩合单宁提取物可以刺激幼年山羊血液中T细胞数量增加且能够提高其先天的免疫应答。然而，有关缩合单宁的营养免疫假说仍缺乏足够的试验证据，有限的试验结果仍具有不确定性[30, 51, 52, 53, 54]。
其二为代谢阻断假说，即缩合单宁能够影响寄生虫的许多重要生物学过程。该假说得到许多体外研究的支持，尤其是山羊和绵羊的短期体内试验[30, 33, 35]。缩合单宁可结合蛋白质并改变其理化性质，线虫的角质层富含脯氨酸和羟脯氨酸结构，这一结构覆盖了虫体、口腔、食道、泄殖腔和外阴[52]，缩合单宁与这些部位的蛋白质结合并损害其正常生理过程。通过扫描电子显微镜，研究者观察到寄生虫遇到缩合单宁后的表皮蛋白的损伤性变化[55]。这一试验结果可以解释，在寄主感染寄生虫的早期，植物单宁可以完全抑制或延迟了Ⅲ期幼虫的脱鞘，而加入PEG后这种作用就消失的试验现象[56]。在秀丽隐杆线虫中的试验表明，鞣花酸单宁能够明显损伤线虫的消化道和生殖道[57]。同时，缩合单宁可抑制蛋白酶活性，从而干预线虫的重要代谢途径中活性酶的分泌，影响线虫的生存[35]。
目前，缩合单宁抗寄生虫的作用机制仍然没有定论，其效果会因寄生虫种类、发育阶段、植物的生物化学特性等因素不同而有所差异[58]。
3 影响植物缩合单宁抗寄生虫性的因素土壤类型、气候、植物种类及其他的环境因素都会影响缩合单宁的生物合成途径[59]，从而影响其化学结构和含量[60]。缩合单宁的结构和含量是影响其抗寄生虫效果的2大主要因素[48, 61]。同时，寄生虫的种类和发育阶段及寄主胃肠道环境等因素也影响着缩合单宁的抗寄生虫性。
3.1 植物缩合单宁的含量有关绵羊、山羊[59]和鹿[19, 62]的研究表明，饲粮中植物缩合单宁的含量至少达到30~40 g/kg(干物质基础)才会表现出抗寄生虫活性。综合部分研究[18, 23, 31, 32, 35, 63, 64, 65, 66]的结果，与采食不含缩合单宁的饲粮相比，采食缩合单宁饲粮(45~55 g/kg干物质)的绵羊和山羊的粪便虫卵数(fecal egg count，FEC)减少了约50%；当饲粮缩合单宁含量增加到55g/kg(干物质基础)以上时，驱虫效果会有所加强；当饲粮缩合单宁含量降到30 g/kg(干物质基础)以下时，FEC变化不再明显。
在研究夜关门(Lespedeza cuneata)中所含缩合单宁对山羊FEC的作用时发现，与对照组相比，夜关门使山羊的FEC从168×104个/d降低至66×104个/d，下降幅度达61%[23, 63]。Min等[58]指出，FEC的减少通常与饲草缩合单宁含量相关，但采食过量的植物次生代谢物对寄主健康不利。Athanasiadou等[35]对绵羊饲喂含有16%白坚木的饲草，结果显示对食欲的负面影响超过了抗寄生虫性带来的正面影响。缩合单宁可改变绵羊的采食行为和蛋白质过瘤胃的比例，进而影响营养和生理反应。因此，适量摄入缩合单宁(3%~6%干物质)通常对寄主生理、生长、产毛量或者产奶量都有好处，而大量缩合单宁(7%~8%干物质) 则会抑制寄主取食，扰乱消化生理，降低消化率和生产能力[20, 48]。因此，必须综合考虑缩合单宁的利与弊[35]，一般认为，含5%缩合单宁的饲粮可减少感染性寄生虫对牧草的污染，并降低了驱虫剂的使用量。
3.2 植物缩合单宁的结构特性缩合单宁的化学结构是影响其生物活性的重要因素之一[60, 67]。缩合单宁是由碳-碳键连接起来的黄烷酮寡聚体和多聚体，相对分子质量较大，结构复杂。根据结构单元环上的取代基种类、数目及位置的不同，可将缩合单宁分为3大类。第1类是原花青素，以(表)儿茶素为基本结构单元；第2类是原翠雀定，以(表)掊儿茶素为基本结构单元；第3类是原天竺葵定，以(表)阿福豆素为基本结构单元[68]。黄烷-3-醇单体试验表明，原翠雀定和原花青素在缩合单宁中的比例会影响其抗寄生虫的效果。Molan等[42]的研究证实，原翠雀定较之原花青素对不同阶段的寄生虫的抑制效果更加明显。一些试验研究比较了多种富含单宁的豆科植物，证实原翠雀定所占比例高于原花青素的酚类植物对胃肠道寄生虫具有更好的寄生虫抑制效果[42, 43]。
3.3 寄生虫种类和发育阶段许多研究表明，植物所含的单宁对不同线虫的抑制效果存在显著的差异。以白坚木为缩合单宁来源饲喂已感染寄生虫的绵羊，观察到肠道内的线虫(巴斯特细颈线虫和蛇形毛圆线虫)繁殖力降低和数量减少，然而皱胃内的线虫(环纹背带线虫和捻转血矛线虫)却没有任何变化[31, 32, 35]。同样处理，单宁降低了山羊体内蛇形毛圆线虫的成虫和捻转血矛线虫的成虫繁殖力[30, 33]，但对环纹背带线虫没有影响[30]。进一步研究发现，与对照组相比较，山羊在感染Ⅲ期幼虫前摄入缩合单宁，其体内的捻转血矛线虫、环纹背带线虫和蛇形毛圆线虫分别减少33%、70%和66%[30, 33]。圈养条件下，马鹿皱胃中的艾氏毛圆线虫比环纹背带线虫对缩合单宁更敏感[69]。可见，寄生虫幼虫刚进入富含缩合单宁的消化道，缩合单宁的主要功效是抑制幼虫的定植，而对于已经定植的寄生虫，其主要的功效是抑制雌寄生虫产卵。因此，缩合单宁对寄生虫的抑制作用随寄生虫的发育阶段而不同[30, 33, 36, 39]。
3.4 寄主消化道环境缩合单宁参与了寄主的消化生理过程。缩合单宁-蛋白质结合是一个非常复杂的反应，受到缩合单宁特性(相对分子质量和组成)、蛋白质(相对分子质量和氨基酸组成)及各种酶的影响，尤其是在中性的瘤胃环境中形成的稳定的缩合单宁-蛋白质复合物在pH<3.5和pH>7.5时会分解[69]。动物的瘤胃、皱胃和小肠的环境完全不同，消化道的不同部位必然影响到植物单宁的存在形式及含量，由此对不同种类的寄生虫及其发育阶段产生不同的抑制效果。Robbins等[70]和Silanikove[71]研究了绵羊、鹿和山羊的消化道生理差异对植物缩合单宁的影响，证实了消化生理过程与植物缩合单宁的作用方式会最终影响到缩合单宁的抗寄生虫性。尽管已有一些研究，消化道不同部位与缩合单宁的抗寄生虫性之间的关系尚需要进一步的研究，以便深入揭示缩合单宁的作用机理。
4 小 结植物缩合单宁具有抗寄生虫的作用，其功效受到缩合单宁的化学结构和含量、寄生虫种类和发育阶段及寄主消化道环境的影响，其抗寄生虫机制可以归纳为营养免疫假说和代谢阻断假说，相关研究为动物肠胃道寄生虫防控提供了新的途径，植物缩合单宁有望成为传统化学驱虫剂的替代物质。从营养学角度来看，缩合单宁既具有负面营养作用又具有正面营养作用，关键在于添加水平或摄入水平。目前认为，适量摄入缩合单宁(3%~6%干物质)对寄主生理、生长、产毛量或者产奶量都有好处，且不会对寄主采食及生理生化造成不良影响。
植物缩合单宁既削弱了植食动物对植物的侵害，也抑制了植食动物的内寄生虫，因而可能广泛参与了植物与植食动物，植食动物与内寄生虫的协同进化。鉴于此，植物缩合单宁可能深刻影响了动物与植物的种间联系，进而参与了生物群落的塑造。因此，研究植物缩合单宁的抗寄生虫特性可能成为揭示生物群落的种间联系的切入点，并可能在家畜和野生动物的食源、牧场和栖息地管理上提供新的思路。
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