果胶对脂类和类胡萝卜素消化利用影响研究进展

刘 璇，刘嘉宁，毕金峰，周 沫，吕 健，彭 健



果胶对脂类和类胡萝卜素消化利用影响研究进展

刘 璇，刘嘉宁，毕金峰※，周 沫，吕 健，彭 健

（中国农业科学院农产品加工研究所，北京 100193）

果胶已经被证实可以影响脂类的消化，脂溶性的类胡萝卜素在消化阶段需要被脂滴包裹才能进入小肠形成胶束，因此果胶对类胡萝卜素的消化利用也会存在潜在影响。该文综述了近年来果胶对脂类和类胡萝卜素消化利用影响研究进展，主要分为果胶对消化液黏度的影响、对消化酶的影响、与钙离子的相互作用、与胆盐的结合作用以及对脂滴的包裹作用这5个方面。该文为后续分析如何提高果蔬中类胡萝卜素生物利用度提供理论依据。

凝胶；脂类；消化；果胶；类胡萝卜素；生物利用度

0 引 言

果胶是一类以D-半乳糖醛酸由-1,4糖苷键连接成的酸性杂多糖，多存在于果蔬细胞壁中[1]，不同果蔬中的果胶结构和功能特性有很大差异。果胶等膳食纤维已经被证实可以抑制脂类的消化吸收，从而减少食物中卡路里的摄入量[2]。类胡萝卜素是一种脂溶性天然色素，主要存在于黄色、橙色、红色的果蔬中[3]。由于类胡萝卜素的亲脂特性，在胃消化阶段需要被脂滴包裹才能进入小肠形成胶束[4]，因此果胶对类胡萝卜素的消化利用也会存在潜在影响。目前许多研究证实果胶对脂类消化的负面影响，并利用改性果胶研究果胶结构对脂类消化的影响，而关于果胶对类胡萝卜素消化吸收的潜在影响的研究尚处于初级阶段。另外，此类研究多采用含有类胡萝卜素的乳液体系，添加不同结构的外源果胶以探究果胶对类胡萝卜素消化吸收的影响，得出的结论与复杂的真实体系中可能并不相符，因此，果蔬真实体系中的内源果胶对类胡萝卜素生物利用度的影响还有待于验证。本文综述了近年来果胶对脂类和类胡萝卜素消化利用影响研究进展并展望了果蔬食品生物利用度相关研究的发展趋势，为后续分析如何提高果蔬中类胡萝卜素生物利用度提供理论依据。

1 果胶的结构与性质

1.1 果胶结构

果胶的主要构成物是D-半乳糖醛酸，世界粮农组织（Food and Agricultural Organization）和欧盟（European Union）规定果胶分子必须含有65%及以上的半乳糖醛酸[5]。果胶的一级结构通常包括以下3种类型：同型半乳糖醛酸聚糖（homogalacturonan，HG）、鼠李半乳糖醛酸聚糖I（rhamngalacturonan I，RG-I）和鼠李半乳糖醛酸聚糖II（rhamngalacturonan II，RG-II）[6]。图1为果胶基本结构，参考Willats等[5]稍作修改。

图1 果胶基本结构图

如图1，这3种多糖结构类型形成了果胶的结构，其中HG是果胶中含量最多的1种以-1,4糖苷键连接的线性半乳糖醛酸聚合体[7]。在HG中，半乳糖醛酸的C6羧基可被甲酯化，在某些情况下，C2和C6羧基也被乙酰化[6]。据报道，在甜菜根和马铃薯块茎中，有丰富的乙酰化HG结构[6,8]。RG-I是1种以鼠李半乳糖醛酸二糖为骨架的含有侧链的结构[9]。RG-I的结构具有多样化的特点，通常认为RG-I与HG区域以糖苷键连接[6]。一般情况下，RG-I中的20%～80%鼠李糖残基被中性和酸性低聚糖支链取代，取代位置为C4位，主要侧链结构包括线性和支链的结构的-L-阿拉伯聚糖和（或）-D-半乳聚糖残基[10]。RG-II是以HG为主链的含有支链的区域[6]，结构较复杂，由至少12种不同多糖以多于20种不同的键合方式连 接[7]。除此之外，HG中的半乳糖醛酸中C3可被木糖残基取代，形成1个新区域，这一区域通常被称为木糖半乳糖醛酸聚糖(xylogalacturonan，XG)[6]。

1.2 果胶性质

果胶的结构决定其性质，结构特点通常指分子量、甲酯化度、乙酰化度、中性糖组成等方面，许多植物性食物的质构特性和流变特性很大程度上依赖于果胶含量和结构[11]。每一种果胶分子都由上百个区域组成，因此具有很高的分子量[4]。果胶分子量是决定其在溶液中构象的关键因素，果胶能在油滴表面形成一层保护层和维持乳液的稳定性都与其分子量有关[12]。通常将水解后果胶分子中甲醇与无水半乳糖醛酸的摩尔数之比作为果胶甲酯化度[13]，果胶的甲酯化度常与果胶的凝胶特性﹑流体动力学特性和水合作用有关[14]。通常将水解后果胶分子中乙酸所占的摩尔百分比视为乙酰化度[15]，乙酰基的存在会增强果胶分子的疏水性，降低在水中的表面张力，从而在油水体系中，使果胶有潜力作为一种表面活性剂存在[16]。Siew等[17]的研究结果表明，在乳化过程中，含中性糖侧链丰富的果胶会优先吸附到油滴上。Funami等[18]采用酶解聚方法研究果胶中性糖侧链结构对其乳化性的影响，侧链降解酶在降低乳液稳定性方面的作用有效性证实了RG-I结构中的中性糖侧链可以提高乳液稳定性[12]。

2 脂类和类胡萝卜素的消化吸收

2.1 脂类的消化吸收

脂类的消化吸收过程如下：首先摄入到口腔的食物与唾液混合，通过咀嚼作用分解成小块食团。食团会快速地通过食道进入胃中，在胃中，它与含有消化酶的酸性消化液混合[19-22]。在这一过程中，食物中的脂肪转化为脂滴。胃脂肪酶与脂滴表面结合并将三酰基甘油水解为二酰基甘油﹑一酰基甘油和游离脂肪酸。通常来说，当10%～30%的脂肪酸从三酰基甘油中释放出来后，水解作用会停止[19]。在胃中被部分消化的食物常被称为食糜。随后，乳化的脂类随着食糜一起转移到十二指肠。由肝脏分泌的胆盐和磷脂是具有表面活性的物质，可以促进脂类的乳化。胰腺分泌的脂肪酶在小肠中使脂类水解。随后，脂类和脂类水解后的产物等（游离脂肪酸﹑一酰基甘油﹑胆固醇﹑磷脂和脂溶性维生素）形成混合胶束并随胶束一起转移到小肠粘膜上[19]。

2.2 类胡萝卜素的消化吸收

近年来，类胡萝卜素生物有效性（bioaccessibility）和生物利用度（bioavailability）逐渐成为国内外食品科学领域的研究重点。类胡萝卜素的生物利用度指可以被人体吸收、贮藏或利用的那部分类胡萝卜素。实现类胡萝卜素的生物利用的前提是类胡萝卜素在小肠中的生物有效性，即食物经胃肠道消化后释放出来的，且可被小肠吸收的那部分类胡萝卜素[23-24]。如图2所示，食物中的类胡萝卜素经过机械处理和（或）热处理等加工过程后初步释放，摄入人体后，在口腔中受到咀嚼作用或唾液作用进一步释放。由于类胡萝卜素的亲脂性，释放出的类胡萝卜素在胃中与脂相结合，并随着脂相一起被乳化成小脂滴。随后，类胡萝卜素从脂滴中转移出来，与胆盐﹑磷脂和脂类及其水解产物在小肠中一起转化为混合胶束，类胡萝卜素随混合胶束一起转移到小肠上皮细胞的刷状缘被上皮细胞吸收，包裹在乳糜颗粒中分泌到淋巴系统[25-26]。

注：：释放出的类胡萝卜素单体；：释放出的类胡萝卜素在胃中与脂相结合，并随着脂相一起被乳化成小脂滴； ：类胡萝卜素从脂滴中转移出来，与胆盐﹑磷脂和脂类及其水解产物在小肠中一起转化为混合胶束。

类胡萝卜素的生物利用度受到许多饮食和生理因素的影响。Castenmiller等[27]将所有可能的影响因素概括为“SLAMENGHI”，包括：类胡萝卜素种类（species of carotenoids）、分子间连接结构（molecular linkage）、饮食中摄入的类胡萝卜素的量（amount of carotenoids consumed in a meal）、类胡萝卜素所在的食物基质（matrix in which the carotenoid is incorporated）、吸收和生物转化的效应物（effectors of absorption and bioconversion）、主体的营养状况（nutrient status of the host）、遗传因素（genetic factors）、与主体相关的因素（host-related factors）、各因素间的相互作用（interactions）。类胡萝卜素所在食物基质种类﹑所处位置和存在状态的不同都会影响其从基质中的释放，进而影响生物利用率。在口腔阶段，咀嚼作用作为一种破碎方式，可以促进食物中类胡萝卜素的释放和与消化酶的作用，从而对脂类和类胡萝卜素的消化吸收有重要作用[28-29]。类胡萝卜素的消化吸收与脂类的消化吸收密切相关，因此脂类也是影响类胡萝卜素生物利用度的重要因素，不同脂类对类胡萝卜素生物利用度的影响也有差异[30]。对于果蔬类食品，其含有较多的膳食纤维，如果胶，被认为是导致水果和蔬菜中类胡萝卜素生物利用度低的因素。一方面，果胶是植物细胞壁的重要组成成分，而细胞壁的存在限制了类胡萝卜素从基质中的释放。另一方面，在消化过程中，果胶也会通过不同途径影响类胡萝卜素的生物利用度。因此，将果胶对类胡萝卜素生物利用度的影响途径进行分类梳理，可以为进一步研究如何提高果蔬中类胡萝卜素生物利用度提供理论基础。

3 果胶对脂类消化和类胡萝卜素生物利用度的 影响

3.1 果胶对消化液黏度的影响

黏度反映一种物质抵抗流动或运动的能力，果胶会增加胃中消化液的黏度，从而影响对食糜的剪切力作 用[19]，延长食物在胃和小肠阶段的消化时间并且降低基质与酶之间的运输效率[31]，改变运输过程[32-33]。果胶对消化液的黏度增加程度取决于许多因素，如结构和化学组成﹑浓度和分子量[34-35]，同时黏度对类胡萝卜素胶束化的影响也受到类胡萝卜素种类的限制。近几年，Yonekura等[36]研究表明-胡萝卜素和叶黄素的胶束化受到果胶的抑制，原因可能是高黏度的消化液引起的，但这一猜测未经证实。Xu等[37]发现在脂类消化过程中，向乳液中添加甜菜果胶会对游离脂肪酸的释放有影响，并将这一现象归因于果胶引起的黏度变化对脂肪酶的移动产生阻碍作用。Verrijssen等[38]的研究表明由果胶引起的胃肠道介质的黏度的增加会降低-胡萝卜素的胶束化程度，而且，介质的黏度取决于果胶的酯化度。果胶的存在和其酯化度的变化会改变胃肠液消化介质的黏度从而影响-胡萝卜素的胶束化[39]。Cervantes-paz等[40]证实高浓度果胶会增加胃肠消化介质的黏度和粒径，对类胡萝卜素的胶束化有阻碍作用。分子量高与分子量低的果胶相比，更有利于胃肠消化介质的黏度并促进极性较低的类胡萝卜素的胶束化。综上所述，果胶可以改变消化液黏度，从而对类胡萝卜素胶束化率产生负面影响。而在不同消化阶段，果胶引起消化液黏度变化的影响因素、黏度变化动力学及其对不同极性营养物质组分传递途径和机制是未来值得研究的一个方向。

3.2 果胶对消化酶的影响

在脂类消化过程中，果胶对胰脂酶存在竞争性抑制作用，在底物存在的情况下，脂肪酶优先与果胶形成复合物，从而抑制脂肪酶对底物的作用，因此限制油脂的消化分解及其混合胶束形成，进而限制混合胶束携带类胡萝卜素。Cudrey等[41]的研究结果表明，果胶与胰脂酶活性部位以共价键结合，并形成稳定复合物。果胶除了直接与脂肪酶结合抑制其活性外，果胶中的羧酸残基也可以使脂肪酶活性部位质子化，这也解释了低甲氧基的果胶对脂肪酶活性有较高的抑制作用[42]，上述现象的存在可能对脂类消化和类胡萝卜素生物有效性产生影响。果胶的分子量、凝胶性和酯化度是影响脂肪酶-果胶复 合物形成的因素[7,43]。Tsujita等[44]的研究结果表明，当果 胶的分子量较低时（90 kDa）对脂肪酶的抑制作用较 强。相反，Edashige等[45]的结果表明，高分子量的果胶（>300 kDa）对脂肪酶活力抑制作用较强，而较低分子量的果胶（<300 kDa）对脂肪酶活力抑制作用较弱。Verrijssen等[38]研究发现当果胶酯化度从99%和66%降为14%时，-胡萝卜素胶束化率显著降低，他们将这一现象归因于消化过程中凝胶状果胶聚集体对油滴的包裹作用，从而抑制了脂肪酶的活性。甲酯基通过中和负电荷[7]，增加果胶的疏水性，从而影响上述竞争性抑制过程。然而，由果胶引起的脂肪酶活力的抑制作用与类胡萝卜素的胶束化和生物有效性关联的研究内容少见报道。由此可见，果胶对脂类消化的影响与消化酶活力有关，但其作用机制尚未明确，特别是对果胶引起的脂肪酶活力的抑制作用类型及其是否直接作用于类胡萝卜素的胶束化过程值得进一步探讨。

3.3 果胶与钙离子的相互作用

许多果蔬和乳制品中含有丰富的钙，而果蔬中的内源果胶可以与钙离子结合，形成凝胶体系，从而对脂类和类胡萝卜素的消化过程起到负面作用[46]。果胶与钙离子相互作用对脂类消化影响与消化液酸碱度和果胶结构特性密切相关。消化过程中，介质的pH值会显著影响果胶与钙离子的结合能力，离子交换能力在接近中性的小肠中比在pH值较低的胃中高[42]，在小肠消化阶段，果胶对脂类消化的抑制作用更强。Hu等[47]研究结果表明：钙离子对乳液中脂类的消化速率有很大影响，果胶-钙复合物可通过脂质絮凝和微凝胶的形成来减小脂滴表面积，影响脂肪酶的作用面积从而降低脂类的消化吸收。果胶中羧基为主要参与形成凝胶的基团，果胶比琼脂和卡拉胶更易与二价阳离子结合[48]。低酯化度的果胶含有较多羧基，与高酯化度果胶相比，更易与金属离子结合[42]，因此可推测低酯化度的果胶对脂类消化的阻碍作用较明显。果胶与钙复合物的形成，抑制了脂类的消化吸收，从而可能会限制类胡萝卜素从脂滴转移到胶束这一过程，也可能通过影响脂类消化产物构成，从而影响胶束的形成，最终对类胡萝卜素的消化吸收产生影响。Verrijssen等[38]研究表明，-胡萝卜素的胶束化程度随着果胶酯化度的降低而减小，其原因是凝胶状果胶油滴的包裹作用抑制了脂肪酶的活性，凝胶结构可能是由于果胶与胃和小肠消化液中的钙离子结合形成的。

果胶与钙离子除了通过形成凝胶体系影响类胡萝卜素消化外，果胶还可能通过影响钙离子与脂类消化产物之间的交互作用降低脂类和类胡萝卜素的消化吸收。钙离子可以使游离脂肪酸从油滴表面沉淀下来，以不溶性钙盐状态存在，这一过程可以避免游离脂肪酸聚集在表面，为脂肪酶与乳化脂滴中甘油三酯的接触提供更多机会[49-50]，研究已经证实为保证脂类消化过程顺利进行，游离脂肪酸必须从脂滴表面及时清除[49,51]。当果胶存在时，阻碍钙离子对脂肪酸的清除作用，从而使游离脂肪酸聚集在脂滴表面，阻碍脂滴的吸收[4]，因此在脂滴中的类胡萝卜素消化可能也会降低。Corte-real等[52]研究表明钙离子的浓度和类胡萝卜素的类型影响类胡萝卜素的胶束化程度，随着钙离子浓度增强，类胡萝卜素胶束化程度降低，当钙离子浓度达到500 mg/L时，胶束化程度几乎降为0。在5种代表不同类胡萝卜素存在状态的食物体系中，钙离子的存在使所有体系中类胡萝卜素的生物利用度均降低[53]。许多研究都证实钙离子对脂类消化和类胡萝卜素胶束化的抑制作用，而钙离子和不同性质果胶的结合作用对类胡萝卜素吸收的影响效果还没有定论，仍需进一步明确。

3.4 果胶与胆盐的结合作用

胆盐是由肝细胞分泌的胆汁酸与甘氨酸或牛磺酸结合而形成的钠盐或钾盐。胆盐的分子结构不同于一般的表面活性剂，它的结构较简单，羟基和甲基各在一侧。在消化过程中，胆盐的2种特性对脂类和类胡萝卜素消化过程中起到重要的作用，首先胆盐具有表面活性，对非水相有较强亲和力。另一方面，胆盐本身也参与胶束的形成，对脂类和类胡萝卜素的溶解和转移到小肠粘膜起到决定性作用[54]。在脂类消化过程中，分泌到十二指肠的胆盐聚集在脂滴表面，有利于脂滴的乳化并减小脂滴体积，最终增加与脂肪酶的有效接触面积[55]。许多研究证明了胆盐在消化过程的重要性，采用体外模拟消化实验时，如果消化过程中不添加胆盐，-胡萝卜素的胶束化率会有很大程度地减小[56-57]。通常来说，胆盐可以在回肠中被再次吸收，然后通过肝肠循环运送到肝脏，而当有果胶存在时，胆盐的再吸收作用减弱，胶束的形成和脂类的乳化作用被限制[4]。因此，果胶与胆盐的结合会影响脂类和类胡萝卜素的吸收。胆盐与果胶的结合能力与胆盐和果胶结构中的羟基有关[4]。果胶浓度越高，与胆盐的结合能力越弱，原因可能是浓度较高时，果胶链的相互作用增强，从而影响果胶与其他物质（如胆盐）的相互作用[40]。果胶与胆盐的结合作用已经被证实可以影响类胡萝卜素的胶束化率，而果胶分子结构类型和侧链特征基团与胆盐的结合作用机理及其对脂类和非极性物质消化、吸收的影响，是未来值得研究的内容。

3.5 果胶对脂滴的包裹作用

果胶对脂滴的包裹作用会直接影响脂类的消化吸收，而其对类胡萝卜素消化吸收和生物利用度的直接影响尚未见报道。在脂类消化过程中，脂滴的中心主要由疏水性较强的二酰基甘油和三酰基甘油组成，极性相对较高的磷脂、游离脂肪酸、胆固醇和胆盐聚集在脂滴表面[4]。带负电的果胶由于表面活性和静电吸引力包裹在脂滴表面形成一层保护膜，阻止脂肪酶与脂滴的接触[31]。果胶结构决定上述保护膜的形成，由于果胶具有表面活性，特别是结构中存在乙酰基时，果胶吸附在油滴周围，形成一层保护膜，通过阻断油滴之间的静电吸引作用来防止油滴的聚集反应[4]。乳状液体系常见与食品体系，而在有果胶存在的乳液体系中，果胶对油滴的包裹作用存在以下3种情况（图3）：1）如果果胶不吸附在油滴表面，由于空缺絮凝作用（depletion flocculation）脂滴会聚集（图3a），聚集现象会降低脂滴有效表面积，从而对脂类的消化起到负面作用。2）当包裹在油滴表面的果胶形成一层较厚的稳定的保护膜时（图3b），接近的脂滴会相互排斥，一方面提高乳液的稳定性，但同时也会阻碍脂类与脂肪酶的接触而影响消化效率。3）当果胶在脂滴周围形成不完整的保护层时（图3c），由于架桥絮凝（bridging flocculation）作用，脂滴可能会产生聚集现象[42]。果胶保护层的形成与果胶结构有关[58]。果胶结构中RG-I区域决定其空间稳定性，HG区域决定其静电稳定性。RG-I区域中的中性糖侧链决定吸收的果胶链分子间相互作用，这一作用形成较厚的吸附层，防止脂滴聚集[18,59]。Zhao等[60]的结果表明，乳液中含有带负电的甜菜果胶时，有很高的稳定性，原因是多糖的高电荷密度促进了被包裹的脂滴之间的静电排斥作用。以上3种果胶存在状态会对脂类及类胡萝卜素消化吸收和乳液稳定体系产生不同影响，而如何通过加工技术、加工单元操作调控果胶结构形成，使其对类胡萝卜素从原料释放、到稳态结构形成、消化过程传递、以及吸收利用实现靶向、高效调控，需要开展系统研究。

注：图3a：果胶不吸附在脂滴表面，与脂滴存在空隙，由于空缺絮凝作用，脂滴会聚集。图3b：包裹在油滴表面的果胶形成一层较厚的稳定的保护膜时，接近的脂滴会相互排斥。图3c：当果胶在脂滴周围形成不完整的保护层时，由于架桥絮凝作用，脂滴可能会产生聚集现象。

表1 果胶对脂类消化和类胡萝卜素生物有效性和生物利用度的影响

4 结论与展望

本文综述了近几年来果胶对脂类消化和类胡萝卜素生物有效性和生物利用度的影响。总的来说，果胶主要通过以下5种方式影响脂类和类胡萝卜素的消化：改变消化液黏度，影响物质移动和运输效率；与消化酶结合，影响消化酶活力；与钙离子结合，形成凝胶体系或使游离脂肪酸聚集在脂滴表面，影响脂类的吸收；与胆盐结合，阻碍胆盐在消化中的作用；包裹在脂滴表面形成一层保护膜，阻止脂肪酶与脂滴的接触。果胶对脂类和类胡萝卜素消化途径和效果的影响主要取决于果胶浓度、分子量和酯化度。

目前，大多数研究采用含有类胡萝卜素的乳液体系，添加外源果胶以探究果胶对类胡萝卜素消化吸收的影响，得出的结论与复杂的真实体系中可能并不相符，因此，果蔬真实体系中的内源果胶对类胡萝卜素生物利用度的影响还需要进一步验证。另外，果胶对脂类和类胡萝卜素的消化吸收的影响也是多方面的，果胶可能通过以上5个方式抑制脂类和类胡萝卜素的消化吸收，也可能由于乳化作用，在加工处理过程中，对类胡萝卜素起到乳化包埋、稳态的作用，提升其在加工、消化传递过程中的稳定性。因此，果胶对类胡萝卜素从原料释放、加工处理、消化和吸收全过程的影响尚未形成定论。对于果蔬原料来说，加工处理方式是决定其物化性质的关键因素，采用一些均细化处理（胶体磨和高压均质）或者热加工处理等可以提高类胡萝卜素从原料中的释放率和部分原料中类胡萝卜素的生物利用度，是否这些均细化处理方式也可以改善果蔬中果胶的结构特性从而使其对类胡萝卜素的生物利用度起到正面作用是未来值得研究的一个方面。

[1] Pérez S, Mazeau K, Penhoat C H D. The three-dimensional structures of the pectic polysaccharides[J]. Plant Physiology & Biochemistry, 2000, 38(1-2): 37－55.

[2] Beysseriat M, Decker E A, Mcclements D J. Preliminary study of the influence of dietary fiber on the properties of oil-in-water emulsions passing through an in vitro human digestion model[J]. Food Hydrocolloids, 2006, 20(6): 800－809.

[3] Cervantes-Paz B, Victoria-Campos C I, Ornelas-Paz J J. Absorption of carotenoids and mechanisms involved in their health-related properties[J]. Subcell Biochem, 2016, 79: 415－454.

[4] Cervantespaz B, Ornelaspaz J J, Ruizcruz S, et al. Effects of pectin on lipid digestion and possible implications for carotenoid bioavailability during pre-absorptive stages: A review[J]. Food Research International, 2017. http://dx.doi. org/10.1016/j.foodres.2017.02.012.

[5] Willats W G T, Knox J P, Mikkelsen J D. Pectin: New insights into an old polymer are starting to gel[J]. Trends in Food Science & Technology, 2006, 17(3): 97－104.

[6] Willats W G T, Mccartney L, Mackie W, et al. Pectin: Cell biology and prospects for functional analysis[J]. Plant Molecular Biology, 2001, 47(1/2): 9－27.

[7] Mohnen D. Pectin structure and biosynthesis.[J]. Current Opinion in Plant Biology, 2008, 11(3): 266－277.

[8] Pauly M, Scheller H V. O-Acetylation of plant cell wall polysaccharides: Identification and partial characterization of a rhamnogalacturonan O-acetyl-transferase from potato suspension-cultured cells[J]. Planta, 2000, 210(4): 659－667.

[9] Voragen A G J, Coenen G J, Verhoef R P, et al. Pectin, a versatile polysaccharide present in plant cell walls[J]. Structural Chemistry, 2009, 20(2): 263－275.

[10] Ridley B L, O'Neill M A, Mohnen D. Pectins: Structure, biosynthesis, and oligogalacturonide-related signaling[J]. Phytochemistry, 2001, 57(6): 929－932.

[11] Sila D N, Buggenhout S V, Duvetter T, et al. Pectins in processed fruit and vegetables: Part II - structure-function relationships[J]. Comprehensive Reviews in Food Science & Food Safety, 2009, 8(2): 86－104.

[12] Ngouémazong E D, Christiaens S, Shpigelman A, et al. The emulsifying and emulsion-stabilizing properties of pectin: A review[J]. Comprehensive Reviews in Food Science & Food Safety, 2015, 14(6): 705－718.

[13] Sila D N, Smout C, Elliot F, et al. Non-enzymatic depolymerization of carrot pectin: Toward a better understanding of carrot texture during thermal processing[J]. Journal of Food Science, 2006, 71(1): 1－9.

[14] Ngouémazong D E, Tengweh F F, Duvetter T, et al. Quantifying structural characteristics of partially de-esterified pectins[J]. Food Hydrocolloids, 2011, 25(3): 434－443.

[15] Wang W, Ma X, Jiang P, et al. Characterization of pectin from grapefruit peel: A comparison of ultrasound-assisted and conventional heating extractions[J]. Food Hydrocolloids, 2016, 61: 730－739.

[16] Rubio-Senent F, Rodríguez-Gutiérrez G, Lama-Muñoz A, et al. Pectin extracted from thermally treated olive oil by-products: Characterization, physico-chemical properties, invitro, bile acid andglucose binding[J]. Food Hydrocolloids, 2015, 43: 311－321.

[17] Siew C K, Williams P A. Role of protein and ferulic acid in the emulsification properties of sugar beet pectin[J]. Journal of Agricultural & Food Chemistry, 2008, 56(11): 4164－4171.

[18] Funami T, Nakauma M, Ishihara S, et al. Structural modifications of sugar beet pectin and the relationship of structure to functionality[J]. Food Hydrocolloids, 2011, 25(2): 221－229.

[19] Beysseriat M, Decker E A, Mcclements D J. Preliminary study of the influence of dietary fiber on the properties of oil-in-water emulsions passing through an in vitro human digestion model[J]. Food Hydrocolloids, 2006, 20(6): 800－809.

[20] Armand M, Pasquier B, André M, et al. Digestion and absorption of fat emulsions with different droplet sizes in the human digestive tract[J]. American Journal of Clinical Nutrition, 1999, 70(6): 1096－1106.

[21] Hu M, Li Y, Decker E A, et al. Role of calcium and calcium-binding agents on the lipase digestibility of emulsified lipids using an in vitro digestion model[J]. Food Hydrocolloids, 2010, 24(8): 719－725.

[22] Mcclements D J, Decker E A, Park Y. Controlling lipid bioavailability through physicochemical and structural approaches.[J]. Critical Reviews in Food Science & Nutrition, 2009, 49(1): 48－67.

[23] Knockaert G, Lemmens L, Buggenhout S V, et al. Changes in-carotene bioaccessibility and concentration during processing of carrot puree[J]. Food Chemistry, 2012, 133(1): 60－67.

[24] Lemmens L, Colle I, Buggenhout S V, et al. Carotenoid bioaccessibility in fruit- and vegetable-based food products as affected by product (micro) structural characteristics and the presence of lipids: A review[J]. Trends in Food Science & Technology, 2014, 38(2): 125－135.

[25] Yonekura L, Nagao A. Intestinal absorption of dietary carotenoids[J]. Molecular Nutrition & Food Research, 2007, 51(1): 107－115.

[26] 雷菲，高彦祥，侯占群. 体外消化过程中影响类胡萝卜素生物利用率的因素[J]. 食品科学，2012，33(21)：368－373. Lei Fei, Gao Yanxiang, Hou Zhanqun. Factors that influence the bioavailability of carotenoids in in vitro digestion[J]. Food Science, 2012, 33(21): 368－373. (in Chinese with English abstract)

[27] Castrnmiller J J M, West C E. Bioavailability and bioconversion of carotenoids[J]. Annual Review of Nutrition, 1998, 18: 19－38.

[28] Low D Y, D'Arcy B, Gidley M J. Mastication effects on carotenoid bioaccessibility from mango fruit tissue[J]. Food Research International, 2015, 67: 238－246.

[29] Guerra A, Etiennemesmin L, Livrelli V, et al. Relevance and challenges in modeling human gastric and small intestinal digestion[J]. Trends in Biotechnology, 2012, 30(11): 591－600.

[30] Nidhi B, Baskaran V. Influence of vegetable oils on micellization of lutein in a simulated digestion model[J]. Journal of the American Oil Chemists Society, 2011, 88(3): 367－372.

[31] Verrijssen T A J, Verkempinck S H E, Christiaens S, et al. The effect of pectin on in vitro,-carotene bioaccessibility and lipid digestion in low fat emulsions[J]. Food Hydrocolloids, 2015, 49: 73－81.

[32] Kristensen M, Jensen M G. Dietary fibres in the regulation of appetite and food intake. Importance of viscosity.[J]. Appetite, 2011, 56(1): 65－70.

[33] Fabek H, Messerschmidt S, Brulport V, et al. The effect of in vitro digestive processes on the viscosity of dietary fibres and their influence on glucose diffusion[J]. Food Hydrocolloids, 2014, 35(3): 718－726.

[34] Cheryl L. Dikeman, George C, Fahey Jr. Viscosity as related to dietary fiber: A review[J]. Critical Reviews in Food Science & Nutrition, 2006, 46(8): 649－663.

[35] Dikeman C L, Murphy M R, Jr F G. Dietary fibers affect viscosity of solutions and simulated human gastric and small intestinal digesta[J]. Journal of Nutrition, 2006, 136(4): 913－919.

[36] Yonekura L, Nagao A. Soluble fibers inhibit carotenoid micellization in vitro and uptake by Caco-2 cells[J]. Bioscience Biotechnology & Biochemistry, 2009, 73(1): 196－199.

[37] Xu D, Yuan F, Gao Y, et al. Influence of whey protein-beet pectin conjugate on the properties and digestibility of-carotene emulsion during in vitro digestion[J]. Food Chemistry, 2014, 156(156): 374－379.

[38] Verrijssen T A J, Balduyck L G, Christiaens S, et al. The effect of pectin concentration and degree of methyl- esterification on the in vitro, bioaccessibility of-carotene- enriched emulsions[J]. Food Research International, 2014, 57: 71－78.

[39] Verrijssen T A J, Verkempinck S H E, Christiaens S, et al. The effect of pectin on invitro,-carotene bioaccessibility and lipid digestion in low fat emulsions[J]. Food Hydrocolloids, 2015, 49: 73－81.

[40] Cervantes-Paz B, Ornelas-Paz J D J, Pérez-Martínez J D, et al. Effect of pectin concentration and properties on digestive events involved on micellarization of free and esterified carotenoids[J]. Food Hydrocolloids, 2016, 60: 580－588.

[41] Cudrey C, Van T H, Gargouri Y, et al. Inactivation of pancreatic lipases by amphiphilic reagents 5-(dodecyldithio)- 2-nitrobenzoic acid and tetrahydrolipstatin. Dependence upon partitioning between micellar and oil phases.[J]. Biochemistry, 1993, 32(50): 13800－13808.

[42] Capuano E. The behaviour of dietary fibre in the gastrointestinal tract determines its physiological effect[J]. Critical Reviews in Food Science & Nutrition, 2016, 57(16): 3543－3564.

[43] Kumar A, Chauhan G S. Extraction and characterization of pectin from apple pomace and its evaluation as lipase (steapsin) inhibitor[J]. Carbohydrate Polymers, 2010, 82(2): 454－459.

[44] Tsujita T, Sumiyosh M, Han L K, et al. Inhibition of lipase activities by citrus pectin.[J]. Journal of Nutritional Science & Vitaminology, 2003, 49(5): 340－345.

[45] Edashige Y, Murakami N, Tsujita T. Inhibitory effect of pectin from the segment membrane of citrus fruits on lipase activity[J]. Journal of Nutritional Science & Vitaminology, 2008, 54(5): 409－415.

[46] Braccini. I, Pérez S. Molecular basis of Ca2+-induced gelation in alginates and pectins:  The egg-box model revisited[J]. Biomacromolecules, 2001, 2(4): 1089－1096.

[47] Hu M, Li Y, Decker E A, et al. Role of calcium and calcium-binding agents on the lipase digestibility of emulsified lipids using an in vitro digestion model[J]. Food Hydrocolloids, 2010, 24(8): 719－725

[48] Debon S J J, Tester R F. In vitro binding of calcium, iron and zinc by non-starch polysaccharides[J]. Food Chemistry, 2001, 73(4): 401－410

[49] Devraj R, Williams H D, Warren D B, et al. In vitro digestion testing of lipid-based delivery systems: Calcium ions combine with fatty acids liberated from triglyceride rich lipid solutions to form soaps and reduce the solubilization capacity of colloidal digestion products[J]. International Journal of Pharmaceutics, 2013, 441(1-2): 323－333.

[50] Zangenberg N H, MuLlertz A, Kristensen H G, et al. A dynamic in vitro lipolysis model I. controlling the rate of lipolysis by continuous addition of calcium[J]. European Journal of Pharmaceutical Sciences, 2001, 14(2): 115－122.

[51] Wieloch T, Borgström B, Piéroni G, et al. Product activation of pancreatic lipase[J]. Journal of Biological Chemistry, 1982, 257(19): 11523－11528.

[52] Cortereal J, Iddir M, Soukoulis C, et al. Effect of divalent minerals on the bioaccessibility of pure carotenoids and on physical properties of gastro-intestinal fluids[J]. Food Chemistry, 2016, 197(Pt A): 546－553.

[53] Cortereal J, Bertucci M, Soukoulis C, et al. Negative effects of divalent mineral cations on the bioaccessibility of carotenoids from plant food matrices and related physical properties of gastro-intestinal fluids.[J]. Food & Function, 2017, 8(3): 1008－1019.

[54] Maldonadovalderrama J, Wilde P, Macierzanka A, et al. The role of bile salts in digestion[J]. Advances in Colloid & Interface Science, 2011, 165(1): 36－46.

[55] Moghimipour E, Ameri A, Handali S. Absorption-enhancing effects of bile salts[J]. Molecules, 2015, 20(8): 14451.

[56] Diaz V. Estimation of carotenoid accessibility from carrots determined by an in vitro digestion method[J]. European Journal of Clinical Nutrition, 2002, 56(5): 425–430.

[57] Wright A J, Pietrangelo C, Macnaughton A. Influence of simulated upper intestinal parameters on the efficiency of beta carotene micellarisation using an in vitro model of digestion[J]. Food Chemistry, 2008, 107(3): 1253－1260.

[58] Leroux, J, Langendorff, V, Schick, G, et al. Emulsion stabilizing properties of pectin[J]. Food Hydrocolloids, 2003, 17: 455－462.

[59] Funami T, Zhang G Y, Hiroe M, et al. Effects of the proteinaceous moiety on the emulsifying properties of sugar beet pectin[J]. Food Hydrocolloids, 2007, 21(8): 1319－1329.

[60] Zhao J, Wei T, Wei Z, et al. Influence of soybean soluble polysaccharides and beet pectin on the physicochemical properties of lactoferrin-coated orange oil emulsion[J]. Food Hydrocolloids, 2015, 44: 443－452.

[61] Espinal-Ruiz M, Restrepo-Sánchez L P, Narváez-Cuenca C E, et al. Impact of pectin properties on lipid digestion under simulated gastrointestinal conditions: Comparison of citrus and banana passion fruit (Passiflora tripartita, var. mollissima) pectins[J]. Food Hydrocolloids, 2016, 52: 329－342.

[62] Verrijssen T A J, Christiaens S, Verkempinck S H E, et al. In vitro-carotene bioaccessibility and lipid digestion in emulsions: Influence of pectin type and degree of methyl‐esterification[J]. Journal of Food Science, 2016, 81(10): 2327－2336.

[63] Espinalruiz M, Paradaalfonso F, Restreposánchez L P, et al. Impact of dietary fibers [methyl cellulose, chitosan, and pectin] on digestion of lipids under simulated gastrointestinal conditions[J]. Food & Function, 2014, 5(12): 3083－3095.

[64] Lemmens L, Buggenhout S V, Oey I, et al. Towards a better understanding of the relationship between the-Carotene in vitro bio-accessibility and pectin structural changes: A case study on carrots[J]. Food Research International, 2009, 42(9): 1323－1330.

[65] Ornelaspaz J D J, Failla M L, Yahia E M, et al. Impact of the stage of ripening and dietary fat on in vitro bioaccessibility of-carotene in ‘Ataulfo’ mango[J]. Journal of Agricultural & Food Chemistry, 2008, 56(4): 1511－1516.

Review on effects of pectin on digestion of lipid and carotenoids

Liu Xuan, Liu Jianing, Bi Jinfeng※, Zhou Mo, Lü Jian, Peng Jian

(100193,)

Pectin is a family of galacturonic acid-rich polysaccharides, which mostly exists in plant cell walls. Pectin structure determines its properties, and the structure characteristics usually refer to the molecular weight, degree of methoxylation and acetylation, galacturonic acid content, neutral sugar composition. The texture and rheological properties of raw fruit and vegetable and their products are dependent on the structure of pectin. Carotenoids are lipophilic pigments responsible for the yellow, orange, and red colors of many fruits and vegetables, which have beneficial health effects. Carotenoid bioavailability is usually considered as the fraction of the ingested carotenoids that are accessible for utilization in normal physiological functions or for storage in the human body. A prerequisite for carotenoid bioavailability is its bioaccessibility in the small intestine. Carotenoid bioaccessibility is defined as the amount of carotenoids that are released from its food matrix during digestion and made available for absorption into intestinal mucosa. A number of studies suggested that certain types of dietary fiber such as pectin could inhibit the digestion and absorption of lipids. Therefore, pectin has a potential impact on the digestion and absorption of carotenoids, since carotenoids might be encapsulated in lipid droplet in stomach phase. The present review summarized recent studies about the effects of pectin on lipid digestion and carotenoid bioavailability in order to provide theoretical basis for further improving the bioavailability of carotenoids in fruit and vegetable-based food products. Additionally, future research challenges in this review are identified. Structure and properties of pectin were summarized at first, and the specific processes of lipid digestion and carotenoid absorption were also elucidated. On one hand, pectin is an important component of plant cell wall, and the presence of cell wall restricts the release of carotenoids from the matrix. On the other hand, pectin may interfere with the the processes of lipid digestion and carotenoid absorption in a variety of different ways, and these could be summarized as 5 aspects. 1) Pectin could change the viscosity of the digestive juice, which would alter the magnitude of the shear forces operating on the chyme, increase the duration in the stomach and small intestinal phase and decrease the transport efficiency. 2) Pectin could act as a physical barrier between substrates and digestive enzymes. Pectin could compete with the substrate for the active site of the enzyme, protonate the enzyme active site through the participation of the carboxylic acid residues and generate direct molecular interactions between pectin and enzymes. 3) Galacturonic and galuronic acid residues of pectin could form gels with calcium ions. These pectin-calcium complexes reduce lipid digestion by reducing the surface area of the lipid droplets where lipase exerts its activity as a consequence of lipid flocculation or microgel formation. Besides gel formation, the binding between calcium ions and pectin might also affect carotenoid absorption in another way. The levels of free calcium in the gastrointestinal medium can be reduced in the presence of pectin, causing accumulation of free fatty acids on the lipid droplet surfaces and reducing lipid droplet digestion. 4) Pectin may bind bile salts in the small intestine, and affect the lipid digestion and the efficiency of carotenoid incorporation into mixed micelles. 5) Pectin may be adsorbed to the surfaces of the emulsified lipids and form a protective coating, which may prevent the lipase from being adsorbed to the droplet surfaces and getting access to the lipids inside the droplets. The effects of pectin on the digestive pathways and digestive efficiency of lipid and carotenoids depend on pectin structure, especially molecular mass, degree of methylesterification and acetylation, and neutral sugars composition. At present, most studies used emulsion system containing carotenoids, and added exogenous pectin to explore the influence of pectin on digestion and absorption of carotenoids. Thus, the results they found in the simulation system might be different in fruit and vegetable-based food products, and the effect of endogenous pectin on the bioavailability of carotenoids in the fruits and vegetables needs further verification. In addition, the effect of pectin on the absorption of lipid and carotenoids is also manifold. Pectin may inhibit digestion and absorption of lipid and carotenoids through the above 5 ways and also form a coating around the carotenoids and thus increase the stability of carotenoids during the processing, storage and further digestion. For fruit and vegetable materials, processing method is the important factor to determine its physicochemical properties, and some crushing and refining treatments, such as colloid mill and high pressure homogenization, can improve the release rate and pathway of carotenoids from the raw materials. Thus, it is worthy to be studied whether these crushing and refining treatments can improve the structural characteristics of pectin and make it play a positive role in carotenoid bioavailability.

gel; lipid; digestion; pectin; carotenoids; bioavailability

2017-12-12

2018-03-05

国家自然科学基金项目资助（31671868）

刘 璇，博士，副研究员，研究方向为果蔬加工适宜性评价、制汁品质形成机理与调控技术。Email：liuxuancaas@126.com

毕金峰，博士，研究员，研究方向为果蔬精深加工与综合利用理论与技术。Email：bijinfeng2010@163.com

10.11975/j.issn.1002-6819.2018.13.038

TS255.1

A

1002-6819(2018)-13-0311-08

刘 璇，刘嘉宁，毕金峰，周 沫，吕 健，彭 健. 果胶对脂类和类胡萝卜素消化利用影响研究进展[J]. 农业工程学报，2018，34(13)：311－318. doi：10.11975/j.issn.1002-6819.2018.13.038 http://www.tcsae.org

Liu Xuan, Liu Jianing, Bi Jinfeng, Zhou Mo, Lü Jian, Peng Jian. Review on effects of pectin on digestion of lipid and carotenoids[J]. Transactions of the Chinese Society of Agricultural Engineering (Transactions of the CSAE), 2018, 34(13): 311－318. (in Chinese with English abstract) doi：10.11975/j.issn.1002-6819.2018.13.038 http://www.tcsae.org