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The preparation, formation, fermentability, and applications of resistant starch
Journal Pre-proofs The preparation, formation, fermentability, and applications of resistant starch Fan Jiang, Chunwei Du, Wenqian Jiang, Liying Wang, Shuang-kui Du PII: DOI: Reference:
S0141-8130(19)35041-X https://doi.org/10.1016/j.ijbiomac.2019.10.124 BIOMAC 13625
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Please cite this article as: F. Jiang, C. Du, W. Jiang, L. Wang, S-k. Du, The preparation, formation, fermentability, and applications of resistant starch, International Journal of Biological Macromolecules (2019), doi: https://doi.org/10.1016/j.ijbiomac.2019.10.124
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The preparation, formation, fermentability, and applications of resistant starch Fan Jianga, Chunwei Dua, Wenqian Jianga, Liying Wanga, Shuang-kui Dua* a
College of Food Science and Engineering, Northwest A&F University, Yangling, Shaanxi 712100,
China
*Corresponding to: Prof. Shuang-kui Du, College of Food Science and Engineering, Northwest A&F University, Yangling, Shaanxi 712100, China Tel.: 86-29-87092206; fax: 86-29-87092486; E-mail address: [email protected](S. K. Du)
Abstract Resistant starch (RS) cannot be digested in the small intestine but can be fermented by microflora in the colon. To meet the demand for RS, effective methods and advanced equipment for preparing RS have emerged, but further development is needed. RS contents are affected by different prepared methodsˈ starch source and certain nutrients such as protein, phenols, and hydrocolloids interacted with RS. As a beneficial fermentation substrate, RS modifies and stabilizes the intestinal flora to balance the intestinal environment and improve intestinal tract health and function. RS is also a kind of ingredient with potential physiological function, even better than that dietary fiber, but also in terms of providing various health benefits. RS has good food-processing characteristics as well and can thus be widely used in the food industry.
Keywords: resistant starch; food matrix compounds; intestinal microorganism.
1. Introduction For a long time, starch has been considered to be completely digestible by the human body because of the lack of residual starch components detected in human excreta. However, researchers have found through in vitro experiments that some starch components are not hydrolyzed by amylase. Moreover, undigested components are termed resistant starch (RS), which as a part of starch molecule is peculiar in resisting to enzymatic digestion in the small intestine and reaching the colon nearly intact. Undigested components have been an emerging food worldwide in recent years [1-3]. Since then, numerous experiments have shown that RS can not be absorbed in the small intestine but can be fermented in the large intestine to produce various short- chain fatty acids (SCFAs) including acetate, propionate and butyrate, which plays a particularly positive role in promoting intestinal health [4]. In addition to SCFAs, RS is fermented by intestinal microorganism to produce gas (mainly H2, CO2 and CH4), lactate, succinate and bacterial cell biomass [5]. With the increasing demands of consumers on the functional foods, the utilization of food raw materials and the development of technology are also increasing. As a new resource of dietary fiber, RS has become a focus of research in food science with better physiological function compared to dietary fiber.
On the basis of their rate and extent of in vitro digestion, starch can be divided into three categories. There are rapidly digestible starch (RDS, namely, the amount of starch is rapidly digested and absorbed by enzymes within 20 min in vitro digestion) and slowly digestible starch (SDS, which can be completely digested but not as fast from 20 min to 120 min) on the first two groups [6]. The third group defined as RS refers to still not be digested within 120 min in the small intestine and therefore passes into the large bowel where it can act as fermentative substrate [7]. In terms of RS, which can be divided originally into three types from the perspectives of nutrition and termed them as physically trapped starch (RS1, that cannot be hydrolyzed because of the barrier effect of cell walls or the isolation effect of proteins, found in partially ground beans and grains), resistant starch granules (RS2, that refers to the natural resistant starch granules such as raw potato and banana starch), and retrograded starch (RS3, which is difficult to be hydrolyzed by amylase because of its crystallization formed during cooling and storage after gelatinization) [8]. With the research development, Englyst added another type of RS, which is a chemically modified starch (RS4, such as carboxymethyl starch and cross-linked starch, which has resistance to enzymatic hydrolysis due to the change of its original molecular structure and the introduction of some chemical functional groups by chemical modification), according to the property of resistance to enzymatic hydrolysis [9]. Lastly, a new RS termed as RS5 is characterized by a complex of amylose and lipids to form a helical structure that is difficult to be digested [10, 11]. Except for RS1 and RS2, all of them need modification to be formed, which can be converted by starch during food
production or processing. Significant different effects on food flavor in addition to the processing among different types of RS are observed. Referring to the physicochemical properties of RS, which is insoluble in water but can be dissolved in the solution of 2 mol/L KOH and dimethyl sulfoxide (DMSO), its average degree of polymerization is 30–200, its amylose crystal is melted at 100 Ԩ-165 Ԩ,
and it has high heat-resistance and low water-holding power from 1.4 g to 2.8 g. X-ray
diffraction type of RS is V-type or B-type with the stable double helix, which has a high degree of order that increases tolerance to α-amylase and thus reduce the digestibility of starch. In addition, almost no losses are observed after high temperature cooking and low caloric content, and its calorific value is less than 10.5 kJ/g [12-14]. Nutritionally, RS is deemed as nondigestible carbohydrate just like nondigestible oligosaccharides and nonstarch polysaccharides [15]. As a functional food, RS has been given great importance benefit for decreasing the incidence of enteric disease. There have been numerous studies that have shown RS has a great number of biological superiority about effectively preventing a variety of intestinal diseases, decreasing of insulin response and glycemia index, and even increasing the amount of beneficial bacteria and mineral absorption [16-18]. As proven, the four types of RS (except RS1) probably ameliorated oxidative stress, produced volatile several SCFAs and promoted gastric emptying to attenuate the morbidity of ethanol-induced gastric ulcerative lesion effectively [19]. Moreover, RS is a good substrate for butyrate production, which can alter microRNA (miRNA) levels in colorectal cancer cells to reducing risk associated with an high red meat diet [20]. Dietary RS might improve gastrointestinal tract function so that improves
human health, especially for people with diabetes. Therefore, the aim of this review is to give a focus on the methods that can be used for preparation, properties and physiology function, along with emerging applications of RS. 2. Resistant starch preparation Given the functional properties and strong market demand of RS, an increasing number of researchers are now committed in promoting the yield of RS by looking for improving the traditional modification methods and developing technological innovations to realize the industrialized production of RS. Therefore, modifying starch is the most important method to improve the RS content. In recent years, the burgeoning methodologies and technologies that can be employed to increase RS content from different sources have become advancing continuously. The methods of improving the RS content from various food sources are summarized in Table 1. By far, several methods are available to prepare RS3 compared with other types of RS. The chemical and enzymatic methods are the main method with high content of RS. However, the chemical methods in most cases have problems associated with low reaction rate, long production time, unstable product quality, and environmental pollution. Moreover, product safety is needed to be considered when chemically modified starch is used in the food industry. The chemical reaction and also the enzyme reaction are relatively complex [37]. However, the physically modified method is environmentally friendly, economical, and applicable. Compared with chemically modified starch, the physicochemical properties of physically modified starch have been significantly
improved. The application range and added value of products have also been greatly improved [38]. In general, the physical methods, most primarily heat-moisture treatment (HMT), autoclaving, and annealing, were the useful laborious method and effectively increased the RS content from various types of starches. In the past few years, some of physical methods with mild processing are burgeoning, such as high hydrostatic pressure (HHP), microwave, extrusion, and sonicate, which are like to replace high energy and time-consuming thermal methods [33]. In the future, the research should be focused on further work in optimizing starch modification methods to improve the RS content, shorten the processing time, avoid environmental pollution, obtain several modified starches with different characteristics, and to offer possibility for the application of starch in food products. 3. Resistant starch formation RS is found in some natural foods, different plant sources and even different genotypes of starch fundamentally affect the formation of RS. In addition, the interaction between starch and some nonstarch component has reduced the degree of starch hydrolysis to promoting the formation of RS [38]. As a primary food matrix, protein has been found to play a significant role in decreasing starch digestibility [39, 40]. Besides, endogenous or exogenous food matrix, such as hydrocolloids and phenolic compounds, were important to mitigate starch digestion behaviour [41]. Therefore, it has been an ideal way to increase RS content that complexation with exogenous or endogenous food matrix.
3.1. Starch source As outlined in Table 1, starches with high amylose are the main raw material for preparing RS, such as high amylose corn starch. Starch grains with larger average size, such as tubers and beans, which have lower hydrolysis rate [42]. As for different genotypes, the starch molecules with higher the average degree of polymerization are more easier to prepare RS [43]. The rapid development of biotechnology provides new ideas and techniques for breeding of high RS crop varieties. Through genetic modification, cultivars with high RS content have been formed in major cereal crops such as rice, corn and wheat. Kim et al. [44] breeded the high-amylose rice mutant named gaomi 2 by mutation breeding with N-methyl-N-nitrosourea (MNU). A new mutant were induced by radiation in rice, which was termed SSċa with high RS content (around 6%) [45]. However, genetic modification of RS still faces severe challenges in increasing amylose content and reducing side effects on crop chemical composition and structure. 3.2. Protein Several in vitro studies have proven that that starch digestibility may be reduced an account of the interaction with proteins, even some cereal grains and oil seeds also support the hypothesis [46-47]. Sample made with only wheat starch released 84.3% soluble starch after 84 min, whereas extrudate with 12% native pea protein or 12% hydrolyzed pea protein released 67.2% and 49.8% soluble starch after 84 min, respectively [48]. Some of the same conclusions have been reported that hydrolyzed
and/or denatured plant proteins significantly increased the RS content compared with intact proteins [49]. Water-insoluble proteins that may act as a physical barrier to digestion are found on the surface of starch granules which embedded starch via forming a elastin network as sheet-like structures, namely RS1, restricting enzymes to access starch so that reduce degree of starch hydrolysis [50, 51]. Furthermore, the low molecular weight protein (hydrolysis or denaturation) may wrap well due to increased starch-protein interaction surface. However, water-soluble proteins can reduce the enzyme activity of α-amylase to mitigate starch digestion potently [52]. Confirmed by Fourier transform infrared spectroscopy (FTIR), the RS content was positively correlated to protein via enhancing retrogradation of amylopectin and restricting starch granule swelling [47]. Because proteins in food matrix are in a position to decrease starch digestibility, that are related with health benefits, such as reduced glycemic index when blended with starch [53]. 3.3. Phenolic Phenolic substances, mainly found in plant extracts and grains, are close relevant to human life effecting digest, nutrition and health with biological activity. Interestingly, some results have been reported that dietary phenolics have the ability to attenuate starch digestion and possess cardioprotective effects [54]. In short, phenolic compounds reduce starch digestion mainly by inhabiting the activity of α-amylase. This phenomenon can be seen in resveratrol-3-O-glucoside occupying one of the binding sites of α-amylase as an antinutritional factor, which modulates starch digestion through phenolic interactions with digestive enzymes [55]. This mechanism is similar to that reported by previous
papers [56, 57]. Moreover, the structures of high-amlyose corn starch can be changed to V-type amylose by interacting with phenolic extracts (Genistein). The V-type starch has a high degree of order that increases tolerance to α-amylase and thus reduce the digestibility of starch [58]. Recent investigation found that can bridge amylose together through hydrogen bonding interaction, which increased the hydrodynamic radius of amylose molecules leading to increased molecular sizes resulting in slow digestion property of starch [59]. Some research on the interactions between maize amylopectin and potato starch with caffeic acid, gallic acid, and ferulic acid, which suggested that maize amylopectin-caffeic acid or amylopectin-ferulic acid mixtures increased RS content from 8.0% to 8.99% or 9.93% compared with maize amylopectin, respectively. Similar results were also observed for potato starch, wherein the RS content increased from 4.55% to 19.2% or 15.9%. However, gallic acid had no significant influence on RS content despite its potential to stimulate amylopectin hydrolysis in low concentration [60]. Collectively, these interactions result in producing slowly digestible starches, especially RS by retarding in starch digestion, in addition to control blood glucose. 3.4. Hydrocolloids The mixtures of the starch and hydrocolloid showed significant stability and good quality used widely in the food industry. However, there are often involved in noticeable presence of other hydrocolloids in the food formulations of RS [61]. Therefore, researching the interactions between RS and hydrocolloids are considerably meaningful. Addition of certain hydrocolloid can protect starch granules against shear during pasting, modify the product rheology, protect against syneresis, and even increase the
retrogradation degree [62]. Chen blended native maize starch with guar gum, tara gum and locust bean gum with heat-moist treatment (HMT) to produce starch- galactomannan complex [63]. RS content of final composites were all significantly increased than that native and HMT starches due to that the crystal structure of composites becomes stable after modification. Li claimed that waxy rice starch was impregnated with xanthan, and increased starch particle size and crystallinity were observed after heat treating [64]. Therefore, the anti-enzymatic hydrolysis was improved to a certain extent. Pectin also has high application value in food industry as the excellent emulsifying, gelling and thickening agent. Zhang discovered through research that the content of SDS and RS both significant increase in retrograded starch-pectin complex [65]. However, its relative crystallinity significantly decreased. β-Glucan is widely found in natural foods, especially oats, beneficial to glycemic control. β-Glucan has a network-like native structure-encapsulating protein and starch to reduce the enzyme accessibility and also the starch digestion [66].These results showed that the digestibility of composites was affected greatly by the composite methods, mixing ratio, and the additive molecular size. 4. Resistant starch fermentability RS can resist the enzymatic digestion in the upper parts of the gastrointestinal tract but can be fermented by resident microorganisms in the hindgut [67]. To our knowledge, RS including some nondigestible carbohydrates provides a major source of energy for bacteria that proliferate in the human large intestine [1]. A plethora of data also showed that microbial fermentation of RS in the colon produces of SCFAs, like lactic acid, acetate, propionate, and butyrate, which are the main end products of microbial
fermentation [68, 69]. SCFA productions in turn create an acidic environment to proliferate colonic and cecal cells, increase the expression of gut genes, and decrease ileal and cecal digesta pH, meanwhile promote the growth of beneficial microorganisms [10]. Acetate can provides energy for the metabolism of the spleen, heart and brain. Propionate can inhibit the synthesis of cholesterol and fatty acids in the liver, thereby decreasing blood lipid levels. And butyrate usually reduces the pH in the colon and thus inhibits the proliferation and metastasis of pathogenic bacteria [70]. Recorded experiment on feeding resistant potato starch (RPS) to weaned pigs for 28 days found that RPS improved the concentrations of acetate and the total volatile fatty acid of cecal digesta but decreased the constituents of branched-chain fatty acids [71]. The clinical study determined the influence of daily consumption of MSPrebiotic® (a RS) more than 3 months, significantly increasing Bifidobacterium and the butyrate levels in the large intestine compared with placebo [72]. RS generally provides the largest source of energy for microbial growth in the human colon. Bacterial species are fecund depending on different types of RS for feeding. Different type of RS is able to alter the different composition of gut microbial community [73]. For example, RS2 produces Ruminococcus bromii and Eubacterium rectale to increase the abundance of butyrate in excreta. Meanwhile, RS4 can increase Parabacteroides distasonis and Bifidobacterium adolescentis to improve lipid metabolism disorders [74]. Similarly, Roseburia spp. and Ruminococcus bromii are important butyrate producers in large intestine, which are increased by retrograded starch (RS3) modulating microbiota profiles [75]. In fact, Ruminococcus bromii is a
keystone species in the human colon for the degradation and utilization of RS, especially RS3. Ruminococcus bromii has a preference for α (1-4)-linked oligosaccharides and releases products from RS that can be utilized by other gut bacteria [76]. RS3 of lotus seed promoted the growth of Bifidobacterium longum producing lots of acetic acid, and Lactobacillus delbrueckii subsp. bulgaricus producing lactic acid, Which in turn inhibited the proliferation and metastasis of pathogenic bacteria because of the low pH in the colon [77]. The above description indicates different chemical structure of RS has the potential to impact the relative abundance of microbial species. From another point of view, adding RS into feed containing high crude protein helps to reduce the consequences of harmful nitrogenous metabolites [78-79]. The fermentation products of this protein contain toxicity and proinflammatory factros causing intestinal disease. Extensive experiments have stated that RS can influence the composition of the microflora to weaken the protein fermentation in the cecum and colon in vitro [80-81]. The study found that prolong RS intake of diet simultaneously increased the contents of mucin and crude protein, whereas decreased NH3-N, tryptamine, tyramine, phenol, cresol, indole and skatole contents in the colon of pigs [82]. RS affects the microbial compositions of the hindgut, and finally changes the fermentation metabolites from protein. In conclusion, RS exerts a beneficial fermentation substrate to balance the intestinal environment, and modify and stabilize the gut microbial community to improve the intestinal health and function.
5. Resistant starch application
With the improvement of living standards, functional food is increasingly favored by people. Dietary fiber, as an extremely important raw food material, has attracted the attention of researchers in nutrition and medical fields. All countries worldwide have strict regulations on the intake of dietary fiber every day. As a new type of food additive, RS has the physiological function of dietary fiber, and other advantages not possessed by dietary fiber. Its basic characteristics are similar to common starch and do not affect the taste, texture and sensory evaluation of food when added to it. To date, the structure, formation mechanism, determination method, and health properties of RS have been extensively studied. In addition, a great number of RS is used in the food industry as food additive [83]. Many RS commodities are also available in the market. Given the unique functional properties and physiological benefits of RS, processing and controlling RS, considering the special low water holding capacity of RS, are easy [84]. RS has the functionality of dietary fiber. Colloidal RS4 nanoparticles prepared from acid-hydrolysis and cross-linking can be widely applied to develop a beverage that is rich in dietary fiber [85].The natural sources, bland flavor, whitish color, good viscosity stability, and rheological properties, and low water-holding power of RS were determined to ensure they meet the functional requirements of the beverage industry [86]. RS acting as a texture modifier is added in wide kinds of baked foods, thereby giving favorable brittlenes and tenderness to bread crumbs [87].
Jain and Anal stated that the formed stability by using the protein hydrolysates was enhanced with the RS addition [88]. RS effectively improves the emulsifying capacity of emulsions and retards the lipid oxidation in food products. This conclusion is consistent with the published paper [89-90]. RS also can be used as a thickening agent in soup and dairy products due to its properties such as increased viscosity, fine particle size, high pasting temperature, and low water-holding properties. Furthermore, RS used as feed additives is an alternative to in-feed antibiotics, which can improve the use of protein and energy to increase the growth rate of animals [67]. However, due to the starch hydrophilicity and to avoid unnecessary release of bioactives in the upper gastrointestinal tract, starches are needed to be modified with insolubility and impermeability used as coating films [91]. To date, some studies indicated that RS is used as coating for food grade microcapsules because of its excellent extrusion and film-forming qualities. Chen et al.[92] developed a novel type of RS-coated microparticles via an aqueous suspension coating, which accurately targeted bioactive compound delivery to the colon. Bie et al. [93] designed concanavalin A-conjugated RS acetate film via film coating and extrusion-spheronization to develope a potential bioadhesive coating material for colon-targeting microcapsules. 6. Conclusion To date, finding the natural functional food with properties of resistance to cardiovascular disease and diabetes has become a research hotspot. The biological and chemical characteristics of RS determine that it can effectively satiate hunger but cannot
be absorbed by the gastrointestinal tract or its absorption rate is very low. Technically, to prepare RS through different physical, enzymatic, and chemical modifications affecting the RS content is possible. RS interaction with certain nutrients, such as protein, cellulose, and phenols, further promotes its health benefits. RS is fermented by microbes in the large intestine, producing SCFAs, and modifies and stabilizes gut microbial community to improve gut health and function. The RS properties, such as bland flavor, fine particle size, low water holding, and film forming qualities, make the formulation of a wide usable range of food products comparing with wheat, corn, banana, and most agricultural products all contain different amounts of RS. Preparing and processing RS applied as additives in the food processing field can also produce great economic and social benefits. Thus, a wider spread of evidence relating to benefit of RS that would be useful in promoting innovation to increasing the RS intake in humans. Acknowledgements The authors would like to thank Shaanxi Province Key Research and Development Program Project (2017NY-177) and Shaanxi Province Agricultural Science and Technology Innovation and Transformation Project (NYKJ-2018-YL19) for the support. References [1] H. J. Flint, The impact of nutrition on the human microbiome, Nutrition Reviews. 70 (Suppl 1) (2012), S10-13. https://doi.org/10.1111/j.1753-4887.2012.00499.x. [2] S. Lockyer, A. P. Nugent, Health effects of resistant starch, Nutrition Bulletin. 42
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Table 1. Process methods and conditions, yield of resistant starch from different starch sources. Methods
Starch source
Conditions
Yield㸦%
Reference
㸧 Physical modification
High-amylose corn
Extrusion cycle: 3 (60% feed moisture, 100 rpm screw speed, 140Ԩ barrel temperature)
45.10
[21]
Potato
Microwave: 300w, 100s; Toughen: 55Ԩ, 26h; Aging: 4Ԩ, 18h
27.09
[22]
High-amylose corn
Gelatinization: boiling water bath for 10min;
43.40
[23]
Autoclaving: 121Ԩ, 30min;
Microwave-storing cycle: 3 (microwave: 160w, 2min oven-storing: 95Ԩ, 45min) Normal rice
Autoclaving-cooling cycle: 2 (autoclaving: 121Ԩ, 30min cooling: 4Ԩ, 24 h )
38.65
[24]
Normal corn
4-α-glucanotransferase (10U/g starch): pH 7.5, 75Ԩ, 4h
17.63
[25]
Normal maize
Thermostable isoamylase(7U/g starch)+ amylase (2NU/g starch): pH 5.0, 70Ԩ, 6h
53.80
[26]
Chemical modification
Brown lentil
Palmitic acid: 10% ; Gelatinization: 95Ԩ water bath for 8min
16.30
[27]
Composite modification
Normal maize
Immobilized pullulanase: sol-gel encapsulate it onto chitosan/Fe3O4 nanoparticles
43.40
[28]
12.13
[29]
Enzymatic modification
(10ASPU/g starch) , at pH 4.4, 50Ԩ, 5h Commercial corn
Guar gum(10%)+citric(2.5%): 25% moisture ; Storage: 4Ԩ, 7day; Extrusion: 30rpm
High-amylose corn
Autoclaving-cooling-storing cycle: 3 (Autoclaving: 145Ԩ,30min storing: 4Ԩ, 72h);
30.41
[30]
47.20
[31]
Acid hydrolysis: 0.1M HCl, 40Ԩ, 24h High-amylose corn
Gelatinization: cooked for 45min; Autoclaving: 121Ԩ, 30min; Pullulanase: 60Ԩ, 48h(1.5U/g starch); Microwave-storing cycle: 1 (microwave: 160w, 4min oven-storing: 95Ԩ, 24h); Oven drying: 50Ԩ
High-amylose rice
Acid hydrolysis: 0.2M citric acid; Heat-moisture: 30% moisture, 110Ԩ, 8h
39.00
[32]
Buckwheat
High pressure-cooling cycle: 3 (high pressure: 600MPa, 9min cooling: 4Ԩ, 24h);
4.33
[33]
42.34
[34]
32.90
[35]
64.60
[36]
Pullulanase: 60Ԩ,16 h(1U/g starch) Red kidney beans
Gelatinization: boiling water bath for 10min; Pullulanase: pH5.3, 60Ԩ, 10h(40U/g starch); Autoclaving: 121Ԩ, 30min
Yellow peas
Gelatinization: 80Ԩ water bath for 10min; Pullulanase: 40 NPUN/g starch; Sonicate: 100% amplitude in pulse mode(1 min of sonication, 9 min off), at pH5.2, 50Ԩ, 6h
Chinese chestnut
Gelatinization: 80Ԩ water bath for 15min; Autoclaving: 121Ԩ, 15min; Pullulanase: pH5.7, 55Ԩ 5h (9 PUN/g starch )
Highlights˖ Summarizing preparation methods in increasing the resistant starch content. Stating the interaction between resistant starch and food matrix compounds. Resistant starch can modify and stabilize the gut microbial community.
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S0141-8130(19)35041-X https://doi.org/10.1016/j.ijbiomac.2019.10.124 BIOMAC 13625
To appear in:
International Journal of Biological Macromolecules
Received Date: Revised Date: Accepted Date:
3 July 2019 11 October 2019 13 October 2019
Please cite this article as: F. Jiang, C. Du, W. Jiang, L. Wang, S-k. Du, The preparation, formation, fermentability, and applications of resistant starch, International Journal of Biological Macromolecules (2019), doi: https://doi.org/10.1016/j.ijbiomac.2019.10.124
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The preparation, formation, fermentability, and applications of resistant starch Fan Jianga, Chunwei Dua, Wenqian Jianga, Liying Wanga, Shuang-kui Dua* a
College of Food Science and Engineering, Northwest A&F University, Yangling, Shaanxi 712100,
China
*Corresponding to: Prof. Shuang-kui Du, College of Food Science and Engineering, Northwest A&F University, Yangling, Shaanxi 712100, China Tel.: 86-29-87092206; fax: 86-29-87092486; E-mail address: [email protected](S. K. Du)
Abstract Resistant starch (RS) cannot be digested in the small intestine but can be fermented by microflora in the colon. To meet the demand for RS, effective methods and advanced equipment for preparing RS have emerged, but further development is needed. RS contents are affected by different prepared methodsˈ starch source and certain nutrients such as protein, phenols, and hydrocolloids interacted with RS. As a beneficial fermentation substrate, RS modifies and stabilizes the intestinal flora to balance the intestinal environment and improve intestinal tract health and function. RS is also a kind of ingredient with potential physiological function, even better than that dietary fiber, but also in terms of providing various health benefits. RS has good food-processing characteristics as well and can thus be widely used in the food industry.
Keywords: resistant starch; food matrix compounds; intestinal microorganism.
1. Introduction For a long time, starch has been considered to be completely digestible by the human body because of the lack of residual starch components detected in human excreta. However, researchers have found through in vitro experiments that some starch components are not hydrolyzed by amylase. Moreover, undigested components are termed resistant starch (RS), which as a part of starch molecule is peculiar in resisting to enzymatic digestion in the small intestine and reaching the colon nearly intact. Undigested components have been an emerging food worldwide in recent years [1-3]. Since then, numerous experiments have shown that RS can not be absorbed in the small intestine but can be fermented in the large intestine to produce various short- chain fatty acids (SCFAs) including acetate, propionate and butyrate, which plays a particularly positive role in promoting intestinal health [4]. In addition to SCFAs, RS is fermented by intestinal microorganism to produce gas (mainly H2, CO2 and CH4), lactate, succinate and bacterial cell biomass [5]. With the increasing demands of consumers on the functional foods, the utilization of food raw materials and the development of technology are also increasing. As a new resource of dietary fiber, RS has become a focus of research in food science with better physiological function compared to dietary fiber.
On the basis of their rate and extent of in vitro digestion, starch can be divided into three categories. There are rapidly digestible starch (RDS, namely, the amount of starch is rapidly digested and absorbed by enzymes within 20 min in vitro digestion) and slowly digestible starch (SDS, which can be completely digested but not as fast from 20 min to 120 min) on the first two groups [6]. The third group defined as RS refers to still not be digested within 120 min in the small intestine and therefore passes into the large bowel where it can act as fermentative substrate [7]. In terms of RS, which can be divided originally into three types from the perspectives of nutrition and termed them as physically trapped starch (RS1, that cannot be hydrolyzed because of the barrier effect of cell walls or the isolation effect of proteins, found in partially ground beans and grains), resistant starch granules (RS2, that refers to the natural resistant starch granules such as raw potato and banana starch), and retrograded starch (RS3, which is difficult to be hydrolyzed by amylase because of its crystallization formed during cooling and storage after gelatinization) [8]. With the research development, Englyst added another type of RS, which is a chemically modified starch (RS4, such as carboxymethyl starch and cross-linked starch, which has resistance to enzymatic hydrolysis due to the change of its original molecular structure and the introduction of some chemical functional groups by chemical modification), according to the property of resistance to enzymatic hydrolysis [9]. Lastly, a new RS termed as RS5 is characterized by a complex of amylose and lipids to form a helical structure that is difficult to be digested [10, 11]. Except for RS1 and RS2, all of them need modification to be formed, which can be converted by starch during food
production or processing. Significant different effects on food flavor in addition to the processing among different types of RS are observed. Referring to the physicochemical properties of RS, which is insoluble in water but can be dissolved in the solution of 2 mol/L KOH and dimethyl sulfoxide (DMSO), its average degree of polymerization is 30–200, its amylose crystal is melted at 100 Ԩ-165 Ԩ,
and it has high heat-resistance and low water-holding power from 1.4 g to 2.8 g. X-ray
diffraction type of RS is V-type or B-type with the stable double helix, which has a high degree of order that increases tolerance to α-amylase and thus reduce the digestibility of starch. In addition, almost no losses are observed after high temperature cooking and low caloric content, and its calorific value is less than 10.5 kJ/g [12-14]. Nutritionally, RS is deemed as nondigestible carbohydrate just like nondigestible oligosaccharides and nonstarch polysaccharides [15]. As a functional food, RS has been given great importance benefit for decreasing the incidence of enteric disease. There have been numerous studies that have shown RS has a great number of biological superiority about effectively preventing a variety of intestinal diseases, decreasing of insulin response and glycemia index, and even increasing the amount of beneficial bacteria and mineral absorption [16-18]. As proven, the four types of RS (except RS1) probably ameliorated oxidative stress, produced volatile several SCFAs and promoted gastric emptying to attenuate the morbidity of ethanol-induced gastric ulcerative lesion effectively [19]. Moreover, RS is a good substrate for butyrate production, which can alter microRNA (miRNA) levels in colorectal cancer cells to reducing risk associated with an high red meat diet [20]. Dietary RS might improve gastrointestinal tract function so that improves
human health, especially for people with diabetes. Therefore, the aim of this review is to give a focus on the methods that can be used for preparation, properties and physiology function, along with emerging applications of RS. 2. Resistant starch preparation Given the functional properties and strong market demand of RS, an increasing number of researchers are now committed in promoting the yield of RS by looking for improving the traditional modification methods and developing technological innovations to realize the industrialized production of RS. Therefore, modifying starch is the most important method to improve the RS content. In recent years, the burgeoning methodologies and technologies that can be employed to increase RS content from different sources have become advancing continuously. The methods of improving the RS content from various food sources are summarized in Table 1. By far, several methods are available to prepare RS3 compared with other types of RS. The chemical and enzymatic methods are the main method with high content of RS. However, the chemical methods in most cases have problems associated with low reaction rate, long production time, unstable product quality, and environmental pollution. Moreover, product safety is needed to be considered when chemically modified starch is used in the food industry. The chemical reaction and also the enzyme reaction are relatively complex [37]. However, the physically modified method is environmentally friendly, economical, and applicable. Compared with chemically modified starch, the physicochemical properties of physically modified starch have been significantly
improved. The application range and added value of products have also been greatly improved [38]. In general, the physical methods, most primarily heat-moisture treatment (HMT), autoclaving, and annealing, were the useful laborious method and effectively increased the RS content from various types of starches. In the past few years, some of physical methods with mild processing are burgeoning, such as high hydrostatic pressure (HHP), microwave, extrusion, and sonicate, which are like to replace high energy and time-consuming thermal methods [33]. In the future, the research should be focused on further work in optimizing starch modification methods to improve the RS content, shorten the processing time, avoid environmental pollution, obtain several modified starches with different characteristics, and to offer possibility for the application of starch in food products. 3. Resistant starch formation RS is found in some natural foods, different plant sources and even different genotypes of starch fundamentally affect the formation of RS. In addition, the interaction between starch and some nonstarch component has reduced the degree of starch hydrolysis to promoting the formation of RS [38]. As a primary food matrix, protein has been found to play a significant role in decreasing starch digestibility [39, 40]. Besides, endogenous or exogenous food matrix, such as hydrocolloids and phenolic compounds, were important to mitigate starch digestion behaviour [41]. Therefore, it has been an ideal way to increase RS content that complexation with exogenous or endogenous food matrix.
3.1. Starch source As outlined in Table 1, starches with high amylose are the main raw material for preparing RS, such as high amylose corn starch. Starch grains with larger average size, such as tubers and beans, which have lower hydrolysis rate [42]. As for different genotypes, the starch molecules with higher the average degree of polymerization are more easier to prepare RS [43]. The rapid development of biotechnology provides new ideas and techniques for breeding of high RS crop varieties. Through genetic modification, cultivars with high RS content have been formed in major cereal crops such as rice, corn and wheat. Kim et al. [44] breeded the high-amylose rice mutant named gaomi 2 by mutation breeding with N-methyl-N-nitrosourea (MNU). A new mutant were induced by radiation in rice, which was termed SSċa with high RS content (around 6%) [45]. However, genetic modification of RS still faces severe challenges in increasing amylose content and reducing side effects on crop chemical composition and structure. 3.2. Protein Several in vitro studies have proven that that starch digestibility may be reduced an account of the interaction with proteins, even some cereal grains and oil seeds also support the hypothesis [46-47]. Sample made with only wheat starch released 84.3% soluble starch after 84 min, whereas extrudate with 12% native pea protein or 12% hydrolyzed pea protein released 67.2% and 49.8% soluble starch after 84 min, respectively [48]. Some of the same conclusions have been reported that hydrolyzed
and/or denatured plant proteins significantly increased the RS content compared with intact proteins [49]. Water-insoluble proteins that may act as a physical barrier to digestion are found on the surface of starch granules which embedded starch via forming a elastin network as sheet-like structures, namely RS1, restricting enzymes to access starch so that reduce degree of starch hydrolysis [50, 51]. Furthermore, the low molecular weight protein (hydrolysis or denaturation) may wrap well due to increased starch-protein interaction surface. However, water-soluble proteins can reduce the enzyme activity of α-amylase to mitigate starch digestion potently [52]. Confirmed by Fourier transform infrared spectroscopy (FTIR), the RS content was positively correlated to protein via enhancing retrogradation of amylopectin and restricting starch granule swelling [47]. Because proteins in food matrix are in a position to decrease starch digestibility, that are related with health benefits, such as reduced glycemic index when blended with starch [53]. 3.3. Phenolic Phenolic substances, mainly found in plant extracts and grains, are close relevant to human life effecting digest, nutrition and health with biological activity. Interestingly, some results have been reported that dietary phenolics have the ability to attenuate starch digestion and possess cardioprotective effects [54]. In short, phenolic compounds reduce starch digestion mainly by inhabiting the activity of α-amylase. This phenomenon can be seen in resveratrol-3-O-glucoside occupying one of the binding sites of α-amylase as an antinutritional factor, which modulates starch digestion through phenolic interactions with digestive enzymes [55]. This mechanism is similar to that reported by previous
papers [56, 57]. Moreover, the structures of high-amlyose corn starch can be changed to V-type amylose by interacting with phenolic extracts (Genistein). The V-type starch has a high degree of order that increases tolerance to α-amylase and thus reduce the digestibility of starch [58]. Recent investigation found that can bridge amylose together through hydrogen bonding interaction, which increased the hydrodynamic radius of amylose molecules leading to increased molecular sizes resulting in slow digestion property of starch [59]. Some research on the interactions between maize amylopectin and potato starch with caffeic acid, gallic acid, and ferulic acid, which suggested that maize amylopectin-caffeic acid or amylopectin-ferulic acid mixtures increased RS content from 8.0% to 8.99% or 9.93% compared with maize amylopectin, respectively. Similar results were also observed for potato starch, wherein the RS content increased from 4.55% to 19.2% or 15.9%. However, gallic acid had no significant influence on RS content despite its potential to stimulate amylopectin hydrolysis in low concentration [60]. Collectively, these interactions result in producing slowly digestible starches, especially RS by retarding in starch digestion, in addition to control blood glucose. 3.4. Hydrocolloids The mixtures of the starch and hydrocolloid showed significant stability and good quality used widely in the food industry. However, there are often involved in noticeable presence of other hydrocolloids in the food formulations of RS [61]. Therefore, researching the interactions between RS and hydrocolloids are considerably meaningful. Addition of certain hydrocolloid can protect starch granules against shear during pasting, modify the product rheology, protect against syneresis, and even increase the
retrogradation degree [62]. Chen blended native maize starch with guar gum, tara gum and locust bean gum with heat-moist treatment (HMT) to produce starch- galactomannan complex [63]. RS content of final composites were all significantly increased than that native and HMT starches due to that the crystal structure of composites becomes stable after modification. Li claimed that waxy rice starch was impregnated with xanthan, and increased starch particle size and crystallinity were observed after heat treating [64]. Therefore, the anti-enzymatic hydrolysis was improved to a certain extent. Pectin also has high application value in food industry as the excellent emulsifying, gelling and thickening agent. Zhang discovered through research that the content of SDS and RS both significant increase in retrograded starch-pectin complex [65]. However, its relative crystallinity significantly decreased. β-Glucan is widely found in natural foods, especially oats, beneficial to glycemic control. β-Glucan has a network-like native structure-encapsulating protein and starch to reduce the enzyme accessibility and also the starch digestion [66].These results showed that the digestibility of composites was affected greatly by the composite methods, mixing ratio, and the additive molecular size. 4. Resistant starch fermentability RS can resist the enzymatic digestion in the upper parts of the gastrointestinal tract but can be fermented by resident microorganisms in the hindgut [67]. To our knowledge, RS including some nondigestible carbohydrates provides a major source of energy for bacteria that proliferate in the human large intestine [1]. A plethora of data also showed that microbial fermentation of RS in the colon produces of SCFAs, like lactic acid, acetate, propionate, and butyrate, which are the main end products of microbial
fermentation [68, 69]. SCFA productions in turn create an acidic environment to proliferate colonic and cecal cells, increase the expression of gut genes, and decrease ileal and cecal digesta pH, meanwhile promote the growth of beneficial microorganisms [10]. Acetate can provides energy for the metabolism of the spleen, heart and brain. Propionate can inhibit the synthesis of cholesterol and fatty acids in the liver, thereby decreasing blood lipid levels. And butyrate usually reduces the pH in the colon and thus inhibits the proliferation and metastasis of pathogenic bacteria [70]. Recorded experiment on feeding resistant potato starch (RPS) to weaned pigs for 28 days found that RPS improved the concentrations of acetate and the total volatile fatty acid of cecal digesta but decreased the constituents of branched-chain fatty acids [71]. The clinical study determined the influence of daily consumption of MSPrebiotic® (a RS) more than 3 months, significantly increasing Bifidobacterium and the butyrate levels in the large intestine compared with placebo [72]. RS generally provides the largest source of energy for microbial growth in the human colon. Bacterial species are fecund depending on different types of RS for feeding. Different type of RS is able to alter the different composition of gut microbial community [73]. For example, RS2 produces Ruminococcus bromii and Eubacterium rectale to increase the abundance of butyrate in excreta. Meanwhile, RS4 can increase Parabacteroides distasonis and Bifidobacterium adolescentis to improve lipid metabolism disorders [74]. Similarly, Roseburia spp. and Ruminococcus bromii are important butyrate producers in large intestine, which are increased by retrograded starch (RS3) modulating microbiota profiles [75]. In fact, Ruminococcus bromii is a
keystone species in the human colon for the degradation and utilization of RS, especially RS3. Ruminococcus bromii has a preference for α (1-4)-linked oligosaccharides and releases products from RS that can be utilized by other gut bacteria [76]. RS3 of lotus seed promoted the growth of Bifidobacterium longum producing lots of acetic acid, and Lactobacillus delbrueckii subsp. bulgaricus producing lactic acid, Which in turn inhibited the proliferation and metastasis of pathogenic bacteria because of the low pH in the colon [77]. The above description indicates different chemical structure of RS has the potential to impact the relative abundance of microbial species. From another point of view, adding RS into feed containing high crude protein helps to reduce the consequences of harmful nitrogenous metabolites [78-79]. The fermentation products of this protein contain toxicity and proinflammatory factros causing intestinal disease. Extensive experiments have stated that RS can influence the composition of the microflora to weaken the protein fermentation in the cecum and colon in vitro [80-81]. The study found that prolong RS intake of diet simultaneously increased the contents of mucin and crude protein, whereas decreased NH3-N, tryptamine, tyramine, phenol, cresol, indole and skatole contents in the colon of pigs [82]. RS affects the microbial compositions of the hindgut, and finally changes the fermentation metabolites from protein. In conclusion, RS exerts a beneficial fermentation substrate to balance the intestinal environment, and modify and stabilize the gut microbial community to improve the intestinal health and function.
5. Resistant starch application
With the improvement of living standards, functional food is increasingly favored by people. Dietary fiber, as an extremely important raw food material, has attracted the attention of researchers in nutrition and medical fields. All countries worldwide have strict regulations on the intake of dietary fiber every day. As a new type of food additive, RS has the physiological function of dietary fiber, and other advantages not possessed by dietary fiber. Its basic characteristics are similar to common starch and do not affect the taste, texture and sensory evaluation of food when added to it. To date, the structure, formation mechanism, determination method, and health properties of RS have been extensively studied. In addition, a great number of RS is used in the food industry as food additive [83]. Many RS commodities are also available in the market. Given the unique functional properties and physiological benefits of RS, processing and controlling RS, considering the special low water holding capacity of RS, are easy [84]. RS has the functionality of dietary fiber. Colloidal RS4 nanoparticles prepared from acid-hydrolysis and cross-linking can be widely applied to develop a beverage that is rich in dietary fiber [85].The natural sources, bland flavor, whitish color, good viscosity stability, and rheological properties, and low water-holding power of RS were determined to ensure they meet the functional requirements of the beverage industry [86]. RS acting as a texture modifier is added in wide kinds of baked foods, thereby giving favorable brittlenes and tenderness to bread crumbs [87].
Jain and Anal stated that the formed stability by using the protein hydrolysates was enhanced with the RS addition [88]. RS effectively improves the emulsifying capacity of emulsions and retards the lipid oxidation in food products. This conclusion is consistent with the published paper [89-90]. RS also can be used as a thickening agent in soup and dairy products due to its properties such as increased viscosity, fine particle size, high pasting temperature, and low water-holding properties. Furthermore, RS used as feed additives is an alternative to in-feed antibiotics, which can improve the use of protein and energy to increase the growth rate of animals [67]. However, due to the starch hydrophilicity and to avoid unnecessary release of bioactives in the upper gastrointestinal tract, starches are needed to be modified with insolubility and impermeability used as coating films [91]. To date, some studies indicated that RS is used as coating for food grade microcapsules because of its excellent extrusion and film-forming qualities. Chen et al.[92] developed a novel type of RS-coated microparticles via an aqueous suspension coating, which accurately targeted bioactive compound delivery to the colon. Bie et al. [93] designed concanavalin A-conjugated RS acetate film via film coating and extrusion-spheronization to develope a potential bioadhesive coating material for colon-targeting microcapsules. 6. Conclusion To date, finding the natural functional food with properties of resistance to cardiovascular disease and diabetes has become a research hotspot. The biological and chemical characteristics of RS determine that it can effectively satiate hunger but cannot
be absorbed by the gastrointestinal tract or its absorption rate is very low. Technically, to prepare RS through different physical, enzymatic, and chemical modifications affecting the RS content is possible. RS interaction with certain nutrients, such as protein, cellulose, and phenols, further promotes its health benefits. RS is fermented by microbes in the large intestine, producing SCFAs, and modifies and stabilizes gut microbial community to improve gut health and function. The RS properties, such as bland flavor, fine particle size, low water holding, and film forming qualities, make the formulation of a wide usable range of food products comparing with wheat, corn, banana, and most agricultural products all contain different amounts of RS. Preparing and processing RS applied as additives in the food processing field can also produce great economic and social benefits. Thus, a wider spread of evidence relating to benefit of RS that would be useful in promoting innovation to increasing the RS intake in humans. Acknowledgements The authors would like to thank Shaanxi Province Key Research and Development Program Project (2017NY-177) and Shaanxi Province Agricultural Science and Technology Innovation and Transformation Project (NYKJ-2018-YL19) for the support. References [1] H. J. Flint, The impact of nutrition on the human microbiome, Nutrition Reviews. 70 (Suppl 1) (2012), S10-13. https://doi.org/10.1111/j.1753-4887.2012.00499.x. [2] S. Lockyer, A. P. Nugent, Health effects of resistant starch, Nutrition Bulletin. 42
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Table 1. Process methods and conditions, yield of resistant starch from different starch sources. Methods
Starch source
Conditions
Yield㸦%
Reference
㸧 Physical modification
High-amylose corn
Extrusion cycle: 3 (60% feed moisture, 100 rpm screw speed, 140Ԩ barrel temperature)
45.10
[21]
Potato
Microwave: 300w, 100s; Toughen: 55Ԩ, 26h; Aging: 4Ԩ, 18h
27.09
[22]
High-amylose corn
Gelatinization: boiling water bath for 10min;
43.40
[23]
Autoclaving: 121Ԩ, 30min;
Microwave-storing cycle: 3 (microwave: 160w, 2min oven-storing: 95Ԩ, 45min) Normal rice
Autoclaving-cooling cycle: 2 (autoclaving: 121Ԩ, 30min cooling: 4Ԩ, 24 h )
38.65
[24]
Normal corn
4-α-glucanotransferase (10U/g starch): pH 7.5, 75Ԩ, 4h
17.63
[25]
Normal maize
Thermostable isoamylase(7U/g starch)+ amylase (2NU/g starch): pH 5.0, 70Ԩ, 6h
53.80
[26]
Chemical modification
Brown lentil
Palmitic acid: 10% ; Gelatinization: 95Ԩ water bath for 8min
16.30
[27]
Composite modification
Normal maize
Immobilized pullulanase: sol-gel encapsulate it onto chitosan/Fe3O4 nanoparticles
43.40
[28]
12.13
[29]
Enzymatic modification
(10ASPU/g starch) , at pH 4.4, 50Ԩ, 5h Commercial corn
Guar gum(10%)+citric(2.5%): 25% moisture ; Storage: 4Ԩ, 7day; Extrusion: 30rpm
High-amylose corn
Autoclaving-cooling-storing cycle: 3 (Autoclaving: 145Ԩ,30min storing: 4Ԩ, 72h);
30.41
[30]
47.20
[31]
Acid hydrolysis: 0.1M HCl, 40Ԩ, 24h High-amylose corn
Gelatinization: cooked for 45min; Autoclaving: 121Ԩ, 30min; Pullulanase: 60Ԩ, 48h(1.5U/g starch); Microwave-storing cycle: 1 (microwave: 160w, 4min oven-storing: 95Ԩ, 24h); Oven drying: 50Ԩ
High-amylose rice
Acid hydrolysis: 0.2M citric acid; Heat-moisture: 30% moisture, 110Ԩ, 8h
39.00
[32]
Buckwheat
High pressure-cooling cycle: 3 (high pressure: 600MPa, 9min cooling: 4Ԩ, 24h);
4.33
[33]
42.34
[34]
32.90
[35]
64.60
[36]
Pullulanase: 60Ԩ,16 h(1U/g starch) Red kidney beans
Gelatinization: boiling water bath for 10min; Pullulanase: pH5.3, 60Ԩ, 10h(40U/g starch); Autoclaving: 121Ԩ, 30min
Yellow peas
Gelatinization: 80Ԩ water bath for 10min; Pullulanase: 40 NPUN/g starch; Sonicate: 100% amplitude in pulse mode(1 min of sonication, 9 min off), at pH5.2, 50Ԩ, 6h
Chinese chestnut
Gelatinization: 80Ԩ water bath for 15min; Autoclaving: 121Ԩ, 15min; Pullulanase: pH5.7, 55Ԩ 5h (9 PUN/g starch )
Highlights˖ Summarizing preparation methods in increasing the resistant starch content. Stating the interaction between resistant starch and food matrix compounds. Resistant starch can modify and stabilize the gut microbial community.
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