What Is the Impact of Diet on Nutritional Diarrhea Associated with Gut Microbiota in Weaning Piglets: A System Review

Gao, Jing; Yin, Jie; Xu, Kang; Li, Tiejun; Yin, Yulong

doi:https://doi.org/10.1155/2019/6916189

BioMed Research International

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Volume 2019 | Article ID 6916189 | https://doi.org/10.1155/2019/6916189

What Is the Impact of Diet on Nutritional Diarrhea Associated with Gut Microbiota in Weaning Piglets: A System Review

Jing Gao,^1,2,3Jie Yin,^1,2,3Kang Xu,^1,2Tiejun Li ,^1,2and Yulong Yin^1,2,3,4

Guest Editor: Deguang Song

Received11 Oct 2019

Revised19 Nov 2019

Accepted03 Dec 2019

Published28 Dec 2019

Abstract

Piglets experience severe growth challenges and diarrhea after weaning due to nutritional, social, psychological, environmental, and physiological changes. Among these changes, the nutritional factor plays a key role in postweaning health. Dietary protein, fibre, starch, and electrolyte levels are highly associated with postweaning nutrition diarrhea (PWND). In this review, we mainly discuss the high protein, fibre, resistant starch, and electrolyte imbalance in diets that induce PWND, with a focus on potential mechanisms in weaned piglets.

1. Introduction

Weaning is sudden and stressful and one of the most challenging periods in a pig’s life [1]. Newly weaned pigs are usually stressed by nutritional, psychological, environmental, physiological, and social factors [2, 3]. Because of such stressors, piglets are often characterized with reduced growth performance and an increased prevalence of diarrhea after weaning [4, 5]. When undergoing the transition from a milk-based diet to a weaned diet, the piglets suffer a severe decrease in feed intake for a couple of days after weaning [6]. Furthermore, in order to adapt to the new environment, the composition of the gastrointestinal microbiota is also modified as a result of changes in feeding behavior and diet composition [6]. This period is often associated with a growth challenge because of a high incidence of gastrointestinal disorders, such as PWND [7].

Postweaning diarrhea is considered a major health problem and causes substantial morbidity and mortality in livestock [8, 9]. It is well established that postweaning diarrhea is a multifactorial gastrointestinal disease, and undernutrition has major etiological factors [10–12]. The gastrointestinal tract is a complex, balanced ecosystem [4, 13]. The dietary composition is a major factor influencing the intestinal microbial ecosystem [14, 15]. Hence, considering the balance between the intestinal microbial ecosystem and the composition of the diet, postweaning nutritional diarrhea (PWND) is a major problem during the postweaning period [11, 16].

The most efficient manner to alleviate the degree of PWND is to regulate the nutritional composition of the diet [15, 17]. Various nutritional approaches for improving the weaning transition and alleviating enteric diseases have been researched over the past several years [11, 18]. Evidence suggests that specific dietary interventions, such as the control of protein [19, 20], fibre [21], starch [22], electrolyte balance [23], and other constituents in the daily diet, could reduce the proliferation of certain PWND [11, 24, 25]. The purpose of the present review is to summarize several common kinds of PWND in order to better expound the role of nutrition in causing and modulating PWND in pigs.

2. High Protein Level Induces PWND

To decrease PWND, piglets are usually given antibiotics; however, antibiotics have been banned for use in livestock for human consumption. Thus, researchers have focused on finding a replacement for antibiotics in piglet feeding. One of the alternatives is the feeding of low-protein diets [26–28].

2.1. The Effect of Dietary Protein on Growth Performance and Digestibility of Nutrients of Weaned Piglets

The consumption of a low crude protein (CP) diet, which has direct effects on PWND, reduces the availability of substrates for bacterial fermentation and improves fecal consistency [29–31]. Dietary CP and individual AAs (amino acids) both affect the formation of metabolites during microbial fermentation [32]. However, high dietary CP concentration for early-weaned piglets could increase microbial fermentation of undigested protein and increase the proliferation of pathogenic bacteria in the gastrointestinal tract [3]. An excessive supply of dietary protein induces protein fermentation by intestinal microbiota in piglets [33]. Volatile fatty acids (VFAs) and potentially toxic compounds produced by bacterial fermentation of undigested protein substances, such as ammonia and amines, can reduce the growth performance of piglets [34, 35]. The increased production of amines has been found to increase the incidence of diarrhea at weaning in pigs [36, 37].

2.2. The Effect of Dietary Protein on the Gut Health of Weaned Piglets

It is well known that both exogenous and endogenous source proteins can be used by the gastrointestinal microbiota as a fermentable substrate [38, 39] and can be used for the production of diet proteins through degradation, including branched-chain fatty acids (BCFAs), ammonia, amines, phenols, and indoles [35, 39]. Bacteria, such as Bacteroides spp., Propionibacterium spp., Streptococcus, and Clostridium species, are associated with the formation of the substances listed above [20]. For example, BCFAs are produced by Clostridia [40]. Furthermore, intestinal concentrations of BCFAs possibly are used as indicators for the extent of protein fermentation [41].

Protein fermentation results in the production of metabolites that are in direct contact with the colonic mucosa and can directly interact with the mucosal cells. Undigested dietary protein and proteins of endogenous origin transfer to the large intestine for fermentation to toxic metabolites, such as ammonia, biogenic amines, and hydrogen sulfide. Most of these products can impair epithelial integrity and promote inflammatory reactions [34, 42]. Then, the metabolites or bacterial toxins may reduce the ability for fluid reabsorption and mask small intestinal hypersecretion [29]. An increased concentration of ammonia was found in parts of the intestinal tract of piglets fed high-protein diets [3]. Infusion of ammonium chloride from the isolated distal colon increased the proliferation of epithelial cells in rats, which may contribute to the development of gastrointestinal disorders [43]. Biogenic amine concentrations increased in the hindgut when feeding on highly fermentable protein, and bacterial putrescine played a role in the potential detrimental effects on gut health by decreasing the energy supply to the colonocytes [44]. Hydrogen sulfide impacts gut health by breaking down the mucus layer and by increasing the permeability of the mucus barrier [45]. According to several studies, high protein fermentation is associated with an increased risk of cancer [46].

2.3. The Effect of Dietary Protein on the Incidence of PWND

PWND is a gut disease induced by the stress of nutrition and is characterized by an increase in the microbial fermentation of supernumerary proteins [47]. Additionally, watery feces, decreased growth performance, high morbidity, and mortality have been noticed to occur with PWND [48]. However, the mechanism between protein fermentation and the gastrointestinal tract (GIT) is still unknown. Some studies showed that a high-protein diet led to a higher incidence of PWND [6, 35]. Interestingly, an increase in ammonia concentration has a detrimental effect on the health of the GIT and a negative effect on the growth and differentiation of intestinal epithelial cells [49, 50]. Additionally, BCFAs and ammonia are toxic metabolites for the intestinal mucosa and most likely trigger PWND and the poor performance in piglets [39, 51, 52]. More importantly, the upregulated expression of ammonia may induce a disorder of the intestinal microbial balance during weaning [20]. Additionally, the initially predominant lactobacilli decrease in number during weaning, leading to the downregulation of the GIT immunity and the formation of short chain fatty acids (SCFAs) [53]. More importantly, piglets fed a high-protein diet experience a high buffering capacity [54], an increase in the small intestinal pH [26], and a decrease in the expression of SCFAs, mainly butyrate, which probably permit a quick recovery of the intestinal epithelium, reducing the incidence and severity of PWND [55].

In summary, a high-protein diet increases the expression of BCFAs and ammonia, which can promote the growth of pathogenic bacteria, while a low-protein diet promises an increase in the expression of SCFAs, which may result in the establishment of beneficial microbes [56, 57]. Therefore, with a low-protein diet, beneficial bacteria rapidly proliferate and occupy the binding sites on the intestinal mucosa that could otherwise be occupied by pathogenic bacteria [58]. These differences between protein levels may reduce the incidence and severity of PWND and improve the growth performance of piglets [3]. Thus, it can be concluded that choosing a low-protein diet to feed postweaned piglets may be an effective way to decrease PWND incidence [3] (Figure 1).

3. The Effect of Dietary Fibre on PWND

Fermentable carbohydrates constitute the major energy source for microbial fermentation and therefore may act as a link between the piglet and its enteric commensal microbiota [59, 60]. Furthermore, dietary fibre may be beneficial for gut health and decreases diarrhea incidence in pigs [61, 62]. And significant effect on diarrhea incidence was observed in the pigs fed the fibre source diet compared with the pigs fed the control diet [63, 64]. A difference in diarrhea incidence was observed among the different sources of fibre diets [60].

3.1. The Effect of Dietary Fibre on Growth Performance and Digestibility of Nutrients of Weaned Piglets

Adding fibre in the daily diet could improve the adaptation of the pigs during the weaning period [64]. Depending on the kinds of fibrous ingredients, the effects of feeding high-fibre diets on the performance of the piglets differed [62, 63]. The impact of dietary fibre on piglets’ nutrition might be determined by the properties of fibre and/or fibre sources [65, 66]. For example, the fibre in the wheat bran diet was adapted by piglets and acted as prebiotics [60]. Wheat bran is a kind of insoluble fibre and when added to the weaned piglets’ diet, it appears that it is related to a higher feed intake and development of the gastrointestinal tract [67, 68]. More research is necessary to clarify the effects of the dietary fibre composition on the growth performance of weaned piglets.

3.2. The Effect of Dietary Fibre on the Gut Health of Weaned Piglets

In consideration of intestinal bacteria, fibre diets influenced the health of piglets around the time of weaning [69, 70]. Previous studies showed that a lower villus height: crypt depth ratio is associated with microbial challenges and antigenic components of the feed [71, 72]. Moreover, a study of intestinal mucosal morphology was used to evaluate the surface area of the intestine undertaken for mucosal integrity [73, 74]. Adding wheat bran fibre to the daily feed elevated the ileal mucosal integrity by improving the ileum villus height and the villus height: crypt depth ratio, which is in agreement with previous findings that showed that feeding high-insoluble-fibre diets protected against pathogenic bacteria by increasing the villus length [75, 76]. Furthermore, research has shown that piglets fed soluble and insoluble dietary fibre had more goblet cells in the ileum than did fibre-free piglets [77, 78]. The goblet cells played an important role in the intestine by synthesizing and secreting several mediators, mainly found in the small and large intestine, that were resistant to proteolytic digestion and stimulated the repair process, such as mucin and peptide trefoil factors [24, 79]. Studies suggested that piglets fed a fibre diet had a higher TGF-α concentration in their colons than that of other fibre-free groups [80]. Altogether, a fibre diet could improve the intestinal barrier function by increasing the concentration of factors associated with intestinal barrier function. However, different dietary fibre compositions induce different changes in the intestinal bacteria [81, 82].

3.3. The Effect of Dietary Fibre on the Incidence of PWND

Dietary fibre has been reported to improve gut health and decrease the diarrhea incidence in pigs [61, 83]. A wheat bran diet has been shown to decrease the amount of pathogenic E. coli in the feces and reduce the incidence of PWND [61, 84]. It is reported that a pea fibre diet could improve the intestinal health in animals by reducing the adhesion and increasing the excretion of enterotoxigenic E. coli, and such a diet could reduce the incidence of PWND as well [85]. However, the effect of a fibre diet on the incidence of diarrhea was not observed between the piglets fed fibre diets and the control group. However, a difference in diarrhea incidence was observed among the fibre source diets [64, 86]. The mechanism of the effects of the dietary fibre source on the incidence of diarrhea in weaned piglets may result from the inconsistent intestinal function in regulating intestinal bacteria [87]. Previous studies have shown that feeding weaned piglets high-insoluble-fibre diets might better protect them against pathogenic bacteria by increasing the villus length [85, 88]. The intestinal barrier integrity reflects the paracellular space between epithelial cells and may prevent the paracellular diffusion of intestinal bacteria across the epithelium [89]. Additionally, tight junction proteins play a key role in intestinal barrier integrity [90]. The probiotic Lactobacillus can increase occludin gene mRNA levels of Caco-2 cells, and E. coli decreases the levels of ZO-1, occludin, and claudin-1 tight junction complex in the epithelial cells, proving that bacteria affect the integrity of the intestinal barrier by regulating the gene expression level of tight junction proteins [91, 92]. The effect of fibre on tight junction proteins is associated with the number of bifidobacteria and lactobacilli [93]. Fibre in the diets has also promoted intestinal proinflammatory cytokine (IL-1 and TNF-α) mRNA levels as interference factors of the intestinal barrier [94, 95]. However, more research between PWND and intestinal bacteria alterations mediated by fibre in the diet must be done.

Complex fibre sources could affect the intestinal mucosal barrier function and regulate intestinal bacteria in weaning piglets. Additionally, fibre composition is considered to be an important factor affecting the intestinal barrier function in piglets and could induce the incidence of PWND (Figure 2).

4. The Effect of Dietary Electrolyte Balance on PWND

4.1. Dietary Electrolyte Absorption in the Intestine

The intestinal lumen accepts 8–10 L/day of fluid, containing ingested food and biological secretions. The small intestine absorbs the highest percentage of this fluid content, and the last 1.5–1.9 L of the fluid is absorbed by the large intestine [96]. Otherwise, <0.1–0.2 L/d of the fluid content is excreted in the feces in an abnormal condition [97]. However, piglets around the time of weaning suffer a significant reduction in the colon absorptive capacity, leading to diarrhea [98, 99].

Electroneutral sodium chloride in the intestine is absorbed by luminal Na⁺/H⁺ and Cl^–/HCO^– exchangers [100, 101]. The remaining absorption of sodium chloride is due to transcellular or paracellular absorption of Cl^– [102]. Na⁺/H⁺ and Cl^–/HCO^– exchangers in luminal brush-border membranes of the colonic epithelial cells are required to absorb sodium chloride [103]. This process is driven by the action of the Na⁺-K⁺-ATPase and is regulated by Na⁺ depletion [104, 105].

The Na⁺/H⁺ exchangers play a key role in Na⁺ and water absorption and the maintenance of intracellular pH and cell volume [106]. Eight types of Na⁺/H⁺ exchangers named NHE have been defined in the intestinal epithelium. In the intestine, NHE1 (SLC9A1), NHE2 (SLC9A2), NHE3 (SLC9A3), and NHE8 (SLC9A8) have been shown to be present in the intestinal epithelium [105, 107]. NHE1 (SLC9A1) is expressed in the basolateral membrane of the intestinal epithelial cells, is not affected by Na⁺ depletion, and does not contribute to luminal ion and water absorption [108, 109]. NHE2 (SLC9A2) and NHE3 (SLC9A3) are both expressed in the intestinal epithelium, with a larger contribution of NHE3 (SLC9A3) to Na⁺ absorption under control conditions [110]. Otherwise, NHE3 (SLC9A3) is reported as the main transporter for Na⁺ absorption in the intestine [97, 111]. NHE3 (SLC9A3)-knockout mice had reduced intestinal Na⁺ and water absorption and induced diarrhea [112, 113]. Na⁺/H⁺ exchange occurs in both surface and crypt epithelium and might be affected by CFTR Cl^– channels [114, 115]. However, the exact impact of CFTR Cl^– channels on the regulation of Na⁺/H⁺ exchange in the small intestine is not clear.

In mammalian intestinal epithelial cells, two types of SLC26 gene families, named DRA (SLC26A3) and PAT-1 (putative anion transporter, SLC26A6), have been identified as representing apical Cl^–/HCO₃^– exchangers [116, 117]. DRA is predominantly expressed in the colon and duodenum, whereas PAT-1 is mainly expressed in the jejunum and ileum [118, 119]. DRA mutations have been found to induce severe diarrhea, massive loss of Cl^– in stools, and metabolic alkalosis as well as serum electrolyte imbalance [120, 121]. PAT-1-knockout mice did not present this diarrhea phenotype [122]. In addition, similar to NHE3, a Cl^–/HCO₃^– exchange is also controlled by CFTR in the colonic epithelium [123, 124]. Taken together, the current studies indicate a regulation of both Na⁺/H⁺ and Cl^–/HCO₃^– exchangers by CFTR, which therefore play an important role in the electroneutral absorption of sodium chloride and regulation of cellular and mucosal pH in the animal gastrointestinal tract [117, 125, 126].

4.2. The Effect of Dietary Electrolyte Balance on the Growth Performance of Weaned Piglets

The animal industry is always concerned about minerals in feed, such as calcium (limestone), phosphorus (calcium phosphate), and sodium and chloride (salt and sodium bicarbonate) [127, 128]. Animal feed adds minerals not only to satisfy the mineral requirements but also to modify the dietary electrolyte balance (EB) [129]. The balance between cation (Na+) and anions (K⁺/Cl^–) and the acid or alkaline load from the diet may strongly alter the acid-base status and growth performance of weaned piglets [130, 131]. It is reported that an excess of chloride ions induces a negative dietary EB and reduces the growth performance of weaned piglets [132–134]. In short, a dietary addition of minerals in postweaning diets, such as calcium chloride and sodium bicarbonate, could affect the EB and significantly alter the feeding behavior, apparent digestibility, and productive performance of postweaned piglets. Additionally, piglets showed a bias toward low-EB diets, which optimized their performance more so than that for high-EB diets [130, 135].

4.3. The Effect of Dietary Electrolyte Balance on the Incidence of PWND

Enteric pathogens have been proven to stimulate intestinal secretion of electrolytes and water [136, 137]. In most species, dietary electrolyte balance may be expressed as Na⁺/H⁺ and Cl^–/HCO₃^– and has been influenced by proportions of monovalent mineral cations and anions [138, 139]. Electrolyte balance plays a critical role in intestinal phenotype and function [140]. The disorder of daily electrolyte balance after weaning makes a large contribution to postweaning diarrhea, induces severe intestinal electrolyte turbulence, and negatively affects the piglets’ growth performance after weaning through excessive loss of salt and water [130, 133]. The gastrointestinal tract exhibits segmental heterogeneity in the various ion transporters and channels in the postweaning period, which play a control role in conjunction and determine the electrolyte content and fluid volume in the lumen. In basic situation, the reason of PWND is the imbalance between the absorption and secretion of ions and solutes across the gut epithelium [141]. This imbalance of electrolytes in the digestive tract of piglets is induced by the presence of bacteria that could deliver toxins into the gut and disturb the development of the epithelium [142]. The enteric pathogens spread rapidly and cause infection in the piglets’ intestines [143]. This situation results in the formation of watery feces, or PWND, in combination with reduced growth performance, morbidity, and even mortality of postweaning piglets.

In principle, the processes that result in induced PWND are proposed as follows. First, postweaning diets contain unabsorbed solutes that exert an osmotic force pulling water and electrolytes into the intestinal lumen [144, 145]. Second, the syndromes result in villus atrophy and crypt hypertrophy, thereby adversely altering the balance of absorption and secretion [146, 147]. Lastly, active secretion is stimulated by unabsorbed dihydroxy bile acid and fatty acid [148]. The altered bile acid and fatty acid transport themselves into the lipid phase of the plasma membrane [149, 150]. Then, the excess fecal water from the decreased intestinal absorption and the increased intestinal secretion is the reason for diarrhea [151, 152]. Generally, the electrolyte imbalance in postweaning diets exhibited alterations in motility, changes in paracellular permeability, loss of absorption surface, a change in electrolyte fluxes in postweaning piglets and, finally, induced PWND [153–155] (Figure 3).

5. The Effect of Dietary Starch Content on PWND

Starch is the main carbohydrate source of animal diets and the main energy source required for both animals and humans [156, 157]. It is composed of two types of a-glucan polymers: amylose and amylopectin [158, 159]. Starch has been proven to have a significant effect on the composition and activity of the intestinal microflora, through an improvement of the growth of beneficial bacteria and a reduction in the development of pathogenic bacteria in the intestines [160, 161]. Based on the digestible capacity, starches could be classified into rapidly digestible starch (RDS), slowly digestible starch (SDS), and resistant starch (RS) [162, 163]. RS cannot be absorbed in the small intestine, but it passes to the large bowel and beneficially modifies the gut microbial populations [164, 165].

5.1. The Effect of Resistant Starch Source on the Intestine Digestive Ability and Function of Postweaning Piglets

To ameliorate PWND and improve the gastrointestinal function of piglets, one useful alternative is to use a dietary prebiotic material, such as RS [166, 167]. The properties of prebiotics such as RS can act as indigestible carbohydrate substrates for cecal and colonic microbiota that influence the host gut health, as shown in animal and human studies [161, 166]. Starch digestion begins in the mouth. The enzyme α-amylase begins to digest starch to oligosaccharides and maltose. Starch does not digest in the stomach but is transported to the small intestine and broken down to glucose and maltose by pancreatic amylase [161, 168]. Then, the small intestine absorbs glucose by active transport, with the residual part being passively diffused through the villi [169, 170]. Starch digestion is influenced by many factors, such as the presence of lipids, proteins, and minerals, the amylose to amylopectin ratio, and digestion conditions [171, 172]. RS starts to be fermented in the large bowel by colonic microflora and then is digested into hydrogen, methane, and short-chain fatty acids (SCFAs), such as acetic, propionic, and butyric acid [173]. In addition, it is said that the concentration of SCFAs is significantly increased in the large intestine after RS consumption [174, 175]. SCFAs play a positive role in colonic muscles and the absorption of calcium, magnesium, and water, and they also positively stimulate the colonic microflora [176, 177]. According to one experiment, a lower level of RS in the diet will decrease the growth challenge seen in postweaning piglets [178]. It is likely that piglets fed diets containing a higher level of RS (14%) exhibited more undigested starch in the ileum compared with that for piglets fed a diet without added RS [179]. It is reported that RS could be hydrolyzed by several Bifidobacterium strains, such as B. adolescentis, B. bifidum, B. breve, B. infantis, B. lactis, and B. longum [180]. In short, the beneficial effects of RS in the large bowel appear mainly because of the appearance of SCFAs formed by the previously mentioned bacterial fermentation [181]. Colonic bacteria ferment RS to SCFAs, mainly acetate, propionate, and butyrate, and benefit the large bowel of the postweaning piglet [166, 182].

5.2. The Effect of Resistant Starch Source on the Incidence of PWND

According to the existing research, a diet containing 7% resistant potato starch reduced the PWND incidence compared to that with a diet containing 14% resistant potato starch [178]. In addition, a diet containing 0.5 or 1.0% of resistant potato starch reduced the incidence of PWND and improved the growth performance in weaning piglets [169]. As we mentioned before, the concentration of SCFAs significantly increases in the large intestine after RS consumption [183]. In contrast, the molar proportion of BCFAs decreases. All of these results occurred because of the greater amounts of substrates available for carbohydrate-utilizing microbiota in the colons of pigs fed diets containing RS [184]. BCFAs are a harmful fermentation product and are a predisposing factor for PWND as well [185]. In addition, RS diets in piglets have a sharp reduction in ileal and cecal digesta pH [186]. According to what we know, bacteria ferment organic matter in the large intestine, including RS to SCFAs, and therefore reduce the pH in the GIT. There is a positive relationship between dietary intake of resistant starch and fecal output [187, 188]. Simply put, postweaning piglets fed a diet that includes a low level of RS leads to increases in the concentration of SCFAs, such as acetate, propionate, and butyrate, as well as the concentration of other terminal products, such as lactate, ethanol, succinate, carbon dioxide, hydrogen, and methane [165, 189]. The increasing SCFA levels decrease the gut pH; help raise gut motility; improve the absorption of nutrients, such as calcium, magnesium, and iron; and provide energy for the colonic epithelium and the host [190, 191]. Importantly, low-level RS diets decrease the concentrations of BCFAs, which are a harmful fermentation product as well as a predisposing factor for PWND [165, 192].

We learned that diets containing increased colonic fermentation associated with substrates such as RS also have striking effects on the composition of the gut microflora in order to increase the bacteria populations that are helpful to the bowel and decrease the bacteria populations that are harmful for a healthy large intestine [193, 194]. According to a previous study, lactobacilli and bifidobacteria are considered beneficial and were found to increase in abundance in the cecum with RS diets [195]. Furthermore, a trial that used a diet with lactobacilli strains added decreased the duration and incidence of diarrhea [196]. In short, supplementing weaned pigs’ diets with at least 0.5% RS increased the populations of bacteria that are potentially good for the large intestines, such as lactobacilli and bifidobacteria [197], which in turn decreased the amount of bacteria that are harmful for a healthy bowel. Finally, the increase in good bacteria populations and the decrease in harmful bacteria populations resulted in a decreased incidence of diarrhea [198, 199] (Figure 4).

6. Conclusion

Weaning is a grand challenge in the swine industry, which frequently induces severe intestinal disorders and gut diseases, raising serious economic and public health concerns. In addition, the gut microbiota derangement induced by changes in the diet of piglets around the time of weaning is the most direct reason of PWND. Despite the progress in modern pig farms during the last decade to prevent infectious diseases and improve global animal health, PWND is still an event that causes significant economic losses in the pig industry. However, we have now learned that the key component that leads to PWND is the composition of the daily diets for postweaning piglets. As described herein, the percentage of protein, fibre, and RS in the diet as well as the electrolyte balance could influence the fermentation products, thus altering the gastrointestinal microbiota composition and, as a result, inducing the incidence of PWND. Clearly, we require well-controlled studies to better understand the impact of nutrition on the growth of piglets around weaning. Controlling the nutrition in the diets is the most promising strategy for the prevention of PWND. The interaction of nutrition along the intestinal tract and the influence it has on the host still must be defined further in order to formulate appropriate “healthy” pig diets.

Conflicts of Interest

The authors declare that there are no conflicts of interest.

Authors’ Contributions

All the authors contributed extensively to the work presented in this manuscript. JG mainly completed this review, performed the literature search, and wrote the manuscript. KX, JY, TL, and YY conceived the work and critically revised it. YY revised the manuscript.

Acknowledgments

This work was funded by the National Key R&D Program of China (2016YFD0501201), the Key Programs of Frontier Scientific Research of the Chinese Academy of Sciences (QYZDY-SSW-SMC008), the National Natural Science Foundation of China (31872371), the Key R&D Program of Hunan Province (2017NK2321), the Earmarked Fund for China Agriculture Research System (CARS-35), and the Hunan Provincial Science and Technology Department (2018TP1031).

References

J. Yin, M. M. Wu, H. Xiao et al., “Development of an antioxidant system after early weaning in piglets,” Journal of Animal Science, vol. 92, no. 2, pp. 612–619, 2014.
View at: Publisher Site | Google Scholar
T. M. Laine, T. Lyytikainen, M. Yliaho, and M. Anttila, “Risk factors for post-weaning diarrhoea on piglet producing farms in Finland,” Acta Veterinaria Scandinavica, vol. 50, p. 21, 2008.
View at: Publisher Site | Google Scholar
J. M. Heo, J. C. Kim, J. Yoo, and J. R. Pluske, “A between-experiment analysis of relationships linking dietary protein intake and post-weaning diarrhea in weanling pigs under conditions of experimental infection with an enterotoxigenic strain of Escherichia coli,” Animal Science Journal, vol. 86, no. 3, pp. 286–293, 2015.
View at: Publisher Site | Google Scholar
J. M. Campbell, J. D. Crenshaw, and J. Polo, “The biological stress of early weaned piglets,” Journal of Animal Science and Biotechnology, vol. 4, no. 1, p. 19, 2013.
View at: Publisher Site | Google Scholar
J. M. Heo, F. O. Opapeju, J. R. Pluske, J. C. Kim, D. J. Hampson, and C. M. Nyachoti, “Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds,” Journal of Animal Physiology and Animal Nutrition, vol. 97, no. 2, pp. 207–237, 2013.
View at: Publisher Site | Google Scholar
J. Kluess, U. Schoenhusen, W. B. Souffrant, P. H. Jones, and B. G. Miller, “Impact of diet composition on ileal digestibility and small intestinal morphology in early-weaned pigs fitted with a T-cannula,” Animal, vol. 4, no. 4, pp. 586–594, 2010.
View at: Publisher Site | Google Scholar
F. H. M. Aherne, E. T. Kornegay, G. C. Shurson et al., Management and Nutrition of the Newly Weaned Pig, National Pork Producers Council, Des Moines, IA, USA, 1992.
W. Zhou, K. Ullman, V. Chowdry et al., “Molecular investigations on the prevalence and viral load of enteric viruses in pigs from five European countries,” Veterinary Microbiology, vol. 182, pp. 75–81, 2016.
View at: Publisher Site | Google Scholar
G. Guan, S. Ding, Y. Yin, V. Duraipandiyan, NA. Al-Dhabi, and G. Liu, “Macleaya cordata extract alleviated oxidative stress and altered innate immune response in mice challenged with enterotoxigenic Escherichia coli,” Science China Life Sciences, vol. 62, pp. 1019–1027, 2019.
View at: Google Scholar
A. G. Atasever, P. E. Ozcan, K. Kasali, T. Abdullah, G. Orhun, and E. Senturk, “The frequency, risk factors, and complications of gastrointestinal dysfunction during enteral nutrition in critically ill patients,” Therapeutics and Clinical Risk Management, vol. 14, pp. 385–391, 2018.
View at: Publisher Site | Google Scholar
J. R. Pluske, D. W. Pethick, D. E. Hopwood, and D. J. Hampson, “Nutritional influences on some major enteric bacterial diseases of pig,” Nutrition Research Reviews, vol. 15, no. 2, pp. 333–371, 2002.
View at: Publisher Site | Google Scholar
J.-P. Lallès, P. Bosi, H. Smidt, and C. R. Stokes, “Nutritional management of gut health in pigs around weaning,” Proceedings of the Nutrition Society, vol. 66, no. 2, pp. 260–268, 2007.
View at: Publisher Site | Google Scholar
X. Ma, P. Fan, L. S. Li, S. Y. Qiao, G. L. Zhang, and D. F. Li, “Butyrate promotes the recovering of intestinal wound healing through its positive effect on the tight junctions1,” Journal of Animal Science, vol. 90, no. 4, pp. 266–268, 2012.
View at: Publisher Site | Google Scholar
B. Jayaraman and C. M. Nyachoti, “Husbandry practices and gut health outcomes in weaned piglets: a review,” Animal Nutrition, vol. 3, no. 3, pp. 205–211, 2017.
View at: Publisher Site | Google Scholar
T. D. Leser, J. Z. Amenuvor, T. K. Jensen, R. H. Lindecrona, M. Boye, and K. Moller, “Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited,” Applied and Environmental Microbiology, vol. 68, no. 2, pp. 673–690, 2002.
View at: Publisher Site | Google Scholar
J. Gao, K. Xu, H. Liu et al., “Impact of the gut microbiota on intestinal immunity mediated by tryptophan metabolism,” Frontiers in Cellular and Infection Microbiology, vol. 8, p. 13, 2018.
View at: Publisher Site | Google Scholar
M. R. A. J. Bedford, Microbial Interactions in the Response to Exogenous Enzyme Utilization, Wallingford, UK, 2001.
E. Bauer, B. A. Williams, H. Smidt, R. Mosenthin, and M. W. A. Verstegen, “Influence of dietary components on development of the microbiota in single-stomached species,” Nutrition Research Reviews, vol. 19, no. 1, pp. 63–78, 2006.
View at: Publisher Site | Google Scholar
G. Wu, “Dietary protein intake and human health,” Food and Function, vol. 7, no. 3, pp. 1251–1265, 2016.
View at: Publisher Site | Google Scholar
V. T. S. Rist, E. Weiss, N. Sauer, R. Mosenthin, and M. Eklund, “Effect of dietary protein supply originating from soybean meal or casein on the intestinal microbiota of piglets,” Anaerobe, vol. 25, pp. 72–79, 2014.
View at: Publisher Site | Google Scholar
C. Mu, L. Zhang, X. He, H. Smidt, and W. Zhu, “Dietary fibres modulate the composition and activity of butyrate-producing bacteria in the large intestine of suckling piglets,” Antonie Van Leeuwenhoek, vol. 110, no. 5, pp. 687–696, 2017.
View at: Publisher Site | Google Scholar
G.-Q. Han, Z.-T. Xiang, B. Yu et al., “Effects of different starch sources on Bacillus spp. in intestinal tract and expression of intestinal development related genes of weanling piglets,” Molecular Biology Reports, vol. 39, no. 2, pp. 1869–1876, 2012.
View at: Publisher Site | Google Scholar
H. A. Merchant, E. L. McConnell, F. Liu et al., “Assessment of gastrointestinal pH, fluid and lymphoid tissue in the Guinea pig, rabbit and pig, and implications for their use in drug development,” European Journal of Pharmaceutical Sciences, vol. 42, no. 1-2, pp. 3–10, 2011.
View at: Publisher Site | Google Scholar
B. Deplancke and H. R. Gaskins, “Microbial modulation of innate defense: goblet cells and the intestinal mucus layer,” The American Journal of Clinical Nutrition, vol. 73, no. 6, pp. 1131S–1141S, 2001.
View at: Publisher Site | Google Scholar
Y. Ji, X. Kong, H. Li, Q. Zhu, Q. Guo, and Y. Yin, “Effects of dietary nutrient levels on microbial community composition and diversity in the ileal contents of pregnant Huanjiang mini-pigs,” PLoS One, vol. 12, no. 2, Article ID e0172086, 2017.
View at: Publisher Site | Google Scholar
J. K. Htoo, B. A. Araiza, W. C. Sauer et al., “Effect of dietary protein content on ileal amino acid digestibility, growth performance, and formation of microbial metabolites in ileal and cecal digesta of early-weaned pigs,” Journal of Animal Science, vol. 85, no. 12, pp. 3303–3312, 2007.
View at: Publisher Site | Google Scholar
I. J. Wellock, P. D. Fortomaris, J. G. Houdijk, and I. Kyriazakis, “Effects of dietary protein supply, weaning age and experimental enterotoxigenic Escherichia coli infection on newly weaned pigs: health,” Animal, vol. 2, pp. 834–842, 2008.
View at: Publisher Site | Google Scholar
F. O. Opapeju, D. O. Krause, R. L. Payne, M. Rademacher, and C. M. Nyachoti, “Effect of dietary protein level on growth performance, indicators of enteric health, and gastrointestinal microbial ecology of weaned pigs induced with postweaning colibacillosis1,2,” Journal of Animal Science, vol. 87, no. 8, pp. 2635–2643, 2009.
View at: Publisher Site | Google Scholar
R. Pieper, C. Villodre Tudela, M. Taciak, J. Bindelle, J. F. Pérez, and J. Zentek, “Health relevance of intestinal protein fermentation in young pigs,” Animal Health Research Reviews, vol. 17, no. 2, pp. 137–147, 2016.
View at: Publisher Site | Google Scholar
K. Qiu, X. Zhang, N. Jiao et al., “Dietary protein level affects nutrient digestibility and ileal microbiota structure in growing pigs,” Animal Science Journal, vol. 89, no. 3, pp. 537–546, 2018.
View at: Publisher Site | Google Scholar
J. Yin, W. Ren, X. Huang, T. Li, and Y. Yin, “Protein restriction and cancer,” Biochimica et Biophysica Acta (BBA)-Reviews on Cancer, vol. 1869, no. 2, pp. 256–262, 2018.
View at: Publisher Site | Google Scholar
G. Wu, F. W. Bazer, Z. Dai, D. Li, J. Wang, and Z. Wu, “Amino acid nutrition in animals: protein synthesis and beyond,” Annual Review of Animal Biosciences, vol. 2, no. 1, pp. 387–417, 2014.
View at: Publisher Site | Google Scholar
R. Gresse, F. Chaucheyras-Durand, M. A. Fleury, T. Van de Wiele, E. Forano, and S. Blanquet-Diot, “Gut microbiota dysbiosis in postweaning piglets: understanding the keys to health,” Trends in Microbiology, vol. 25, no. 10, pp. 851–873, 2017.
View at: Publisher Site | Google Scholar
V. T. S. Rist, E. Weiss, M. Eklund, and R. Mosenthin, “Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: a review,” Animal, vol. 7, no. 7, pp. 1067–1078, 2013.
View at: Publisher Site | Google Scholar
P. Bikker, A. Dirkzwager, J. Fledderus et al., “The effect of dietary protein and fermentable carbohydrates levels on growth performance and intestinal characteristics in newly weaned piglets1,” Journal of Animal Science, vol. 84, no. 12, pp. 3337–3345, 2006.
View at: Publisher Site | Google Scholar
P. Porter and R. Kenworthy, “A study of intestinal and urinary amines in pigs in relation to weaning,” Research in Veterinary Science, vol. 10, no. 5, pp. 440–447, 1969.
View at: Publisher Site | Google Scholar
M. S. Riaz Rajoka, J. Shi, H. M. Mehwish et al., “Interaction between diet composition and gut microbiota and its impact on gastrointestinal tract health,” Food Science and Human Wellness, vol. 6, no. 3, p. 10, 2017.
View at: Publisher Site | Google Scholar
J. Zhao, X. Zhang, H. Liu, M. A. Brown, and S. Qiao, “Dietary protein and Gut microbiome composition and function,” Current Protein and Peptide Science, vol. 20, no. 2, pp. 145–154, 2019.
View at: Publisher Site | Google Scholar
B. A. Williams, M. W. Bosch, A. Awati et al., “In vitro assessment of gastrointestinal tract (GIT) fermentation in pigs: fermentable substrates and microbial activity,” Animal Research, vol. 54, no. 3, pp. 191–201, 2005.
View at: Publisher Site | Google Scholar
G. T. MSaM, Proteolysis and Amino Acid Fermentation, CRC Press, Boca Raton, FL, USA, 1995.
G. Macfarlane, E. Beatty, and J. H. Cummings, “Estimation of short-chain fatty acid production from protein by human intestinal bacteria based on branched-chain fatty acid measurements,” FEMS Microbiology Letters, vol. 101, no. 2, pp. 81–88, 1992.
View at: Publisher Site | Google Scholar
H. M. Hamer, V. De Preter, K. Windey, and K. Verbeke, “Functional analysis of colonic bacterial metabolism: relevant to health?” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 302, no. 1, pp. G1–G9, 2012.
View at: Publisher Site | Google Scholar
H. Ichikawa and T. Sakata, “Stimulation of epithelial cell proliferation of isolated distal colon of rats by continuous colonic infusion of ammonia or short-chain fatty acids is nonadditive,” The Journal of Nutrition, vol. 128, no. 5, pp. 843–847, 1998.
View at: Publisher Site | Google Scholar
R. Pieper, S. Kröger, J. F. Richter et al., “Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets,” The Journal of Nutrition, vol. 142, no. 4, pp. 661–667, 2012.
View at: Publisher Site | Google Scholar
N. Ijssennagger, C. Belzer, G. J. Hooiveld et al., “Gut microbiota facilitates dietary heme-induced epithelial hyperproliferation by opening the mucus barrier in colon,” Proceedings of the National Academy of Sciences, vol. 112, no. 32, pp. 10038–10043, 2015.
View at: Publisher Site | Google Scholar
C. D. Davis and J. A. Milner, “Gastrointestinal microflora, food components and colon cancer prevention,” The Journal of Nutritional Biochemistry, vol. 20, no. 10, pp. 743–752, 2009.
View at: Publisher Site | Google Scholar
Y. Wu, Z. Jiang, C. Zheng et al., “Effects of protein sources and levels in antibiotic-free diets on diarrhea, intestinal morphology, and expression of tight junctions in weaned piglets,” Animal Nutrition, vol. 1, no. 3, pp. 170–176, 2015.
View at: Publisher Site | Google Scholar
I. J. Wellock, P. D. Fortomaris, J. G. Houdijk, and I. Kyriazakis, “Effects of dietary protein supply, weaning age and experimental enterotoxigenic Escherichia coli infection on newly weaned pigs: performance,” Animal, vol. 2, pp. 825–833, 2008.
View at: Publisher Site | Google Scholar
H. R. Gaskins, Intestinal Bacteria and Their Influence on Swine Growth, CRC Press LLC, Boca Raton, FL, USA, 2001.
M. Ni Lochlainn, R. C. E. Bowyer, and C. J. Steves, “Dietary protein and muscle in aging people: the potential role of the gut microbiome,” Nutrients, vol. 10, 2018.
View at: Publisher Site | Google Scholar
R. G. Hermes, F. Molist, M. Ywazaki et al., “Effect of dietary level of protein and fiber on the productive performance and health status of piglets1,” Journal of Animal Science, vol. 87, no. 11, pp. 3569–3577, 2009.
View at: Publisher Site | Google Scholar
K. E. García, T. C. R. de Souza, G. M. Landín, A. A. Barreyro, M. G. B. Santos, and J. G. G. Soto, “Microbial fermentation patterns, diarrhea incidence, and performance in weaned piglets fed a low protein diet supplemented with probiotics,” Food and Nutrition Sciences, vol. 5, no. 18, pp. 1776–1786, 2014.
View at: Publisher Site | Google Scholar
B. Jensen, “The impact of feed additives on the microbial ecology of the gut in young pigs,” Journal of Animal and Feed Sciences, vol. 7, pp. 45–64, 1998.
View at: Publisher Site | Google Scholar
K. H. Partanen and Z. Mroz, “Organic acids for performance enhancement in pig diets,” Nutrition Research Reviews, vol. 12, no. 1, pp. 117–145, 1999.
View at: Publisher Site | Google Scholar
D. G. Burrin, Y. Petersen, B. Stoll, and P. Sangild, “Glucagon-like peptide 2: a nutrient-responsive gut growth factor,” The Journal of Nutrition, vol. 131, no. 3, pp. 709–712, 2001.
View at: Publisher Site | Google Scholar
B. A. Williams, M. W. A. Verstegen, and S. Tamminga, “Fermentation in the large intestine of single-stomached animals and its relationship to animal health,” Nutrition Research Reviews, vol. 14, no. 2, pp. 207–227, 2001.
View at: Publisher Site | Google Scholar
N. Ma, Y. Tian, Y. Wu, and X. Ma, “Contributions of the interaction between dietary protein and gut microbiota to intestinal health,” Current Protein and Peptide Science, vol. 18, pp. 795–808, 2017.
View at: Publisher Site | Google Scholar
T. Anthony, T. Rajesh, N. Kayalvizhi, and P. Gunasekaran, “Influence of medium components and fermentation conditions on the production of bacteriocin(s) by Bacillus licheniformis AnBa9,” Bioresource Technology, vol. 100, no. 2, pp. 872–877, 2009.
View at: Publisher Site | Google Scholar
L. Zhang, C. Mu, X. He et al., “Effects of dietary fibre source on microbiota composition in the large intestine of suckling piglets,” FEMS Microbiology Letters, vol. 363, no. 14, 2016.
View at: Publisher Site | Google Scholar
H. Chen, X. Mao, J. He et al., “Dietary fibre affects intestinal mucosal barrier function and regulates intestinal bacteria in weaning piglets,” British Journal of Nutrition, vol. 110, no. 10, pp. 1837–1848, 2013.
View at: Publisher Site | Google Scholar
F. Molist, A. G. de Segura, J. Gasa et al., “Effects of the insoluble and soluble dietary fibre on the physicochemical properties of digesta and the microbial activity in early weaned piglets,” Animal Feed Science and Technology, vol. 149, no. 3-4, pp. 346–353, 2009.
View at: Publisher Site | Google Scholar
F. Molist, M. van Oostrum, J. F. Pérez, G. G. Mateos, C. M. Nyachoti, and P. J. van der Aar, “Relevance of functional properties of dietary fibre in diets for weanling pigs,” Animal Feed Science and Technology, vol. 189, pp. 1–10, 2014.
View at: Publisher Site | Google Scholar
C. Yu, S. Zhang, Q. Yang et al., “Effect of high fibre diets formulated with different fibrous ingredients on performance, nutrient digestibility and faecal microbiota of weaned piglets,” Archives of Animal Nutrition, vol. 70, no. 4, pp. 263–277, 2016.
View at: Publisher Site | Google Scholar
P. Superchi, R. Saleri, P. Borghetti et al., “Effects of a dietary crude fibre concentrate on growth in weaned piglets,” Animal, vol. 11, no. 11, pp. 1905–1912, 2017.
View at: Publisher Site | Google Scholar
J. E. Lindberg, “Fiber effects in nutrition and gut health in pigs,” Journal of Animal Science and Biotechnology, vol. 5, p. 15, 2014.
View at: Publisher Site | Google Scholar
R. Jha and J. D. Berrocoso, “Review: dietary fiber utilization and its effects on physiological functions and gut health of swine,” Animal, vol. 9, no. 9, pp. 1441–1452, 2015.
View at: Publisher Site | Google Scholar
H. Chen, W. Wang, J. Degroote et al., “Arabinoxylan in wheat is more responsible than cellulose for promoting intestinal barrier function in weaned male piglets,” The Journal of Nutrition, vol. 145, no. 1, pp. 51–58, 2015.
View at: Publisher Site | Google Scholar
H. D. Holscher, “Dietary fiber and prebiotics and the gastrointestinal microbiota,” Gut Microbes, vol. 8, no. 2, pp. 172–184, 2017.
View at: Publisher Site | Google Scholar
K. Schedle, C. Plitzner, T. Ettle, L. Zhao, K. J. Domig, and W. Windisch, “Effects of insoluble dietary fibre differing in lignin on performance, gut microbiology, and digestibility in weanling piglets,” Archives of Animal Nutrition, vol. 62, no. 2, pp. 141–151, 2008.
View at: Publisher Site | Google Scholar
T. S. Nielsen, H. Jørgensen, K. E. B. Knudsen, and H. N. Lærke, “The microbial fermentation characteristics depend on both carbohydrate source and heat processing: a model experiment with ileo-cannulated pigs,” International Journal of Food Sciences and Nutrition, vol. 68, no. 7, pp. 811–820, 2017.
View at: Publisher Site | Google Scholar
C. W. Huang, T. T. Lee, Y. C. Shih, and B. Yu, “Effects of dietary supplementation of Chinese medicinal herbs on polymorphonuclear neutrophil immune activity and small intestinal morphology in weanling pigs,” Journal of Animal Physiology and Animal Nutrition, vol. 96, no. 2, pp. 285–294, 2012.
View at: Publisher Site | Google Scholar
W. Ren, P. Wang, J. Yan et al., “Melatonin alleviates weanling stress in mice: involvement of intestinal microbiota,” Journal of Pineal Research, vol. 64, no. 2, Article ID e12448, 2018.
View at: Publisher Site | Google Scholar
J. Wang, L. Zeng, B. Tan et al., “Developmental changes in intercellular junctions and Kv channels in the intestine of piglets during the suckling and post-weaning periods,” Journal of Animal Science and Biotechnology, vol. 7, no. 1, 2016.
View at: Publisher Site | Google Scholar
L. Montagne, G. Boudry, C. Favier, I. L. Huërou-Luron, J.-P. Lallès, and B. Sève, “Main intestinal markers associated with the changes in gut architecture and function in piglets after weaning,” British Journal of Nutrition, vol. 97, no. 1, pp. 45–57, 2007.
View at: Publisher Site | Google Scholar
M. S. Hedemann, M. Eskildsen, H. N. Lærke et al., “Intestinal morphology and enzymatic activity in newly weaned pigs fed contrasting fiber concentrations and fiber properties1,” Journal of Animal Science, vol. 84, no. 6, pp. 1375–1386, 2006.
View at: Publisher Site | Google Scholar
T. Fukunaga, M. Sasaki, Y. Araki et al., “Effects of the soluble fibre pectin on intestinal cell proliferation, fecal short chain fatty acid production and microbial population,” Digestion, vol. 67, no. 1-2, pp. 42–49, 2003.
View at: Publisher Site | Google Scholar
S. B. J. A. Kirk, R. Mohammad et al., “Modulation of intestinal goblet cell function during infection by an attaching and effacing bacterial pathogen,” Infection and Immunity, vol. 76, no. 2, pp. 796–811, 2008.
View at: Google Scholar
H. N. T. Shingo, S. Kei et al., “Small intestinal goblet cell proliferation induced by ingestion of soluble and insoluble dietary fiber is characterized by an increase in sialylated mucins in rats,” The Journal of Nutrition, vol. 142, pp. 1429–1436, 2012.
View at: Publisher Site | Google Scholar
J. P. Raymond, S. Ghosh, and A. Mahmood, “Growth factors and trefoil peptides in gastrointestinal health and disease,” Current Opinion in Pharmacology, vol. 4, no. 6, pp. 567–571, 2004.
View at: Publisher Site | Google Scholar
T. M. Holling, E. Schooten, and P. J. van Den Elsen, “Function and regulation of MHC class II molecules in T-lymphocytes: of mice and men,” Human Immunology, vol. 65, no. 4, pp. 282–290, 2004.
View at: Publisher Site | Google Scholar
B. U. Metzler-Zebeli, S. Hooda, R. Pieper et al., “Nonstarch polysaccharides modulate bacterial microbiota, pathways for butyrate production, and abundance of pathogenic Escherichia coli in the pig gastrointestinal tract,” Applied and Environmental Microbiology, vol. 76, no. 11, pp. 3692–3701, 2010.
View at: Google Scholar
H. Chen, D. Chen, J. Michiels, and S. De Smet, “Dietary fiber affects intestinal mucosal barrier function by regulating intestinal bacteria in weaning piglets,” Communications in Agricultural and Applied Biological Sciences, vol. 78, pp. 71–78, 2013.
View at: Google Scholar
I. J. Wellock, P. D. Fortomaris, J. G. M. Houdijk, J. Wiseman, and I. Kyriazakis, “The consequences of non-starch polysaccharide solubility and inclusion level on the health and performance of weaned pigs challenged with enterotoxigenic Escherichia coli,” British Journal of Nutrition, vol. 99, no. 3, pp. 520–530, 2008.
View at: Publisher Site | Google Scholar
H. L. Simpson and B. J. Campbell, “Review article: dietary fibre-microbiota interactions,” Alimentary Pharmacology & Therapeutics, vol. 42, no. 2, pp. 158–179, 2015.
View at: Publisher Site | Google Scholar
P. M. W. P. Becker, A. J. Jansman et al., “Pea dietary fiber for adhesion and excretion of enterotoxigenic E. coli K88 to prevent intestinal colonization,” Journal of Animal Science, vol. 87, pp. 172–189, 2009.
View at: Google Scholar
R. Zhao, Y. Wang, Y. Huang et al., “Effects of fiber and probiotics on diarrhea associated with enteral nutrition in gastric cancer patients,” Medicine, vol. 96, no. 43, p. e8418, 2017.
View at: Publisher Site | Google Scholar
A. Seidu, C. Dongsheng, Q. Guixin, J. Hailong, R. Han, and C. Tlotliso Sello, “Interactions of dietary fiber with nutritional components on gut microbial composition, function, and health in monogastrics,” Current Protein and Peptide Science, vol. 19, no. 10, pp. 1011–1023, 2018.
View at: Publisher Site | Google Scholar
J. W. McRorie Jr. and N. M. McKeown, “Understanding the physics of functional fibers in the gastrointestinal tract: an evidence-based approach to resolving enduring misconceptions about insoluble and soluble fiber,” Journal of the Academy of Nutrition and Dietetics, vol. 117, no. 2, pp. 251–264, 2017.
View at: Publisher Site | Google Scholar
K. Zhang, M. W. Hornef, and A. Dupont, “The intestinal epithelium as guardian of gut barrier integrity,” Cellular Microbiology, vol. 17, no. 11, pp. 1561–1569, 2015.
View at: Publisher Site | Google Scholar
S. M. Curry, K. J. Schwartz, K. J. Yoon, N. K. Gabler, and E. R. Burrough, “Effects of porcine epidemic diarrhea virus infection on nursery pig intestinal function and barrier integrity,” Veterinary Microbiology, vol. 211, pp. 58–66, 2017.
View at: Publisher Site | Google Scholar
B. P. Blackwood, C. Y. Yuan, D. R. Wood et al., “Integrity in experimental necrotizing enterocolitis,” Journal of Probiotics and Health, vol. 5, 2017.
View at: Google Scholar
M. C. Valenzano, K. DiGuilio, J. Mercado et al., “Remodeling of tight junctions and enhancement of barrier integrity of the CACO-2 intestinal epithelial cell layer by micronutrients,” PLoS One, vol. 10, Article ID e0133926, 2015.
View at: Publisher Site | Google Scholar
R. C. Anderson, A. L. Cookson, W. C. McNabb et al., “Lactobacillus plantarum MB452 enhances the function of the intestinal barrier by increasing the expression levels of genes involved in tight junction formation,” BMC Microbiology, vol. 10, no. 1, p. 316, 2010.
View at: Publisher Site | Google Scholar
M. Ogata, T. Ogita, H. Tari, T. Arakawa, and T. Suzuki, “Supplemental psyllium fibre regulates the intestinal barrier and inflammation in normal and colitic mice,” British Journal of Nutrition, vol. 118, no. 9, pp. 661–672, 2017.
View at: Publisher Site | Google Scholar
T. Chen, C. Y. Kim, A. Kaur et al., “Dietary fibre-based SCFA mixtures promote both protection and repair of intestinal epithelial barrier function in a Caco-2 cell model,” Food and Function, vol. 8, no. 3, pp. 1166–1173, 2017.
View at: Publisher Site | Google Scholar
H. J. Binder, “Mechanisms of diarrhea in inflammatory bowel diseases,” Annals of the New York Academy of Sciences, vol. 1165, no. 1, pp. 285–293, 2009.
View at: Publisher Site | Google Scholar
R. D. Gill, Mechanisms and Regulation of NaCl Absorption in the Human Intestine, Research Signpost, Thiruvananthapuram, India, 2003.
S. Priyamvada, R. Gomes, R. K. Gill, S. Saksena, W. A. Alrefai, and P. K. Dudeja, “Mechanisms underlying dysregulation of electrolyte absorption in inflammatory bowel disease-associated diarrhea,” Inflammatory Bowel Diseases, vol. 21, no. 12, pp. 2926–2935, 2015.
View at: Publisher Site | Google Scholar
C. M. Surawicz, “Mechanisms of diarrhea,” Current Gastroenterology Reports, vol. 12, no. 4, pp. 236–241, 2010.
View at: Publisher Site | Google Scholar
H. H. Wenzl, “Diarrhea in chronic inflammatory bowel diseases,” Gastroenterology Clinics of North America, vol. 41, no. 3, pp. 651–675, 2012.
View at: Publisher Site | Google Scholar
K. M. Hoque, S. Chakraborty, I. A. Sheikh, and O. M. Woodward, “New advances in the pathophysiology of intestinal ion transport and barrier function in diarrhea and the impact on therapy,” Expert Review of Anti-infective Therapy, vol. 10, no. 6, pp. 687–699, 2012.
View at: Publisher Site | Google Scholar
F. K. Ghishan and P. R. Kiela, “Small intestinal ion transport,” Current Opinion in Gastroenterology, vol. 28, no. 2, pp. 130–134, 2012.
View at: Publisher Site | Google Scholar
J. Foulke-Abel, J. In, J. Yin et al., “Human enteroids as a model of upper small intestinal ion transport physiology and pathophysiology,” Gastroenterology, vol. 150, no. 3, pp. 638–649e8, 2016.
View at: Publisher Site | Google Scholar
J. P. Geibel, V. M. Rajendran, and H. J. Binder, “Na+-dependent fluid absorption in intact perfused rat colonic crypts,” Gastroenterology, vol. 120, no. 1, pp. 144–150, 2001.
View at: Publisher Site | Google Scholar
M. Donowitz, C. Ming Tse, and D. Fuster, “SLC9/NHE gene family, a plasma membrane and organellar family of Na⁺/H⁺ exchangers,” Molecular Aspects of Medicine, vol. 34, no. 2-3, pp. 236–251, 2013.
View at: Publisher Site | Google Scholar
A. Kato and M. F. Romero, “Regulation of electroneutral NaCl absorption by the small intestine,” Annual Review of Physiology, vol. 73, no. 1, pp. 261–281, 2011.
View at: Publisher Site | Google Scholar
P. R. Kiela, H. Xu, and F. K. Ghishan, “Apical NA⁺/H⁺ exchangers in the mammalian gastrointestinal tract,” Journal of Physiology and Pharmacology, vol. 57, no. 7, pp. 51–79, 2006.
View at: Google Scholar
M. D. Parker, E. J. Myers, and J. R. Schelling, “Na+-H+ exchanger-1 (NHE1) regulation in kidney proximal tubule,” Cellular and Molecular Life Sciences, vol. 72, no. 11, pp. 2061–2074, 2015.
View at: Publisher Site | Google Scholar
P. G. Vallés, V. Bocanegra, A. Gil Lorenzo, and V. V. Costantino, “Physiological functions and regulation of the Na,” Kidney and Blood Pressure Research, vol. 40, no. 5, pp. 452–466, 2015.
View at: Publisher Site | Google Scholar
A. Shawki, M. A. Engevik, R. S. Kim et al., “Intestinal brush-border Na+/H+ exchanger-3 drives H+-coupled iron absorption in the mouse,” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 311, pp. G423–G430, 2016.
View at: Publisher Site | Google Scholar
P. He, L. Zhao, L. Zhu et al., “Restoration of Na⁺/H⁺ exchanger NHE3-containing macrocomplexes ameliorates diabetes-associated fluid loss,” Journal of Clinical Investigation, vol. 125, pp. 3519–3531, 2015.
View at: Publisher Site | Google Scholar
C. B. Larmonier, D. Laubitz, F. M. Hill et al., “Reduced colonic microbial diversity is associated with colitis in NHE3-deficient mice,” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 305, no. 10, pp. G667–G677, 2013.
View at: Publisher Site | Google Scholar
A. Kumar, P. Malhotra, H. Coffing et al., “Epigenetic modulation of intestinal Na(+)/H(+) exchanger-3 expression,” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 314, pp. G309–G318, 2018.
View at: Publisher Site | Google Scholar
R. L. Jakab, A. M. Collaco, and N. A. Ameen, “Characterization of CFTR high expresser cells in the intestine,” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 305, pp. G453–G465, 2013.
View at: Publisher Site | Google Scholar
K. Gholami, S. Muniandy, and N. Salleh, “In-vivo functional study on the involvement of CFTR, SLC26A6, NHE-1 and CA isoenzymes II and XII in uterine fluid pH, volume and electrolyte regulation in rats under different sex-steroid influence,” International Journal of Medical Sciences, vol. 10, no. 9, pp. 1121–1134, 2013.
View at: Publisher Site | Google Scholar
W. Xia, Q. Yu, B. Riederer et al., “The distinct roles of anion transporters Slc26a3 (DRA) and Slc26a6 (PAT-1) in fluid and electrolyte absorption in the murine small intestine,” Pflügers Archiv: European Journal of Physiology, vol. 466, pp. 1541–1556, 2014.
View at: Publisher Site | Google Scholar
J. Malakooti, S. Saksena, R. K. Gill, and P. K. Dudeja, “Transcriptional regulation of the intestinal luminal Na(+) and Cl(–) transporters,” Biochemical Journal, vol. 435, pp. 313–325, 2011.
View at: Publisher Site | Google Scholar
S. L. Alper and A. K. Sharma, “The SLC26 gene family of anion transporters and channels,” Molecular Aspects of Medicine, vol. 34, no. 2-3, pp. 494–515, 2013.
View at: Publisher Site | Google Scholar
Q. Xie, R. Welch, A. Mercado, M. F. Romero, and D. B. Mount, “Molecular characterization of the murine Slc26a6 anion exchanger: functional comparison with Slc26a1,” American Journal of Physiology-Renal Physiology, vol. 283, pp. F826–F838, 2002.
View at: Publisher Site | Google Scholar
S. Wedenoja, E. Pekansaari, P. Hoglund, S. Makela, C. Holmberg, and J. Kere, “Update on SLC26A3 mutations in congenital chloride diarrhea,” Human Mutation, vol. 32, no. 7, pp. 715–722, 2011.
View at: Publisher Site | Google Scholar
C. W. Schweinfest, D. D. Spyropoulos, K. W. Henderson et al., “slc26a3 (dra)-deficient mice display chloride-losing diarrhea, enhanced colonic proliferation, and distinct up-regulation of ion transporters in the colon,” Journal of Biological Chemistry, vol. 281, no. 49, pp. 37962–37971, 2006.
View at: Publisher Site | Google Scholar
M. N. Chernova, L. Jiang, B. E. Shmukler et al., “Acute regulation of the SLC26A3 congenital chloride diarrhoea anion exchanger (DRA) expressed in Xenopus oocytes,” The Journal of Physiology, vol. 549, no. 1, pp. 3–19, 2003.
View at: Publisher Site | Google Scholar
K. Gholami, S. Muniandy, and N. Salleh, “Progesterone downregulates oestrogen-induced expression of CFTR and SLC26A6 proteins and mRNA in rats’ uteri,” Journal of Biomedicine and Biotechnology, vol. 2012, p. 596084, 2012.
View at: Publisher Site | Google Scholar
M. W. Musch, D. L. Arvans, G. D. Wu, and E. B. Chang, “Functional coupling of the downregulated in adenoma Cl-/base exchanger DRA and the apical Na⁺/H⁺ exchangers NHE2 and NHE3,” American Journal of Physiology-Gastrointestinal and Liver Physiology, vol. 296, pp. G202–G210, 2009.
View at: Publisher Site | Google Scholar
X. F. Wang, M. K. Yu, S. Y. Lam et al., “Expression, immunolocalization, and functional activity of Na⁺/H⁺ exchanger isoforms in mouse endometrial epithelium,” Biology of Reproduction, vol. 68, pp. 302–308, 2003.
View at: Publisher Site | Google Scholar
V. J. Wheat, H. Shumaker, C. Burnham, G. E. Shull, J. R. Yankaskas, and M. Soleimani, “CFTR induces the expression of DRA along with Cl(–)/HCO(3)(–) exchange activity in tracheal epithelial cells,” American Journal of Physiology-Cell Physiology, vol. 279, no. 1, pp. C62–C71, 2000.
View at: Publisher Site | Google Scholar
E. J. Joy, E. L. Ander, S. D. Young et al., “Dietary mineral supplies in Africa,” Physiologia Plantarum, vol. 151, no. 3, pp. 208–229, 2014.
View at: Publisher Site | Google Scholar
Y. Liu, Y. L. Ma, J. M. Zhao, M. Vazquez-Anon, and H. H. Stein, “Digestibility and retention of zinc, copper, manganese, iron, calcium, and phosphorus in pigs fed diets containing inorganic or organic minerals,” Journal of Animal Science, vol. 92, no. 8, pp. 3407–3415, 2014.
View at: Publisher Site | Google Scholar
R. A. Budde and T. D. Crenshaw, “Chronic metabolic acid load induced by changes in dietary electrolyte balance increased chloride retention but did not compromise bone in growing swine,” Journal of Animal Science, vol. 81, no. 1, pp. 197–208, 2003.
View at: Publisher Site | Google Scholar
S. A. Guzman-Pino, D. Sola-Oriol, R. Davin, E. G. Manzanilla, and J. F. Perez, “Influence of dietary electrolyte balance on feed preference and growth performance of postweaned piglets,” Journal of Animal Science, vol. 93, no. 6, pp. 2840–2848, 2015.
View at: Publisher Site | Google Scholar
Y. Dersjant-Li, M. W. Verstegen, A. Jansman, H. Schulze, J. W. Schrama, and J. A. Verreth, “Changes in oxygen content and acid-base balance in arterial and portal blood in response to the dietary electrolyte balance in pigs during a 9-h period after a meal,” Journal of Animal Science, vol. 80, no. 5, pp. 1233–1239, 2002.
View at: Publisher Site | Google Scholar
L. N. Edwards, T. E. Engle, M. A. Paradis, J. A. Correa, and D. B. Anderson, “Persistence of blood changes associated with alteration of the dietary electrolyte balance in commercial pigs after feed withdrawal, transportation, and lairage, and the effects on performance and carcass quality,” Journal of Animal Science, vol. 88, no. 12, pp. 4068–4077, 2010.
View at: Publisher Site | Google Scholar
J. F. Patience, R. E. Austic, and R. D. Boyd, “Effect of dietary electrolyte balance on growth and acid-base status in swine,” Journal of Animal Science, vol. 64, no. 2, pp. 457–466, 1987.
View at: Publisher Site | Google Scholar
Y. Dersjant-Li, H. Schulze, J. W. Schrama, J. A. Verreth, and M. W. Verstegen, “Feed intake, growth, digestibility of dry matter and nitrogen in young pigs as affected by dietary cation-anion difference and supplementation of xylanase,” Journal of Animal Physiology and Animal Nutrition, vol. 85, no. 3-4, pp. 101–109, 2001.
View at: Publisher Site | Google Scholar
P. G. Lawlor, P. B. Lynch, P. J. Caffrey, J. J. O’Reilly, and M. K. O’Connell, “Measurements of the acid-binding capacity of ingredients used in pig diets,” Irish Veterinary Journal, vol. 58, pp. 447–452, 2005.
View at: Publisher Site | Google Scholar
T. Suzuki, “Regulation of intestinal epithelial permeability by tight junctions,” Cellular and Molecular Life Sciences, vol. 70, no. 4, pp. 631–659, 2013.
View at: Publisher Site | Google Scholar
V. K. Viswanathan, K. Hodges, and G. Hecht, “Enteric infection meets intestinal function: how bacterial pathogens cause diarrhoea,” Nature Reviews Microbiology, vol. 7, no. 2, pp. 110–119, 2009.
View at: Publisher Site | Google Scholar
M. H. Farahat, E. I. Hassanein, W. M. Abdel-Razik, and S. L. Noll, “Effect of dietary corn dried distillers grains with solubles, canola meal, and chloride on electrolyte balance, growth performance, and litter moisture of growing turkeys,” Poultry Science, vol. 92, no. 5, pp. 1254–1265, 2013.
View at: Publisher Site | Google Scholar
L. J. Magnoni, E. Salas-Leiton, M. J. Peixoto et al., “Dietary electrolyte balance affects growth performance, amylase activity and metabolic response in the meagre (Argyrosomus regius),” Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, vol. 211, pp. 8–15, 2017.
View at: Publisher Site | Google Scholar
S. Wedenoja, P. Hoglund, and C. Holmberg, “Review article: the clinical management of congenital chloride diarrhoea,” Alimentary Pharmacology and Therapeutics, vol. 31, no. 4, pp. 477–485, 2010.
View at: Publisher Site | Google Scholar
D. S. Merrell, S. M. Butler, F. Qadri et al., “Host-induced epidemic spread of the cholera bacterium,” Nature, vol. 417, pp. 642–645, 2002.
View at: Publisher Site | Google Scholar
S. M. Butler, E. J. Nelson, N. Chowdhury, S. M. Faruque, S. B. Calderwood, and A. Camilli, “Cholera stool bacteria repress chemotaxis to increase infectivity,” Molecular Microbiology, vol. 60, no. 2, pp. 417–426, 2006.
View at: Publisher Site | Google Scholar
J. A. S. Guttman, F. N. Samji, Y. Li, W. Deng, A. Lin, and B. Brett Finlay, “Aquaporins contribute to diarrhoea caused by attaching and effacing bacterial pathogens,” Cellular Microbiology, vol. 9, pp. 131–141, 2007.
View at: Publisher Site | Google Scholar
R. K. Buddington, P. T. Sangild, B. Hance, E. Y. Huang, and D. D. Black, “Prenatal gastrointestinal development in the pig and responses after preterm birth,” Journal of Animal Science, vol. 90, no. 4, pp. 290–298, 2012.
View at: Publisher Site | Google Scholar
G. Boudry, E. S. David, V. Douard, I. M. Monteiro, I. Le Huerou-Luron, and R. P. Ferraris, “Role of intestinal transporters in neonatal nutrition: carbohydrates, proteins, lipids, minerals, and vitamins,” Journal of Pediatric Gastroenterology and Nutrition, vol. 51, no. 4, pp. 380–401, 2010.
View at: Publisher Site | Google Scholar
W. F. Stenson, “Postnatal growth in the intestine,” Current Opinion in Gastroenterology, vol. 29, no. 2, pp. 107–111, 2013.
View at: Publisher Site | Google Scholar
O. Adeola and D. E. King, “Developmental changes in morphometry of the small intestine and jejunal sucrase activity during the first nine weeks of postnatal growth in pigs,” Journal of Animal Science, vol. 84, no. 1, pp. 112–118, 2006.
View at: Publisher Site | Google Scholar
A. F. Hofmann, V. Loening-Baucke, J. E. Lavine et al., “Altered bile acid metabolism in childhood functional constipation: inactivation of secretory bile acids by sulfation in a subset of patients,” Journal of Pediatric Gastroenterology and Nutrition, vol. 47, no. 5, pp. 598–606, 2008.
View at: Publisher Site | Google Scholar
M. Kim, L. Friesen, J. Park, H. M. Kim, and C. H. Kim, “Microbial metabolites, short-chain fatty acids, restrain tissue bacterial load, chronic inflammation, and associated cancer in the colon of mice,” European Journal of Immunology, vol. 48, no. 7, pp. 1235–1247, 2018.
View at: Publisher Site | Google Scholar
E. Prince and G. J. Fuchs, “1.3.6 Fluid and electrolytes. 1.3 Nutritional needs,” World Review of Nutrition and Dietetics, vol. 113, pp. 56–61, 2015.
View at: Publisher Site | Google Scholar
R. N. Appleby and J. R. Walters, “The role of bile acids in functional GI disorders,” Neurogastroenterology and Motility, vol. 26, no. 8, pp. 1057–1069, 2014.
View at: Publisher Site | Google Scholar
J. M. Ridlon, D. J. Kang, P. B. Hylemon, and J. S. Bajaj, “Gut microbiota, cirrhosis, and alcohol regulate bile acid metabolism in the gut,” Digestive Diseases, vol. 33, no. 3, pp. 338–345, 2015.
View at: Publisher Site | Google Scholar
L. Bishop, “Nutritional tips for managing electrolyte imbalances in post-renal transplant patients,” Journal of Renal Nutrition, vol. 22, no. 4, pp. e37–e38, 2012.
View at: Publisher Site | Google Scholar
S. Saravanan, I. Geurden, Z. G. Orozco, S. J. Kaushik, J. A. Verreth, and J. W. Schrama, “Dietary electrolyte balance affects the nutrient digestibility and maintenance energy expenditure of Nile tilapia,” British Journal of Nutrition, vol. 110, no. 11, pp. 1948–1957, 2013.
View at: Publisher Site | Google Scholar
C. Fusch and F. Jochum, “Water, sodium, potassium and chloride,” in World Rev Nutr Diet, vol. 110, pp. 99–120, 2014.
View at: Publisher Site | Google Scholar
J. Wiseman, “Variations in starch digestibility in non-ruminants,” Animal Feed Science and Technology, vol. 130, no. 1-2, pp. 66–77, 2006.
View at: Publisher Site | Google Scholar
C. Souza da Silva, D. Haenen, S. J. Koopmans et al., “Effects of resistant starch on behaviour, satiety-related hormones and metabolites in growing pigs,” Animal, vol. 8, pp. 1402–1411, 2014.
View at: Publisher Site | Google Scholar
Y. Li, A. R. Zhang, H. F. Luo et al., “In vitro and in vivo digestibility of corn starch for weaned pigs: effects of amylose:amylopectin ratio, extrusion, storage duration, and enzyme supplementation,” Journal of Animal Science, vol. 93, no. 7, pp. 3512–3520, 2015.
View at: Publisher Site | Google Scholar
Y. M. Lim, P. Hoobin, D. Ying, I. Burgar, P. R. Gooley, and M. A. Augustin, “Physical characterisation of high amylose maize starch and acylated high amylose maize starches,” Carbohydrate Polymers, vol. 117, pp. 279–285, 2015.
View at: Publisher Site | Google Scholar
S. Liu, F. Ren, L. Zhao et al., “Starch and starch hydrolysates are favorable carbon sources for bifidobacteria in the human gut,” BMC Microbiology, vol. 15, no. 1, p. 54, 2015.
View at: Publisher Site | Google Scholar
Z. Zhou, Y. Zhang, P. Zheng, X. Chen, and Y. Yang, “Starch structure modulates metabolic activity and gut microbiota profile,” Anaerobe, vol. 24, pp. 71–78, 2013.
View at: Publisher Site | Google Scholar
M. Miao, B. Jiang, S. W. Cui, T. Zhang, and Z. Jin, “Slowly digestible starch–a review,” Critical Reviews in Food Science and Nutrition, vol. 55, no. 12, pp. 1642–1657, 2015.
View at: Publisher Site | Google Scholar
S. Y. You, S. K. Oh, H. S. Kim, and H. J. Chung, “Influence of molecular structure on physicochemical properties and digestibility of normal rice starches,” International Journal of Biological Macromolecules, vol. 77, pp. 375–382, 2015.
View at: Publisher Site | Google Scholar
L. B. Bindels, J. Walter, and A. E. Ramer-Tait, “Resistant starches for the management of metabolic diseases,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 18, no. 6, pp. 559–565, 2015.
View at: Publisher Site | Google Scholar
M. J. Keenan, J. Zhou, M. Hegsted et al., “Role of resistant starch in improving gut health, adiposity, and insulin resistance,” Advances in Nutrition, vol. 6, no. 2, pp. 198–205, 2015.
View at: Publisher Site | Google Scholar
S. A. Zaman and S. R. Sarbini, “The potential of resistant starch as a prebiotic,” Critical Reviews in Biotechnology, vol. 36, pp. 578–584, 2016.
View at: Publisher Site | Google Scholar
D. F. Birt, T. Boylston, S. Hendrich et al., “Resistant starch: promise for improving human health,” Advances in Nutrition, vol. 4, no. 6, pp. 587–601, 2013.
View at: Publisher Site | Google Scholar
B. Svihus, “Starch digestion capacity of poultry,” Poultry Science, vol. 93, no. 9, pp. 2394–2399, 2014.
View at: Publisher Site | Google Scholar
S. K. Bhandari, C. M. Nyachoti, and D. O. Krause, “Raw potato starch in weaned pig diets and its influence on postweaning scours and the molecular microbial ecology of the digestive tract,” Journal of Animal Science, vol. 87, no. 3, pp. 984–993, 2009.
View at: Publisher Site | Google Scholar
A. M. V. Perera and R. T. Tyler, “Resistant starch: a review of analytical protocols for determining resistant starch and of factors affecting the resistant starch content of foods,” Food Research International, vol. 43, no. 8, pp. 1959–1974, 2010.
View at: Publisher Site | Google Scholar
J. S. Al-Rabadi, R. G. Gilbert, and M. J. Gidley, “Effect of particle size on kinetics of starch digestion in milled barley and sorghum grains by porcine alpha-amyla-se,” Journal of Cereal Science, vol. 50, no. 2, pp. 198–204, 2009.
View at: Publisher Site | Google Scholar
M. K. M. Leeman, A. C. Eliasson, and I. Bjorck, “Resistant starch formation in temperature treated potato starches varying in amylose/amylopectin ratio,” Carbohydrate Polymers, vol. 65, no. 3, pp. 306–313, 2006.
View at: Publisher Site | Google Scholar
A. A. Alsaffar, “Effect of thermal processing and storage on digestibility of starch in whole wheat grains,” Journal of Cereal Science, vol. 52, no. 3, pp. 480–485, 2010.
View at: Google Scholar
K. Lange, F. Hugenholtz, M. C. Jonathan et al., “Comparison of the effects of five dietary fibers on mucosal transcriptional profiles, and luminal microbiota composition and SCFA concentrations in murine colon,” Molecular Nutrition and Food Research, vol. 59, pp. 1590–1602, 2015.
View at: Publisher Site | Google Scholar
D. Haenen, J. Zhang, C. Souza da Silva et al., “A diet high in resistant starch modulates microbiota composition, SCFA concentrations, and gene expression in pig intestine,” The Journal of Nutrition, vol. 143, no. 3, pp. 274–283, 2013.
View at: Publisher Site | Google Scholar
E. Puertollano, S. Kolida, and P. Yaqoob, “Biological significance of short-chain fatty acid metabolism by the intestinal microbiome,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 17, no. 2, pp. 139–144, 2014.
View at: Publisher Site | Google Scholar
C. S. Byrne, E. S. Chambers, D. J. Morrison, and G. Frost, “The role of short chain fatty acids in appetite regulation and energy homeostasis,” International Journal of Obesity, vol. 39, no. 9, pp. 1331–1338, 2015.
View at: Publisher Site | Google Scholar
T. C. Rideout, Q. Liu, P. Wood, and M. Z. Fan, “Nutrient utilisation and intestinal fermentation are differentially affected by the consumption of resistant starch varieties and conventional fibres in pigs,” British Journal of Nutrition, vol. 99, no. 5, pp. 984–992, 2008.
View at: Publisher Site | Google Scholar
O. C. Umu, J. A. Frank, J. U. Fangel et al., “Resistant starch diet induces change in the swine microbiome and a predominance of beneficial bacterial populations,” Microbiome, vol. 3, no. 1, p. 16, 2015.
View at: Publisher Site | Google Scholar
R. G. Crittenden, L. F. Morris, M. L. Harvey, L. T. Tran, H. L. Mitchell, and M. J. Playne, “Selection of a Bifidobacterium strain to complement resistant starch in a synbiotic yoghurt,” Journal of Applied Microbiology, vol. 90, no. 2, pp. 268–278, 2001.
View at: Publisher Site | Google Scholar
I. Figueroa-Gonzalez, G. Quijano, G. Ramirez, and A. Cruz-Guerrero, “Probiotics and prebiotics–perspectives and challenges,” Journal of the Science of Food and Agriculture, vol. 91, no. 8, pp. 1341–1348, 2011.
View at: Publisher Site | Google Scholar
A. R. Bird, M. A. Conlon, C. T. Christophersen, and D. L. Topping, “Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics,” Beneficial Microbes, vol. 1, no. 4, pp. 423–431, 2010.
View at: Publisher Site | Google Scholar
W. Wu, J. Xie, and H. Zhang, “Dietary fibers influence the intestinal SCFAs and plasma metabolites profiling in growing pigs,” Food and Function, vol. 7, no. 11, pp. 4644–4654, 2016.
View at: Publisher Site | Google Scholar
J. M. Heo, A. K. Agyekum, Y. L. Yin, T. C. Rideout, and C. M. Nyachoti, “Feeding a diet containing resistant potato starch influences gastrointestinal tract traits and growth performance of weaned pigs,” Journal of Animal Science, vol. 92, no. 9, pp. 3906–3913, 2014.
View at: Publisher Site | Google Scholar
E. G. Manzanilla, M. Nofrarias, M. Anguita et al., “Effects of butyrate, avilamycin, and a plant extract combination on the intestinal equilibrium of early-weaned pigs,” Journal of Animal Science, vol. 84, no. 10, pp. 2743–2751, 2006.
View at: Publisher Site | Google Scholar
E. Hijova and A. Chmelarova, “Short chain fatty acids and colonic health,” Bratisl Lek Listy, vol. 108, pp. 354–358, 2007.
View at: Google Scholar
D. L. Topping and P. M. Clifton, “Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides,” Physiological Reviews, vol. 81, no. 3, pp. 1031–1064, 2001.
View at: Publisher Site | Google Scholar
T. S. Nielsen, P. K. Theil, S. Purup, N. P. Norskov, and K. E. Bach knudsen, “Effects of resistant starch and arabinoxylan on parameters related to large intestinal and metabolic health in pigs fed fat-rich diets,” Journal of Agricultural and Food Chemistry, vol. 63, no. 48, pp. 10418–10430, 2015.
View at: Publisher Site | Google Scholar
J. L. Slavin, “Carbohydrates, dietary fiber, and resistant starch in white vegetables: links to health outcomes,” Advances in Nutrition, vol. 4, no. 3, pp. 351S–355S, 2013.
View at: Publisher Site | Google Scholar
D. Subaric, D. Ackar, J. Babic, and B. Milicevic, “Starch for health,” Medicinski Glasnik, vol. 9, pp. 17–22, 2012.
View at: Google Scholar
J. M. Wong, R. de Souza, C. W. Kendall, A. Emam, and D. J. Jenkins, “Colonic health: fermentation and short chain fatty acids,” Journal of Clinical Gastroenterology, vol. 40, no. 3, pp. 235–243, 2006.
View at: Publisher Site | Google Scholar
R. L. Ordonio and M. Matsuoka, “Increasing resistant starch content in rice for better consumer health,” Proceedings of the National Academy of Sciences, vol. 113, no. 45, pp. 12616–12618, 2016.
View at: Publisher Site | Google Scholar
X. He, W. Sun, T. Ge, C. Mu, and W. Zhu, “An increase in corn resistant starch decreases protein fermentation and modulates gut microbiota during in vitro cultivation of pig large intestinal inocula,” Animal Nutrition, vol. 3, no. 3, pp. 219–224, 2017.
View at: Publisher Site | Google Scholar
H. Yan, R. Potu, H. Lu et al., “Dietary fat content and fiber type modulate hind gut microbial community and metabolic markers in the pig,” PLoS One, vol. 8, Article ID e59581, 2013.
View at: Publisher Site | Google Scholar
X. Zhao, Y. Xian, C. Li et al., “Feeding Lactobacillus plantarum and Lactobacillus casei increased microbial diversity and short chain fatty acids production in the gut-intestinal tract of weaning piglets,” Wei Sheng Wu Xue Bao, vol. 56, pp. 1291–1300, 2016.
View at: Google Scholar
V. Rosenfeldt, K. F. Michaelsen, M. Jakobsen et al., “Effect of probiotic Lactobacillus strains in young children hospitalized with acute diarrhea,” The Pediatric Infectious Disease Journal, vol. 21, no. 5, pp. 411–416, 2002.
View at: Publisher Site | Google Scholar
P. Janczyk, R. Pieper, H. Smidt, and W. B. Souffrant, “Changes in the diversity of pig ileal lactobacilli around weaning determined by means of 16S rRNA gene amplification and denaturing gradient gel electrophoresis,” FEMS Microbiology Ecology, vol. 61, no. 1, pp. 132–140, 2007.
View at: Publisher Site | Google Scholar
J. A. Higgins, “Resistant starch and energy balance: impact on weight loss and maintenance,” Critical Reviews in Food Science and Nutrition, vol. 54, no. 9, pp. 1158–1166, 2014.
View at: Publisher Site | Google Scholar
L. A. Bello-Perez, P. C. Flores-Silva, E. Agama-Acevedo, and J. Tovar, “Starch digestibility: past, present, and future,” Journal of the Science of Food and Agriculture, 2018.
View at: Publisher Site | Google Scholar

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