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      Microbial Mechanistic Insight into the Role of Inulin in Improving Maternal Health in a Pregnant Sow Model

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          Abstract

          General consumption of “western diet” characterized by high refined carbohydrates, fat and energy intake has resulted in a global obesity epidemics and related metabolic disturbance even for pregnant women. Pregnancy process is accompanied by substantial hormonal, metabolic and immunological changes during which gut microbiota is also remarkably remodeled. Dietary fiber has been demonstrated to have a striking role in shifting the microbial composition so as to improve host metabolism and health in non-pregnant individuals. The present study was conducted to investigate effects of adding a soluble dietary fiber inulin (0 or 1.5%) to low- or high- fat (0 or 5% fat addition) gestational diet on maternal and neonatal health and fecal microbial composition in a sow model. Results showed that inulin addition decreased the gestational body weight gain and fat accumulation induced by fat addition. Circulating concentrations of pro-inflammatory cytokine IL-6, adipokine leptin and chemerin were decreased by inulin supplementation. Inulin addition remarkably reduced the average BMI of newborn piglets and the within litter BMI distributions (%) ranging between 17 and 20 kg/m 2, and increased the BMI distribution ranging between 14 and 17 kg/m 2. 16S rRNA gene sequencing of the V3-V4 region showed that fecal microbial changes at different taxonomic levels triggered by inulin addition predisposed the pregnant sow to be thinner and lower inflammatory. Meanwhile, fecal microbial composition was also profoundly altered by gestation stage with distinct changes occurring at perinatal period. Most representative volatile fatty acid (VFA) producing-related genera changed dramatically when reaching the perinatal period and varied degrees of increases were detected with inulin addition. Fecal VFA concentrations failed to show any significant effect with dietary intervention, however, were markedly increased at perinatal period. Our findings indicate that positive microbial changes resulted by 1.5% soluble fiber inulin addition would possibly be the potential mechanisms under which maternal body weight, metabolic and inflammatory status and neonatal BMI were improved. Besides, distinct changes of microbial community at perinatal period indicated the mother sow is undergoing a catabolic state with increased energy loss and inflammation response at that period compared with other stages of gestation.

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          Intestinal Short Chain Fatty Acids and their Link with Diet and Human Health

          The colon is inhabited by a dense population of microorganisms, the so-called “gut microbiota,” able to ferment carbohydrates and proteins that escape absorption in the small intestine during digestion. This microbiota produces a wide range of metabolites, including short chain fatty acids (SCFA). These compounds are absorbed in the large bowel and are defined as 1-6 carbon volatile fatty acids which can present straight or branched-chain conformation. Their production is influenced by the pattern of food intake and diet-mediated changes in the gut microbiota. SCFA have distinct physiological effects: they contribute to shaping the gut environment, influence the physiology of the colon, they can be used as energy sources by host cells and the intestinal microbiota and they also participate in different host-signaling mechanisms. We summarize the current knowledge about the production of SCFA, including bacterial cross-feedings interactions, and the biological properties of these metabolites with impact on the human health.
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            Swine as models in biomedical research and toxicology testing.

            Swine are considered to be one of the major animal species used in translational research, surgical models, and procedural training and are increasingly being used as an alternative to the dog or monkey as the choice of nonrodent species in preclinical toxicologic testing of pharmaceuticals. There are unique advantages to the use of swine in this setting given that they share with humans similar anatomic and physiologic characteristics involving the cardiovascular, urinary, integumentary, and digestive systems. However, the investigator needs to be familiar with important anatomic, histopathologic, and clinicopathologic features of the laboratory pig and minipig in order to put background lesions or xenobiotically induced toxicologic changes in their proper perspective and also needs to consider specific anatomic differences when using the pig as a surgical model. Ethical considerations, as well as the existence of significant amounts of background data, from a regulatory perspective, provide further support for the use of this species in experimental or pharmaceutical research studies. It is likely that pigs and minipigs will become an increasingly important animal model for research and pharmaceutical development applications.
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              The influence of diet on the gut microbiota.

              Diet is a major factor driving the composition and metabolism of the colonic microbiota. The amount, type and balance of the main dietary macronutrients (carbohydrates, proteins and fats) have a great impact on the large intestinal microbiota. The human colon contains a dense population of bacterial cells that outnumber host cells 10-fold. Bacteroidetes, Firmicutes and Actinobacteria are the three major phyla that inhabit the human large intestine and these bacteria possess a fascinating array of enzymes that can degrade complex dietary substrates. Certain colonic bacteria are able to metabolise a remarkable variety of substrates whilst other species carry out more specialised activities, including primary degradation of plant cell walls. Microbial metabolism of dietary carbohydrates results mainly in the formation of short chain fatty acids and gases. The major bacterial fermentation products are acetate, propionate and butyrate; and the production of these tends to lower the colonic pH. These weak acids influence the microbial composition and directly affect host health, with butyrate the preferred energy source for the colonocytes. Certain bacterial species in the colon survive by cross-feeding, using either the breakdown products of complex carbohydrate degradation or fermentation products such as lactic acid for growth. Microbial protein metabolism results in additional fermentation products, some of which are potentially harmful to host health. The current 'omic era promises rapid progress towards understanding how diet can be used to modulate the composition and metabolism of the gut microbiota, allowing researchers to provide informed advice, that should improve long-term health status. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                17 November 2017
                2017
                : 8
                : 2242
                Affiliations
                Key Laboratory of Animal Disease–Resistance Nutrition and Feed Science, Ministry of Agriculture, People's Republic of China, Animal Nutrition Institute, Sichuan Agricultural University , Chengdu, China
                Author notes

                Edited by: Giovanna Suzzi, Università di Teramo, Italy

                Reviewed by: Shyamal Das Peddada, National Institute of Environmental Health Sciences (NIH), United States; Luciana Pellegrini Pisani, Federal University of São Paulo, Brazil

                *Correspondence: De Wu sow_nutrition@ 123456sina.com

                This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2017.02242
                5698696
                9aa3cc24-e329-43c2-b510-ac4e1aaca49a
                Copyright © 2017 Zhou, Zhao, Zhang, Li, Gui, Wang, Jin, Che, Li, Lin, Xu, Feng, Fang and Wu.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 07 June 2017
                : 31 October 2017
                Page count
                Figures: 5, Tables: 4, Equations: 1, References: 101, Pages: 17, Words: 13173
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                dietary fiber,gestation,microbial composition,maternal health,neonatal body mass index

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