Effects of functional oligosaccharide on regulating gut microbiota in obese mice: a short review

Abstract

Obesity is considered a complex and multifactorial disease that is rapidly spreading around the world, and it has become a global epidemic. As an “invisible organ” carrying the “second gene” of the human body, the intestinal flora participates in the metabolism of nutrients and energy in the human body. Current research suggested that gut microbiota might play a role in the development of obesity and associated comorbidities, affecting energy intake, lipid metabolism, immune responses, and endocrine functions. Functional oligosaccharides can be utilized by intestinal microorganisms to produce short-chain fatty acids, which affect the body's energy metabolism, absorption, and intestinal permeability, thereby mediating the occurrence and development of obesity. This study took obese mice as the main object and reviewed the effect of obesity on the gut microbiota, the effect of functional oligosaccharides on gut microbiota structure, and the mechanisms of gut microbiota in improving obesity, which aimed to provide therapeutic ideas for the prevention and treatment of obesity.

Keywords:
functional oligosaccharides; obesity; gut microbiota; obese mice

1 Introduction

Obesity is one of the most prevalent chronic metabolic diseases in the world, mainly caused by an energy imbalance, resulting in abnormal or excessive accumulation of body fat (Wang et al., 2022; Yildiz et al., 2021). With the advent of fast-paced life and changes in diet, the global obesity problem is rapidly spreading among adults, adolescents, and even children. Obesity can lead to various diseases and conditions, especially cardiovascular disease, type-2 diabetes, obstructive sleep apnea, cancer, osteoarthritis, and depression (Kleinert et al., 2018).

As an environmental factor, the gut microbiota can modulate the intake, absorption, and storage of energy in the host, thereby causing obesity. Prebiotic is an important example, it was defined as a substrate that is selectively utilized by host microorganisms conferring a health benefit (Gibson et al, 2017; Zhang et al., 2022). The findings suggest that gut microbiota dysbiosis can cause metabolic syndrome such as obesity. Compared with normal microbiota, the gut microbiota of obese hosts has lower gene richness and higher dietary energy acquisition capacity (Cotillard et al., 2013). A high-fat diet can alter the gut microbiota, leading to an increase in gut permeability and bacterial metabolites (e.g. endotoxin LPS). Excessive fat intake can lead to the increase of chylomicrons in the intestine. Endotoxin can combine with these chylomicrons, penetrates into the blood, and participates in systemic circulation, causing inflammation and metabolic diseases such as obesity (Boulangé et al., 2016; Cani et al., 2009). Prebiotics such as oligosaccharides and dietary fiber can alter gut microbiota structure, improve the integrity of gut connections, reduce endotoxemia, and prevent obesity. Of which, Lactobacillus and Bifidobacterium can regulate the intestinal microbial colony of mice with metabolic syndrome induced by a high-fat diet, as well as ease metabolic syndrome such as obesity (Wang et al., 2015). However, because of potential safety concerns, direct administration of probiotics to patients is not recommended. Studies have shown that oligofructose can reduce fat accumulation in high-fat mice, increase cecal weight, modulate gut microbiota, and increase fecal short-chain fatty acids (SCFAs) content (Respondek et al., 2013; Wang et al., 2017; Kao et al., 2018). Intake of xylooligosaccharides in mice can reduce serum cholesterol levels and increase the number of Bifidobacteria and Lactobacilli (Li et al., 2015). Moreover, Neyrinck et al. found that arabinoxylan oligosaccharides could control body weight and fat mass in mice with a high-fat diet by modulating the microbiota structure (Neyrinck et al., 2012). Therefore, the intake of functional oligosaccharides could be considered an effective method for reducing obesity-induced inflammation and intestinal dysbiosis.

2 The effect of obesity on gut microbiota

Under normal circumstances, the gut microbiota and the host are in an intricate dynamic balance, interacting with each other. For example, the host usually provides nutrients, and the gut microbes absorb them. At the same time, the host needs to use microbes to degrade substances that the host can not decompose and absorb. At present, studies have found that obvious changes in the gut microbiota could characterize obesity. Le et al. used metagenomics to analyze the gut microbial composition of 123 non-obese and 169 obese individuals in Denmark (Le Chatelier et al., 2013). The results showed that the number of gut microbial genes and the abundance of gut bacteria differed between the two groups. Individuals with low bacterial abundance have more pronounced overall obesity, insulin resistance, dyslipidemia, and inflammation than individuals with high bacterial abundance. Zmora et al. (2019) showed that a high-fat diet could easily induce obesity, and the increase of gram-negative bacteria for producing LPS in the intestine led to the imbalance of intestinal flora. In addition, LPS could stimulate CD14 and Toll-like receptor 4, resulting in increased white fat volume. Meijnikman et al. (2018) suggested that obesity decreased butyrate-producing bacteria. By comparing, it was found that obesity was associated with changes in the relative abundance of bacteria and proteus. Metagenomic and biochemical analysis indicated these changes affected the metabolic potential of the mouse gut microbiota. The results showed that the obesogenic microbiota could improve the ability to obtain energy from the diet (Turnbaugh et al., 2006). Finally, several prospective studies have shown that individuals with higher levels of Staphylococcus aureus and lower levels of Bifidobacterium in the gut during childhood were more likely to be overweight in adulthood (Guzzardi et al., 2022).

Furthermore, obesity could also be characterized by increased tone of the endocannabinoid (eCB) system and mild inflammation. It has been reported that the gut microbiota could modulate the hue of the gut eCB system, which in turn modulated gut permeability and plasma lipopolysaccharide (LPS) levels (Muccioli et al., 2010; Liu et al., 2003). The eCB system was found to control gut permeability and lipogenesis. LPS acted as a master switch by blocking cannabinoid-driven adipogenesis to control adipose tissue metabolism in vivo and in vitro. The results suggested that the gut microbiota determined adipose tissue physiology through the LPS-eCB system regulatory circuit and might play a key role in adipose tissue plasticity during obesity (Muccioli et al., 2010; Liu et al., 2003). Caesar et al. (2015) established an obese mouse model with a feed rich in lard. The study showed that Bacteroides, Tulsibacterium, and Bisporium acidophilus proliferated in the mouse gut, and the proliferation of these bacteria led to intestinal inflammation and insulin resistance.

Interestingly, obesity can also lead to altered gut microbiota in offspring. Animal experiments have shown that the gut microbiota of the offspring of obese mothers differs from controls (Ley et al., 2005). At the phylum level, the Bacteroidetes, Firmicutes, and Proteobacteria of obese mothers increased, whereas Firmicutes of the offspring decreased. This resulted in an increased Bacteroidetes/Firmicute ratio in the gut microbiota of the offspring. At the genus level, Bacteroides, Pasteurella, Desulfovibrio, and Myxospira were more abundant in the offspring of obese mothers, while Altobacterium, Clostridium cluster XIVa, Lachnospira Genus, and Oscillatory sp. were less abundant.

3 The effect of functional oligosaccharides on gut microbiota structure

3.1 Metabolism of functional oligosaccharides

After the functional oligosaccharide enters the human body, it will not be digested and absorbed in the gastric and small intestine environments. Therefore, the function of functional oligosaccharides is mainly realized through the bacterial fermentation process in the large intestine (Meyer & Stasse-Wolthuis, 2009). On the one hand, gut bacteria could utilize oligosaccharides, leading to changes in the microbiota composition. On the other hand, after reaching the intestinal tract and fermenting, bacteria could ferment oligosaccharides to produce short-chain fatty acids, which were used as energy sources for intestinal cells and probiotics, thereby promoting probiotic proliferation, inhibiting the growth of harmful bacteria, enhancing intestinal immunity. It is worth mentioning that the utilization of oligosaccharides by microorganisms requires the participation of glycosidases and transporters, which mainly include two ways: 1) hydrolyzed first and then transported, 2) transported first and then hydrolyzed.

3.2 Effects of functional oligosaccharides on the microbiota structure of obese mice

Functional oligosaccharides can alter the gut microbiota structure, improve the integrity of gut connections, and reduce blood endotoxemia in obese mice. Wang et al. studied the effects of konjac mannose oligosaccharides on the gut microbiota of obese mice, and the results showed that the intake of konjac mannose oligosaccharides increased the beneficial effects of Akkermansia muciniphila, Bacteroides acidifaciens, Lactobacillus gasseri, and Bifidobacterium pseudolongum in the intestinal tract of obese mice, as well as decreased the ratio of Firmicutes/Bacteroidetes (Wang et al., 2018). Respondek et al. (2013) showed that short-chain fructooligosaccharides could reduce fat deposition, increase cecal weight, and regulate some specific bacteria in obese mice. Cheng et al. (2018) studied the changes in gut microbiota after galacto-oligosaccharide intake in obese mice, and the results showed that the abundance of Ruminococcaceae and Oscillibacter decreased, while the abundance of Alloprevotella, Bacteroides, and Parasutterella increased. Zheng et al. (2018) used chitin oligosaccharide to improve obesity in mice and found that the abundance of Bifidobacterium, Lactobacillus, Akkermansia, and Bacteroides in the intestine of obese mice was lower than that of mice fed with chitin oligosaccharide. Hoving et al. (2018) studied the effect of konjac mannose oligosaccharide intake on the gut microbiota of obese mice and found that the abundance of Bacteroidetes was increased while the abundance of Firmicutes was decreased. Therefore, it was suggested that Bifidobacterium, Lactobacillus, Akkermansia, and Bacteroides abundances are negatively correlated with the obesity degree and can improve obesity symptoms (Dao et al., 2016; Moya-Pérez et al., 2015; Herrmann et al., 2017), while Oscillospira, Coprococcus, and Ruminococcus are positively associated with obesity (Tims et al., 2013). As mentioned by Cornejo-Pareja et al., ingested functional oligosaccharides were fermented by intestinal microorganisms to produce a large amount of short-chain fatty acids, which were utilized by microorganisms to increase the richness of the flora (Cornejo-Pareja et al., 2018).

4 The mechanisms of gut microbiota in improving obesity

4.1 Probiotic

In general, functional non-digestible oligosaccharides, such as isomalt oligosaccharides, fructooligosaccharides, and raffinose mixed lactose, can selectively promote the proliferation of Bifidobacteria, inhibiting the corrupt microorganisms multiply. Studies have found that many gut bacteria can use functional oligosaccharides. It was found that galacto-oligosaccharides, raffinose, or arabino-oligosaccharides could be used by Rectobacter, Roche, Erwinia, Bacteroides, and Clostridium. Short-chain fatty acids produced by gut microbial fermentation of oligosaccharides could induce thermogenesis in adipose tissue, by activating the intestinal receptor GPR43 or brown fat and downregulating peroxisome proliferator-activated receptor γ, thereby reducing body weight in high-fat diet-induced obese individuals (Rooks & Garrett, 2016). In conclusion, the possible mechanisms of oligosaccharides in the treatment of obesity include: 1) regulating gut microbes, 2) strengthening intestinal barrier, 3) inhibiting pathogens, and 4) regulating immunity. Among them, reducing the risk of obesity by regulating gut microbiota is the most popular in current research, attracting extensive attention from researchers.

4.2 Brain-gut axis

The brain-gut interaction is critical for energy homeostasis, which will be disrupted in obesity, leading to positive energy balance and weight gain. Perry et al. found that changes in rodent gut microbiota could increase acetate production (Perry et al., 2016), activating parasympathetic nerves, promoting insulin secretion, muscle augmentation, and ghrelin secretion, ultimately leading to violent pathological feedback pathways of binge eating. As an autoactive substance, 90% of 5-hydroxytryptamine (5-HT) is distributed in enterochromaffin cells and is often stored in cell granules together with ATP and other substances and will be secreted and released after being stimulated. It was found that the 5-HT is more present in the cerebral cortex and nerve synapses, which can control human appetite, reduce energy intake, increase energy consumption, and achieve the purpose of weight loss (Wu & Liu, 2017). Furthermore, Zmora et al. indicated that the body could ingest functional oligosaccharides to produce a large amount of short-chain fatty acids (Zmora et al., 2019), which could improve obesity symptoms, by stimulating the short-chain fatty acid receptor GPR41, exciting the central nervous system to promote intestinal glycogenesis, and inhibiting the production of LPS.

4.3 Chronic inflammation

The gut microbiota is currently considered having a potential effect on the development of obesity and its associated comorbidities. It is well known that excessive fat intake can cause an imbalance of intestinal flora in animals. The gut microbiota imbalance can lead to increased intestinal permeability and endotoxemia, further leading to low-grade chronic inflammation in animals. Therefore, chronic inflammation plays an important role in the induction and promotion of obesity (Al-Assal et al., 2018). Functional oligosaccharides can promote the proliferation of beneficial bacteria in the body, inhibit the release of endotoxin, reduce intestinal permeability, and indirectly prevent endotoxin from entering the blood through the intestine and binding to endotoxin-binding proteins, thereby reducing the activation of gene encoding inflammatory effectors to improve obesity. Boulangé et al. (2016) suggested that chronic inflammation was closely related to LPS-induced macrophage infiltration, obesity, and related metabolic diseases, and it could impact the gut microbiota.

5 Conclusion and prospects

As prebiotic, functional oligosaccharides can improve obesity by regulating the gut microbiota, and the mechanism is related to the proliferation of beneficial bacteria, the regulation of metabolism based on the brain-gut axis, and the inhibition of chronic inflammation. The various effects of gut microbiota and its metabolites on the host need more basic and clinical trials to study to provide a more theoretical basis for the prevention and treatment of obesity. With the development of metagenomics and metabolomics, intestinal intervention can be carried out for sensitive bacteria, such as the development of prebiotic-specific strains, intestinal transplantation of sensitive strains, and development of agonists or blockers related to the action of metabolites, which can provide guidelines for the prevention and treatment of chronic diseases. In addition, more and more multifunctional oligosaccharides have been discovered, such as human milk oligosaccharides, bird's nest polysaccharides, and wolfberry polysaccharides, and their functional properties are being studied to provide a scientific basis for the development of functional food ingredients.

• Practical Application: The effect of obesity on the gut microbiota, the effect of functional oligosaccharides on gut microbiota structure, and the mechanisms of gut microbiota in improving obesity were reviewed.

• Funding

  This research received no external funding.

References

• Al-Assal, K., Martinez, A. C., Torrinhas, R. S., Cardinelli, C., & Waitzberg, D. (2018). Gut microbiota and obesity. Clinical Nutrition Experimental, 20, 60-64. http://dx.doi.org/10.1016/j.yclnex.2018.03.001
  » http://dx.doi.org/10.1016/j.yclnex.2018.03.001
• Boulangé, C. L., Neves, A. L., Chilloux, J., Nicholson, J. K., & Dumas, M. E. (2016). Impact of the gut microbiota on inflammation, obesity, and metabolic disease. Genome Medicine, 8(1), 42. http://dx.doi.org/10.1186/s13073-016-0303-2 PMid:27098727.
  » http://dx.doi.org/10.1186/s13073-016-0303-2
• Caesar, R., Tremaroli, V., Kovatcheva-Datchary, P., Cani, P. D., & Bäckhed, F. (2015). Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling. Cell Metabolism, 22(4), 658-668. http://dx.doi.org/10.1016/j.cmet.2015.07.026 PMid:26321659.
  » http://dx.doi.org/10.1016/j.cmet.2015.07.026
• Cani, P. D., Possemiers, S., Van de Wiele, T., Guiot, Y., Everard, A., Rottier, O., Geurts, L., Naslain, D., Neyrinck, A., Lambert, D. M., Muccioli, G. G., & Delzenne, N. M. (2009). Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut, 58, 1091-1103. http://dx.doi.org/10.1136/gut.2008.165886 PMid:19240062.
  » http://dx.doi.org/10.1136/gut.2008.165886
• Cheng, W., Lu, J., Lin, W., Wei, X., Li, H., Zhao, X., Jiang, A., & Yuan, J. (2018). Effects of a galacto-oligosaccharide-rich diet on fecal microbiota and metabolite profiles in mice. Food & Function, 9(3), 1612-1620. http://dx.doi.org/10.1039/C7FO01720K PMid:29465126.
  » http://dx.doi.org/10.1039/C7FO01720K
• Cornejo-Pareja, I., Muñoz-Garach, A., Clemente-Postigo, M., & Tinahones, F. J. (2018). Importance of gut microbiota in obesity. European Journal of Clinical Nutrition, 72(Suppl 1), 26-37. http://dx.doi.org/10.1016/B978-0-12-801238-3.65351-5 PMid:30487562.
  » http://dx.doi.org/10.1016/B978-0-12-801238-3.65351-5
• Cotillard, A., Kennedy, S., Kong, L., Prifti, E., Pons, N., Le Chatelier, E., Almeida, M., Quinquis, B., Levenez, F., Galleron, N., Gougis, S., Rizkalla, S., Batto, J. M., Renault, P., Doré, J., Zucker, J. D., Clément, K., Ehrlich, S. D., Blottière, H., Leclerc, M., Juste, C., de Wouters, T., Lepage, P., Fouqueray, C., Basdevant, A., Henegar, C., Godard, C., Fondacci, M., Rohia, A., Hajduch, F., Weissenbach, J., Pelletier, E., Le Paslier, D., Gauchi, J.-P., Gibrat, J.-F., Loux, V., Carré, W., Maguin, E., van de Guchte, M., Jamet, A., Boumezbeur, F., & Layec, S., & ANR MicroObes Consortium. (2013). Dietary intervention impact on gut microbial gene richness. Nature, 500(7464), 585-588. http://dx.doi.org/10.1038/nature12480 PMid:23985875.
  » http://dx.doi.org/10.1038/nature12480
• Dao, M. C., Everard, A., Aron-Wisnewsky, J., Sokolovska, N., Prifti, E., Verger, E. O., Kayser, B. D., Levenez, F., Chilloux, J., Hoyles, L., Dumas, M. E., Rizkalla, S. W., Doré, J., Cani, P. D., & Clément, K., & MICRO-Obes Consortium. (2016). Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut, 65(3), 426-436. http://dx.doi.org/10.1136/gutjnl-2014-308778 PMid:26100928.
  » http://dx.doi.org/10.1136/gutjnl-2014-308778
• Gibson, G. R., Hutkins, R., Sanders, M. E., Prescott, S. L., Reimer, R. A., Salminen, S. J., Scott, K., Stanton, C., Swanson, K. S., Cani, P. D., Verbeke, K., & Reid, G. (2017). Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nature Reviews. Gastroenterology & Hepatology, 14(8), 491-502. http://dx.doi.org/10.1038/nrgastro.2017.75 PMid:28611480.
  » http://dx.doi.org/10.1038/nrgastro.2017.75
• Guzzardi, M. A., Ederveen, T. H. A., Rizzo, F., Weisz, A., Collado, M. C., Muratori, F., Gross, G., Alkema, W., & Iozzo, P. (2022). Maternal pre-pregnancy overweight and neonatal gut bacterial colonization are associated with cognitive development and gut microbiota composition in pre-school-age offspring. Brain, Behavior, and Immunity, 100, 311-320. http://dx.doi.org/10.1016/j.bbi.2021.12.009
  » http://dx.doi.org/10.1016/j.bbi.2021.12.009
• Herrmann, E., Young, W., Rosendale, D., Reichert-Grimm, V., Riedel, C. U., Conrad, R., & Egert, M. (2017). RNA-based stable isotope probing suggests Allobaculum spp. As particularly active glucose assimilators in a complex murine microbiota cultured in vitro. BioMed Research International, 2017, 1829685. http://dx.doi.org/10.1155/2017/1829685 PMid:28299315.
  » http://dx.doi.org/10.1155/2017/1829685
• Hoving, L. R., Katiraei, S., Heijink, M., Pronk, A., van der Wee-Pals, L., Streefland, T., Giera, M., Willems van Dijk, K., & van Harmelen, V. (2018). Dietary Mannan Oligosaccharides modulate gut microbiota, increase fecal bile acid excretion, and decrease plasma cholesterol and atherosclerosis development. Molecular Nutrition & Food Research, 62(10), e1700942. http://dx.doi.org/10.1002/mnfr.201700942 PMid:29665623.
  » http://dx.doi.org/10.1002/mnfr.201700942
• Kao, W. M., Chang, C. R., Chang, T. J., Li, S. Y., Chen, W. J., & Chau, C. F. (2018). Inclusion of fructooligosaccharide and resistant maltodextrin in high fat diets promotes simultaneous improvements on body fat reduction and fecal parameters. Molecules (Basel, Switzerland), 23(9), 2169-2178. http://dx.doi.org/10.3390/molecules23092169 PMid:30154352.
  » http://dx.doi.org/10.3390/molecules23092169
• Kleinert, M., Clemmensen, C., Hofmann, S. M., Moore, M. C., Renner, S., Woods, S. C., Huypens, P., Beckers, J., de Angelis, M. H., Schürmann, A., Bakhti, M., Klingenspor, M., Heiman, M., Cherrington, A. D., Ristow, M., Lickert, H., Wolf, E., Havel, P. J., Müller, T. D., & Tschöp, M. H. (2018). Animal models of obesity and diabetes mellitus. Nature Reviews. Endocrinology, 14(3), 140-162. http://dx.doi.org/10.1038/nrendo.2017.161 PMid:29348476.
  » http://dx.doi.org/10.1038/nrendo.2017.161
• Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., Almeida, M., Arumugam, M., Batto, J.-M., Kennedy, S., Leonard, P., Li, J., Burgdorf, K., Grarup, N., Jørgensen, T., Brandslund, I., Nielsen, H. B., Juncker, A. S., Bertalan, M., Levenez, F., Pons, N., Rasmussen, S., Sunagawa, S., Tap, J., Tims, S., Zoetendal, E. G., Brunak, S., Clément, K., Doré, J., Kleerebezem, M., Kristiansen, K., Renault, P., Sicheritz-Ponten, T., de Vos, W. M., Zucker, J.-D., Raes, J., Hansen, T., Guedon, E., Delorme, C., Layec, S., Khaci, G., van de Guchte, M., Vandemeulebrouck, G., Jamet, A., Dervyn, R., Sanchez, N., Maguin, E., Haimet, F., Winogradski, Y., Cultrone, A., Leclerc, M., Juste, C., Blottière, H., Pelletier, E., LePaslier, D., Artiguenave, F., Bruls, T., Weissenbach, J., Turner, K., Parkhill, J., Antolin, M., Manichanh, C., Casellas, F., Boruel, N., Varela, E., Torrejon, A., Guarner, F., Denariaz, G., Derrien, M., van Hylckama Vlieg, J. E. T., Veiga, P., Oozeer, R., Knol, J., Rescigno, M., Brechot, C., M’Rini, C., Mérieux, A., Yamada, T., Bork, P., Wang, J., Ehrlich, S. D., & Pedersen, O. (2013). Richness of human gut microbiome correlates with metabolic markers. Nature, 500(7464), 541-546. http://dx.doi.org/10.1038/nature12506 PMid:23985870.
  » http://dx.doi.org/10.1038/nature12506
• Ley, R. E., Bäckhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D., & Gordon, J. I. (2005). Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences of the United States of America, 102(31), 11070-11075. http://dx.doi.org/10.1073/pnas.0504978102 PMid:16033867.
  » http://dx.doi.org/10.1073/pnas.0504978102
• Li, Z., Summanen, P. H., Komoriya, T., & Finegold, S. M. (2015). In vitro study of the prebiotic xylooligosaccharide (XOS) on the growth of Bifidobacterium spp and Lactobacillus spp. International Journal of Food Sciences and Nutrition, 66(8), 919-922. http://dx.doi.org/10.3109/09637486.2015.1064869 PMid:26171632.
  » http://dx.doi.org/10.3109/09637486.2015.1064869
• Liu, J., Batkai, S., Pacher, P., Harvey-White, J., Wagner, J. A., Cravatt, B. F., Gao, B., & Kunos, G. (2003). Lipopolysaccharide induces anandamide synthesis in macrophages via CD14/MAPK/ phosphoinositide 3-kinase/NF-kappa B independently of platelet-activating factor. The Journal of Biological Chemistry, 278(45), 45034-45039. http://dx.doi.org/10.1074/jbc.M306062200 PMid:12949078.
  » http://dx.doi.org/10.1074/jbc.M306062200
• Meijnikman, A. S., Gerdes, V. E., Nieuwdorp, M., & Herrema, H. (2018). Evaluating causality of gut microbiota in obesity and diabetes in humans. Endocrine Reviews, 39(2), 133-153. http://dx.doi.org/10.1210/er.2017-00192 PMid:29309555.
  » http://dx.doi.org/10.1210/er.2017-00192
• Meyer, D., & Stasse-Wolthuis, M. (2009). The bifidogenic effect of inulin and oligofructose and its consequences for gut health. European Journal of Clinical Nutrition, 63(11), 1277-1289. http://dx.doi.org/10.1038/ejcn.2009.64 PMid:19690573.
  » http://dx.doi.org/10.1038/ejcn.2009.64
• Moya-Pérez, A., Neef, A., & Sanz, Y. (2015). Bifidobacterium pseudocatenulatum CECT 7765 reduces obesity-associated inflammation by restoring the lymphocyte-macrophage balance and gut microbiota structure in high-fat diet-fed mice. PLoS One, 10(7), e0126976. http://dx.doi.org/10.1371/journal.pone.0126976 PMid:26161548.
  » http://dx.doi.org/10.1371/journal.pone.0126976
• Muccioli, G. G., Naslain, D., Bäckhed, F., Reigstad, C. S., Lambert, D. M., Delzenne, N. M., & Cani, P. D.. (2010). The endocannabinoid system links gut microbiota to adipogenesis. Molecular Systems Biology, 6(1), 392. http://dx.doi.org/10.1038/msb.2010.46 PMid:20664638.
  » http://dx.doi.org/10.1038/msb.2010.46
• Neyrinck, A. M., Van Hée, V. F., Piront, N., De Backer, F., Toussaint, O., Cani, P. D., & Delzenne, N. M. (2012). Wheat-derived arabinoxylan oligosaccharides with prebiotic effect increase satietogenic gut peptides and reduce metabolic endotoxemia in diet-induced obese mice. Nutrition & Diabetes, 2(1), e28. http://dx.doi.org/10.1038/nutd.2011.24 PMid:23154683.
  » http://dx.doi.org/10.1038/nutd.2011.24
• Perry, R. J., Peng, L., Barry, N. A., Cline, G. W., Zhang, D., Cardone, R. L., Petersen, K. F., Kibbey, R. G., Goodman, A. L., & Shulman, G. I. (2016). Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome. Nature, 534(7606), 213-217. http://dx.doi.org/10.1038/nature18309 PMid:27279214.
  » http://dx.doi.org/10.1038/nature18309
• Respondek, F., Gerard, P., Bossis, M., Boschat, L., Bruneau, A., Rabot, S., Wagner, A., & Martin, J. C.. (2013). Short-chain fructo-oligosaccharides modulate intestinal microbiota and metabolic parameters of humanized gnotobiotic diet induced obesity mice. PLoS One, 8(8), e71026. http://dx.doi.org/10.1371/journal.pone.0071026 PMid:23951074.
  » http://dx.doi.org/10.1371/journal.pone.0071026
• Rooks, M. G., & Garrett, W. S. (2016). Gut microbiota, metabolites and host immunity. Nature Reviews. Immunology, 16(6), 341-352. http://dx.doi.org/10.1038/nri.2016.42 PMid:27231050.
  » http://dx.doi.org/10.1038/nri.2016.42
• Tims, S., Derom, C., Jonkers, D. M., Vlietinck, R., Saris, W. H., Kleerebezem, M., de Vos, W. M., & Zoetendal, E. G. (2013). Microbiota conservation and BMI signatures in adult monozygotic twins. The ISME Journal, 7(4), 707-717. http://dx.doi.org/10.1038/ismej.2012.146 PMid:23190729.
  » http://dx.doi.org/10.1038/ismej.2012.146
• Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 444(7122), 1027-1031. http://dx.doi.org/10.1038/nature05414 PMid:17183312.
  » http://dx.doi.org/10.1038/nature05414
• Wang, G., Zhang, J., Zhang, K., Zhao, Q., Zhou, F., Xu, J., Xue, W., Zhang, C., & Fu, C. (2022). Possible action mechanisms of vitamin D supplementation in combating obesity and obesity-related issues of bone health: a mini review. Food Science and Technology (Campinas), 42, e114621. http://dx.doi.org/10.1590/fst.114621
  » http://dx.doi.org/10.1590/fst.114621
• Wang, H., Zhang, X., Wang, S., Li, H., Lu, Z., Shi, J., & Xu, Z. (2018). Mannan-oligosaccharide modulates the obesity and gut microbiota in high-fat diet-fed mice. Food & Function, 9(7), 3916-3929. http://dx.doi.org/10.1039/C8FO00209F PMid:29974116.
  » http://dx.doi.org/10.1039/C8FO00209F
• Wang, J., Tang, H., Zhang, C., Zhao, Y., Derrien, M., Rocher, E., van-Hylckama Vlieg, J. E., Strissel, K., Zhao, L., Obin, M., & Shen, J. (2015). Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. The ISME Journal, 9(1), 1-15. http://dx.doi.org/10.1038/ismej.2014.99 PMid:24936764.
  » http://dx.doi.org/10.1038/ismej.2014.99
• Wang, L., Hu, L., Yan, S., Jiang, T., Fang, S., Wang, G., Zhao, J., Zhang, H., & Chen, W. (2017). Effect of different oligosaccharides at various dosages on the composition of gut microbiota and short-chain fatty acids in mice with constipation. Food & Function, 8(5), 1966-1978. http://dx.doi.org/10.1039/C7FO00031F PMid:28475191.
  » http://dx.doi.org/10.1039/C7FO00031F
• Wu, L. J., & Liu, T. H. (2017). The Role of gut microbiota in the pathogenesis of obesity. World Science and Technology-Modernization of Traditional Chinese Medicine, 19(9), 1572-1579. http://dx.doi.org/http://dx.doi.org.
  » https://doi.org/http://dx.doi.org» https://doi.org/http://dx.doi.org
• Yildiz, E., Guldas, M., Ellergezen, P., Acar, A. G., & Gurbuz, O. (2021). Obesity-associated Pathways of Anthocyanins. Food Science and Technology (Campinas), 41(suppl 1), 1-13. http://dx.doi.org/10.1590/fst.39119
  » http://dx.doi.org/10.1590/fst.39119
• Zhang, J., Mu, J., Li, X., & Zhao, X. (2022). Relationship between probiotics and obesity: a review of recent research. Food Science and Technology (Campinas), 42, e30322. http://dx.doi.org/10.1590/fst.30322
  » http://dx.doi.org/10.1590/fst.30322
• Zheng, J., Cheng, G., Li, Q., Jiao, S., Feng, C., Zhao, X., Yin, H., Du, Y. H., & Liu, H. (2018). Chitin oligosaccharide modulates gut microbiota and attenuates high-fat-diet-induced metabolic syndrome in mice. Marine Drugs, 16(2), 66. http://dx.doi.org/10.3390/md16020066 PMid:29463060.
  » http://dx.doi.org/10.3390/md16020066
• Zmora, N., Suez, J., & Elinav, E. (2019). You are what you eat: diet, health and the gut microbiota. Nature Reviews. Gastroenterology & Hepatology, 16(1), 35-56. http://dx.doi.org/10.1038/s41575-018-0061-2 PMid:30262901.
  » http://dx.doi.org/10.1038/s41575-018-0061-2

Publication Dates

• Publication in this collection
  06 Jan 2023
• Date of issue
  2023

History

• Received
  30 Sept 2022
• Accepted
  15 Nov 2022