Factors Affecting Gut Microbiome in Daily Diet
Qi Su
Qin Liu- Department of Medicine and Therapeutics, The Chinese University of Hong Kong, Hong Kong, China
There is a growing recognition that a good diet can help people maintain mental and physical health, while a bad one will cause the disorder of body function, and even lead to several diseases. A lot of attentions have been devoted to analyze every possible health-related factor in the daily diet, including food ingredients, additives, and cooking process. With the support of high-throughput sequencing technology, there is accumulating evidence gradually clarifying that most of these factors are mainly through the interactions with gut microbiome to trigger downstream effects. The gut microbiome may be able to act as a very sensitive mirror in response to human daily diet. A complex network of interactions among diet, gut microbiome, and health has been gradually depicted, but it is rarely discussed from a more comprehensive perspective. To this end, this review summarized the latest updates in diet-gut microbiome interactions, analyzed most identified factors involved in this process, showed the possibility of maintaining health or alleviating diseases by diet intervention, aiming to help people choose a suitable recipe more accurately.
Introduction
Food provides energy and nutrition that has a great impact on health, mainly by changing the gut conditions and then influencing host immunology homeostasis. Trillions of microbes settle in the gut and play fundamental roles in metabolism, endocrine, neuronal, immune and many other aspects of body function. Notably, diet can greatly influence gut microbiome (1), which can greatly impact host's health. Given the inextricable relationship among diet, gut microbiome, and health, numerous studies have been carried out to explore the underlying mechanism (2). Especially at present, obesity, inflammatory bowel disease, allergic diseases, cognitive aging, Alzheimer's disease, and many other non-communicable diseases have become an important health problem in developed and developing countries (3–5), highlighting a need to understand how to attenuate these problems, while diet intervention seems to be the most effective and pleasant way (6, 7).
Dietary habits have a profound effect in shaping the gut microbiome in real time since birth. Microbes colonize the gut immediately after birth, and such early development of gut microbiome is thought to be driven and regulated, at least in part, by specific compounds present in breast milk (8, 9). Several host and external factors modulate the establishment of the immunity during the fetal and early postnatal life, however, few are as important as the interaction with commensal microbes, which is not only the most intimate environmental exposure but also represents a challenge to the development of host (10–13). For example, infants with lower relative abundance of Bifidobacterium, Akkermansia, and Faecalibacterium are at higher risk of CD4+ T cell dysfunction, which might induce to childhood atopy and asthma (10), and the dysbiosis of these microbes is currently clearly related to unsuitable formula feeding (12, 13), showing the importance of early feeding of babies. On the other hand, some Bifidobacterial species have evolved to utilize glycan in human secretion, which represents the adaptive ability at transformation of symbiotic microorganisms to the host, and it is believed that both sides will benefit (14–16) via microbiome-host cell interactions.
Infancy is the starting point for the development of gut microbiome, which will gradually mature in the next 3 years and undergo changes over a life-long time (17). From infants to adults, the host itself and gut microbes are co-evolving and interacting, while it is important to provide a harmonious environment for each side (18–20). In healthy adults, the overall composition of the gut microbiome can be stable for several years (21), but the relative abundance of each member contained in is highly variable (22). Long term dietary habits affect the development and maturation of gut microbiome, but this does not mean that temporary adjustment is not possible to achieve the desired aims, especially foodborne microorganisms, including bacteria, fungi and even viruses, can quickly colonize the gut. A study of human diet intervention showed that changes or adjustments of food types in an extremely short time can quickly change the structure of gut microbiome, which will become completely different in 3 or 4 days, and overwhelms the individual differences in microbial gene expression and personal genetic background (22, 23), showing the universality and potential of the dietary intervention (23). Therefore, no matter for any stage of life, choosing a reasonable diet has an obvious salutary influence on health.
In the long history, people's eating habits are also gradually changing. From the original menu shared by primitive humans and wild animals, such as orangutans and monkeys, to the farming period when people ate certain kinds of grains with little meat, and then to the modern food produced by complex process and containing a variety of additives in the industrial era, gut microbiome itself has also undergone the challenges of these changes, and become completely different. It's still hard to say whether this change is good or bad. The previous study concerning the traditional populations gives us an overview of human-related microbes influenced by industrialization, and also a window into the co-evolution between the microbiome and human, showing that not only the microbiome from the Hadza hunter-gatherers of Tanzania seasonally shift in bacterial taxa, diversity, and carbohydrate utilization, but also shares certain microbes with several other traditional populations that are almost rare or absent from microbiomes of modern countries (24, 25). Given the positive correlation between the diversity of gut microbiome and health, there is no doubt that the transition from the traditional farming era to the industrial age has resulted in the loss of critical organisms and functionality for industrialized populations, even if their effects on health have not been elucidated. There is no doubt that food in the industrial era has not made our gut microbiome more resilient, which may be the reason why the incidence rate of many non-communicable diseases is increasing with the development of society and is more significant in developed countries (3, 26–28). As a result, for most people with long-term unchanged recipes, their gut microbial diversity is gradually lost, which in turn affects the host, causing more diseases. For example, the western diet (ultra-processed foods with excess fat, sugar, additives, and a very small amount of micronutrients and dietary fiber) is closely related with the current prevalence of obesity and several other metabolic diseases, because the environment shaped in the gut by this dietary patterns provides fertile soil for microbes that can induce diverse inflammatory diseases (29–31). Therefore, clarifying the role of the microbiome in diet-related diseases is of great importance to precision medicine, dietary recommendation, and food production practice.
At present, it has been widely recognized that there are a large amount of microbial species that settle in the gut, while the composition and function of it are closely related to the diseases of the digestive, nervous, respiratory, metabolic, and cardiovascular system (32). A lot of work has focused on exploring the potential relationship and related mechanisms of microbial mediated diseases, and many new findings have been used to guide patients to choose appropriate long-term or short-term diet intervention to alleviate the disease or accelerate the recovery (33, 34). Most of them demonstrated that low energy or high fiber diet is very helpful to revitalize gut microbiome, which happens to provide an improvement suggestion for those who have already adapted to the western diet, especially for people who are suffering from obesity or autism (35–39). With the help of advanced sequencing technology and analysis technology, we can accurately depict the profile of gut microbiome in people with or without a certain condition, but it is difficult to say whether these differences are the cause or the consequences of related diseases. Relatively few randomized, clinically controlled dietary interventions targeting gut microbiome have been reported in humans, thus more accurate experiments should be carried out as soon as possible to make up for these gaps.
Now, the accumulated evidence is gradually clarifying the relationship between diet, microbiome and disease. This review will analyze the effects of diet on the gut microbiome from different aspects, including food (carbohydrates, fats, proteins, minerals, and vitamins), additives and different cooking and processing etc., and try to establish a complete framework from these perspectives, show the focus of related research, and lay a foundation for future research and development.
Carbohydrates
Carbohydrates are composed of carbon, hydrogen, and oxygen, which are the most abundant organic compounds with broad-spectrum chemical structure and biological functions (40). They can be expressed by the general formula Cx(H2O)y and works as the main source of energy for the human body. Generally, there are two types of carbohydrates in food: the effective carbohydrates that people can totally digest and then absorb as well as the ineffective counterparts that people can't digest by themselves, namely non-digestible carbohydrates, which are far away from the way digestible carbohydrates go in the gut. Non-digestible carbohydrates get through the first part of the digestive tract completely to the ileum and colon, and then will be digested by the microbes that reside there, thus they can also be called microbiome-accessible carbohydrates (MACs) and offers the main energy for colonic microbes (41). These non-digestible carbohydrates have a huge impact on the gut microbiome, while dietary fiber is one of them that has been most clearly studied. As early as 45 years ago, Trowell's study showed that the cause of type 2 diabetes may be due to the lack of dietary fiber in the diet, while rapid changes in dietary habits led to a large-scale epidemic of diabetes in the Pima Indians, who changed their traditional diet containing sufficient non-digestible carbohydrates to a modern diet with scarce fibers and cereal products (42). These non-digestible carbohydrates, including human milk oligosaccharides (HMO), serve as not only anti-sticking agents that prevent pathogen adhesion and promote immune maturation, but also providing guidance for the maturation of the gut microbiome, contributing to human health (43, 44). For this purpose, specific non-digestible carbohydrates (NDC) are being produced, such as galactooligosaccharides (GOS) and fructooligosaccharides (FOS), which are currently being added to infant formulas to help the healthy development of the gut microbiome in China (45).
Application of the state-of-art sequencing methods has updated our knowledge of the function of dietary fiber, demonstrating that it plays an important role in affecting the microbiome structure and function. For example, the gut microbiome generates short-chain fatty acids (SCFAs) essential for gut health (46–49). There was a significant correlation between SCFAs levels and microbial community composition. Fermentation of dietary fiber could reduce the pH in the colon (5.5 to 6.5), and slow down the growth of several gram-negative pathogens, such as Salmonella and Escherichia coli (50, 51), providing a clear clue to the mechanism of dietary fiber regulating gut microbiome. Based on this theory, many studies have clearly described the negative effects of dietary fiber deficiency on gut microbiome and host, and demonstrated the benefits of short-term or long-term dietary fiber supplementation, especially for people with obesity and metabolic diseases. For example, an insufficient supply of dietary fiber will make certain beneficial bacteria strains disappear (52). More seriously, in chronic or intermittent dietary fiber deficiency, intestinal microbes will digest mucus glycoprotein secreted by the host, and erode the colonic mucus barrier. Lack of dietary fiber, combined with fiber deficiency and mucus corroding microbes, gives the mucosal pathogen, Citrobacter rodentium, more opportunities to contact the epithelium and cause fatal colitis (53).
In contrast, extra dietary fiber supplements seem to be beneficial. Eating 25 to 38 g dietary fiber each day was confirmed to be closely related to a reduced risk of type 2 diabetes by 20–30% (54). Furthermore, dietary fibers from chicory inulin and sugar beet pectin can be employed to control the immune response to nosocomial infections caused by non-fermenting Gram-negative bacilli, such as Sphingomonas paucimobilis (55), confirming again the importance of carbohydrates in the diet. The opposite is a so-called “weight loss” diet that are high in protein and low in carbohydrate, which will increase the number of Bacteroides and reduce Firmicutes, and then lead to higher risk of colon disease (56).
Fats
Fat is mainly digested in the upper part of the small intestine, where it will be hydrolyzed into glycerin and fatty acids by various enzymes and bile acid salts, and then works as the main source of calories, satisfying half of the energy needs of us (57, 58). The gut microbiome also interacts intensively with dietary fat. On the one hand, gut microbiome impacts the energy balance of host, playing an important role in the absorption and metabolism of dietary fat (58, 59). What's more interesting is that gut microbes can even determine the distribution of fat in the body, thus forming different body shapes (60). On the other hand, the high-fat diet can effectively alter diurnal patterns of gut microbiome structure and function, finally achieving a new balance (57), but a lot of times it's harmful. High-fat diets are associated with a reduction in intestinal bacterial diversity, changes in membrane integrity, inducing increased permeability and increased lipopolysaccharide translocation, changes in the immune system, and generation of low-intensity systemic inflammation. Mouse experiments demonstrated that a high-fat diet causes a significant increase in intestinal deoxycholic acid (DCA) that promotes liver cancer (61). Although there is no evidence that there is a corresponding phenomenon in the human body, it cannot be ignored that some potential negative effects must exist. Another study further confirmed that the animal-based diet significantly increased the activity of bacterial genes that encode microbial bile salt hydrolases (22), which are necessary for DCA production by intestinal microorganisms (62). Elevated DCA levels may in turn lead to microbial disorders in the animal-based diet, as this bile acid inhibits the growth of Bacteroides and Firmicutes members (63). A high-fat diet also promotes the growth of B. wadsworthia (22), while the production of B. wadsworthia, H2S, is thought to inflame intestinal tissue and then case the inflammatory bowel disease (64). The mechanism behind this has also been fully analyzed. Firstly, Bifidobacterium-containing clusters are positively correlated with long-term dairy as well as baseline saturated fat intake, supporting the potential association with milk-related saturated fat (64); secondly, the animal-based diet increases the concentrations of fecal bile acid significantly; thirdly, the relative abundance of microbial DNA or RNA encoding sulfite reductase in the animal-based diet is significantly increased (22). All these findings support the idea that the effect of the diet-related factors on gut microbiome may induce inflammatory bowel disease.
Different from what is generally believed, the harm of the high-fat diet is not only for the old who have a low metabolic level but also for the young. In a recent study, 217 young adults (18 to 35 years old; body mass index below 28 kg per m2; 48% men) were invited to a 6-month randomized controlled-feeding trial by taking three different diets (20, 30, and 40% fat energy), demonstrated that the high fat intake of healthy young people seems to be related to adverse changes in the gut microbiome, fecal metabolic profiles and plasma pro-inflammatory factors, while these taking a lower-fat diet showed an increased α-diversity, increased abundance of beneficial Blautia and Faecalibacterium (65). Intestinal Blautia is related with decreased death risk from graft-vs. host disease, and Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium (66–68). Besides, the high-fat diet of young mothers is also important for the composition of their children's gut microbiome, which indirectly indicates that excessive fat intake is also unhealthy for infants (69). Therefore, excessive fat intake should be avoided at any stage of life to minimize the risks associated with it.
Many cases highlighted the benefits of the low-fat diet. Hyuju et al. found that the low-fat/high-fiber diet can promote anastomotic healing by regulating the microbiome in mice (70). In short, compared with low-fat/high-fiber (SD)-fed mice, Western diet (WD)-fed mice have an increased risk of anastomotic leakage, an increase in the relative abundance of Enterococcus in the intestinal lumen. After the operation, the microbial community of SD-fed mice (rather than WD-fed mice) returned to its preoperative composition. When WD-fed mice were exposed to the SD diet for 2 days before antibiotics and surgery, anastomotic healing was also significantly improved (70). Such study should be repeated in humans, and if the same results exist, it will be very helpful to develop specific diets to help patients recover from trauma.
However, an extremely low-fat diet is not always good, and the most important thing is to find a balance. Evidence from an animal experiment showed that long-term low-fat diet inhibited cholecystokinin (CCK) satiation, changed the caecal metabolome, and then reduced caecal weight in rats (71), which indicates that the low-fat diet must be used with caution, even for those who want to lost weight, before determining all potential side effects of it.
Proteins
Protein and corresponding metabolites (mainly amino acids) are vital to human body functions and are also the main source of nitrogen for gut microbes. Digestion of protein starts in the stomach, where the pepsinogen can non-specifically degrade a variety of water-soluble proteins into polypeptides, oligopeptides and a small number of amino acids (72). After entering the intestine, these primary digestion products can be further degraded by trypsin and chymotrypsin into small peptides or amino acid molecules that can be absorbed (73). Gut microbiome seems to be involved in all the above processes and play an important role in downstream absorption, metabolism, transformation, and even mediate the interaction between dietary protein and host immunity (74–76). Amino acids can be further metabolized into a variety of microbial metabolites, which participate in a lot of host functions related to health and diseases. At the same time, different sources, concentration and components of dietary protein also affect the composition, structure, and function of the gut microbiome (77). In response to changes in dietary protein, microbial metabolites (including SCFAs, ammonia, amines, hydrogen, sulfide and methane, and other gases related to colon cancer and inflammatory bowel disease) have undergone significant changes (78–80).
Dietary guidelines from popular science often suggest high protein intake, especially from animal sources with diverse and enough essential amino acids, to combat muscle atrophy, obesity, weakness, osteoporosis, surgical stress and death rate. However, a proper ratio of protein to carbohydrate, or even a relatively low protein diet, is more recommended because excessive protein promotes the growth of pathogenic microorganisms, inducing a high risk of metabolic-related diseases (81). Residual nitrogenous compounds not absorbed by the small intestine are transferred to the distal intestine and metabolized by microorganisms in this part. Protein intake affects the quantity and species of microbial metabolites, but some of them are toxic, such as hydrogen sulfide, ammonia and indole compounds, which have potentially negative effects on host health (82–84). Some bioactive substances participate in various physiological processes of the host (76). Besides, high concentrations of protein supplementation will lead to an increase in the number of potential pathogens, which is due to the destruction of the homeostasis of the intestinal micro-ecosystem and the reduction of the number of beneficial microorganisms. This observation highlights the interaction between the gut microbiome and host health. Dietary protein altered gut microbiome affects host metabolism by regulating intestinal barrier function, intestinal motility and immune system. More seriously, there is evidence that after a high-protein diet, individuals with or without impaired renal function may experience deterioration in renal function (85, 86).
Micronutrients
Micronutrients, namely minerals and vitamins, mean nutrients that the human body needs less, but are necessary for maintaining survival, growth, development and health. It is well-known that the “western diet”, lacking in micronutrients, drives nearly all modern chronic conditions by encouraging gut dysbiosis, while micronutrients also play an important role in this process (87). For example, obesity is related to changes in hormones, especially bone regulating hormones, such as vitamin D (88–90). Mild chronic inflammation can lead to an increase of pro-inflammatory cytokines by activating multiple signaling pathways, finally leading to obesity (91), while vitamin D has been recognized as having anti-inflammatory effects on various immune cells, although it has not been confirmed in randomized controlled trials (92). Research by Guo et al. showed that vitamin D can stimulate the expression of cathelidin antimicrobial peptide (CAMP) gene, which is expressed through immune cells and epithelial cells to enhance barrier function (93), suggesting that vitamin D is antibacterial. Also, vitamin D modifies epithelial cells' integrity, immune responses especially for the innate immunity, and the diversity as well as the composition of the gut microbiome (94), and is expected to alleviate inflammatory bowel disease by regulating homeostasis in the gut (95). In one clinical trial in patients with inflammatory bowel disease, receiving 1,200 IU/day of Vitamin D for 1 year reduced the relapse rate from 29 to 13% when compared with the placebo group (96). Dietary habits may also affect the synthesis of some micronutrients by affecting the structure and function of the gut microbiome. In the cecum, liver and kidneys, the vitamin K was primarily derived from microbes and was decreased by 32 to 66% in mice treated by large doses of antibiotics compared to untreated animals, which in turn seriously affects bone development (97), suggesting the importance of metabolites produced by the healthy gut microbiome, including various vitamins, to the body.
Recent reports have also shown that gut microbes affect mineral metabolism of the host, involving calcium, iron, magnesium, selenium, copper, zinc, and silver (98–108). Generally, the gut microbiome regulates the absorption of minerals, such as iron and calcium (109–111), helping them achieve a good balance for health. In turn, these minerals also have a great effect on the gut microbiome. For example, iron is responsible for intestinal bacteria to extract energy from nutrients obtained by the host (112). Studies have shown that the normal gut microbiome can improve the utilization of dietary iron by translating ellagic acid (EA) into urolithin A (UA), which does not bind Fe3+ and still maintains the biological function in the presence of Fe3+. UA inhibits the production of reactive oxygen species (ROS), and its increased synthesis has a positive impact on the health by protecting the host from oxidative stress and inflammation (113). Besides, due to the excreted p-hydroxyphenyllactic acid, Lactobacillus fermentum residing in the gut exhibits iron-reducing activity, catalyzing Fe3+ to Fe2+ (101). Fe2+, unlike Fe3+, can be absorbed by the host's enterocytes (114). In other words, the intestinal microbiota optimizes the dietary non-heme iron conversion in the intestine not only by increasing the content of Fe3+, but also supporting the reduction of Fe3+ to Fe2+, thereby improving the utilization of iron (115). Similar to these, other minerals interact with the gut microbiome, and this good interaction is the key to maintaining health, but that doesn't mean everyone needs mineral supplements. The most appropriate dietary recommendations are self-monitoring and supplementation of minerals and vitamins when deficiencies are identified.
Food Additives
Food additives refer to artificial or natural substances added to food to improve the color, aroma, taste, as well as for the needs of anti-corrosion and special processing, including anti-caking agent, defoamer, acidity regulator, antioxidant, leavening agent, colorant, bleaching agent, enzyme preparation, flavor enhancer, color-protecting agent, preservative, sweetener, thickener, and spice etc. (116). More and more evidence showed that these food additives can disrupt the homeostasis of the gut, thus promoting tissue injury inflammatory response. For example, mice treated with emulsifiers carboxymethyl cellulose and polysorbate 80 developed biological disorders with overgrowth of mucus-degrading bacteria, leading to colitis in animals lacking interleukin-10 involving in anti-inflammatory and cell regulatory or toll-like receptor 5 (a cell receptor targeting bacterial flagellin) (117). Similarly, enhanced endoplasmic reticulum stress will be induced by maltodextrin in intestinal goblet cells, thus promoting mucus release and improving the host's susceptibility to colitis (118–121). Besides, by inducing changes in the composition and function of intestinal microflora, non-caloric artificial sweeteners (NAS) can lead to the development of glucose intolerance, even though it is regarded as very safe due to their low caloric content (122). Moreover, maternal exposure to NAS impacts progeny's metabolism and microbiome, including general downregulation of liver detoxification mechanisms and significant alterations in bacterial metabolites, posing a threat to the infant's metabolism (123). The potential harm of other artificial sweeteners should also not be ignored. Both of Splenda and Neotame can cause intestinal disorders, especially in people with Crohn's Disease-Like Ileitis (124, 125). Some dietary microparticles, such as titanium dioxide which is used as a colorant and food whitening agent, can inhibit macrophage phagocytic activity and work as adjuvants with bacterial stimuli, leading to the complex disorder of immune responses (126–128). The antimicrobial agent used for antisepsis is also unsafe. It has been well recognized that they can induce anxiety by remodeling gut microbiome (129, 130).
Although there are strict restrictions on the use of food additives in many countries (131, 132), the formulation of those standards is rarely based on systematic and rigorous scientific experiments (133). It may be wise to minimize the intake of food additives until the correlation between the dose and hazard of food additives is fully understood.
Cooking and Processing
Cooking and processing are essential parts of most foods before they are eaten. Although few studies measured the effects of them on the gut microbiome, some existing experimental results may provide us with a deeper understanding. Carmody et al. pointed out that raw or cooked plant feeds reshaped the gut microbiome of mice differently, and its impact was attributed to the improvement of starch digestibility and the degradation of plant-derived compounds, while changes in the gut microbiota regulated the host energy status and similar phenomenon can also be detected in humans (134). In another more detailed study, the effects of three different cooking methods on gut microbiome were compared and analyzed with five different foods. The results showed that, compared to milder treatments (boiling), intense cooking techniques (roasting and grilling) increased the abundance of beneficial bacteria, such as Ruminococcus spp. or Bifidobacterium spp. However, for some foods (bananas or bread), intense cooking can reduce the level of healthy bacteria (135). Also, eating red meat or processed meat is linked to an increased risk of colorectal cancer partly due to the interaction between gut microbiome and carcinogens (136, 137). On the other hand, cooking utensils can also cause the accumulation of harmful substances in the cooking and processing, especially the use of aluminum cookers. Thirty eight percentage of aluminum intake accumulates in intestinal mucosa and disturbs the normal regulation of intestinal permeability, intestinal flora and immunity (138, 139).
Effects of Gut Microbiome on Human Body Function and Diseases
Generally, almost all factors in the diet are closely related to the homeostasis of the gut microbiome, while unhealthy habit will definitely cause the decline of body function and even lead to pathological changes. The data of the recent decade's explosion clearly described the relationship between the gut microbiome and health from multiple perspectives, and explain the mechanism of many specific intestinal microorganisms in the development of diseases (32, 140). Dysbiosis of gut microbiome is closely related with gastrointestinal diseases (141), bone (142), mental (143, 144), aging-related inflammation (145), cancer (146), cardiovascular diseases (147, 148), circulatory rhythms (149), metabolic diseases (150–152), etc. Beyond to this, the co-evolution between gut microbiome benefits human a lot (153–155), including fighting against pathogens, stimulating the immunity (156–158), maintaining the intestinal barrier integrity, and generating micronutrients (160).
It is well-acknowledged that the diversity of gut microbiome is positively correlated with health, and a good gut microbiome not only keeps us from getting sick but also makes our bodies work more smoothly. For example, the metabolites of the gut microbiome can regulate a variety of physiological activities and have a strong signal transduction function (159). Microbial-derived SCFAs (butyrate, propionate, and acetate), appear in specific amounts, and their proportions will vary according to age, diet, and disease (160). The formation of SCFA is the result of the complex interaction between diet and the gut microbiota in the environment of the intestinal cavity. The level of SCFAs is largely affected by the proportion of intestinal commensal bacteria, and its dysbiosis can lead to unbalanced SCFAs, which serve as the main communication medium between the gut microbiota and the immune system (161). SCFAs also promote epithelial metabolism and decreases intracellular O2, contributing to the stabilization of HIF-1 (a transcription factor) and epithelial barrier function (162). It should be noted that the gut microbiome produces many other kinds of metabolites, such as bile acids and amino acid derivatives, which may also have important signaling functions (163). For example, gut microbiome-related bile acid metabolism regulates liver cancer via natural killer T cells (164, 165), suggesting these metabolic pathways associated with gut microbes may become an important target of precision medicine. However, in some abnormal intestinal conditions, the rapid increase of microbes-deprived metabolites may cause many diseases (166, 167). Unfortunately, the existing technology and analysis methods are still difficult to accurately locate the strains that play a key role. Therefore, more studies are needed to explore the core interactions between disease and the gut microbiome. But until all the mechanisms have been elucidated, it seems that we can enjoy the benefits of regulating the gut microbiome early, through a potentially harmless approach–dietary intervention.
Dietary Intervention in Diseases
Recent studies have demonstrated that dietary intervention can significantly regulate the structure and function of the gut microbiome, and contribute to the health of gut microbiome and its host. A dietary intervention (calorie restriction) in obesity improved the abundance of Akkermansia muciniphila and then promoted metabolic health, helping to achieve good weight loss (168). Dietary fiber (mainly fructans and galacto-oligosaccharides) intervention increases the fecal abundance of Bifidobacterium and Lactobacillus spp, suggesting the possibility of precisely regulating certain microorganisms through specific dietary formulas (169). Besides, dietary intervention using functional foods decreased metabolic endotoxaemia and reduced biochemical abnormalities by improving gut microbiome in people suffering from type 2 diabetes, demonstrating that a high-fiber, polyphenol-enriched, and vegetable-protein-based diet may work as a potential therapy for the improvement of glycaemic control, dyslipidaemia, and inflammation (170, 171). Also, anti-inflammatory diets may reduce neuroinflammation through several indirect immune pathways from the gut microbiome and systemic circulation, introducing a new way to control Alzheimer's disease (AD) and neurodegeneration (172). All these data tell us that reasonable diet intervention may be an effective means to alleviate diseases or maintain health. The research of microbiome can not only help us to determine the microbes and dietary patterns that are directly beneficial to the body but also can be used as an indicator to predict the progress of disease and help us carry out the effective intervention in time. In the process of tackling the obesity pandemic, a lot of efforts have been devoted to formulating effective weight loss strategies. However, many dieters have failed to maintain weight loss for a long time and instead experienced excessive weight recovery cycles. The mechanism leading to the relapse of obesity after dieting remains largely elusive. Thaiss et al. developed a machine learning algorithm that can make personalized microbiome-based predictions on the degree of weight recovery after dieting, and found that the microbiome helps reduce flavonoid levels and energy consumption. And proved that flavonoid-based “post-biological” interventions have improved the secondary excessive weight gain (173). In other words, real-time and accurate tracking of microbiome dynamic changes is also necessary for timely and effective dietary intervention.
More than that, more and more studies show that a more appropriate diet can effectively improve physical function and even significantly reduce all-cause mortality. Recent evidence in mouse models shows that physical and emotional stress during exercise is highly correlated with changes in the microbial composition of the gastrointestinal tract. For example, induced exercise stress reduced Turicibacter spp. in the cecum but increased Ruminococcus gnavus, which has a clear role in intestinal mucus degradation and immune function (1, 174), providing an effective reference for athletes to solve fatigue, mood disturbances, underperformance and gastrointestinal distress. More importantly, a reasonable diet plan can help athletes shape gut microbiome which is more conducive to lactic acid degradation, which can effectively improve their exercise performance and achieve better results (175, 176). Similarly, dietary intervention is also suitable for ordinary people to improve their health and significantly reduce the incidence rate of many diseases (177, 178), so gut microbes can really tell you what to eat.
Conclusion
Factors in the diet, including different dietary components (carbohydrates, fats, proteins, minerals, vitamins, etc.), food additives, cooking and processing, can change the structure and function of the gut microbiome, and these changes are closely related to maintaining the health of the body. Long term unhealthy eating habits, such as western diet, are an important factor in a variety of non-communicable diseases. Many years of research has depicted the basic principles of the interaction between diet and gut microbiome, while the dietary intervention program based on this has been proved to be effective. However, it cannot be ignored that many factors outside the diet that will also affect the composition of the gut microbiome, including age, genetics, smoking, sports activities and the like, so it is very challenging to accurately determine the specific role of diet in diseases. Also, it is difficult to draw definite conclusions on the therapeutic benefits of diet intervention for chronic diseases. As our review shows, most studies have been conducted on animals, and only a few human intervention studies exist. More randomized controlled studies are needed to ensure that enough subjects participate in the trial to fully understand the relationship between diet, gut microbiome and health.
Author Contributions
QS draft the manuscript. QL provided critical comments on the manuscript.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
1. Clark A, Mach N. Exercise-induced stress behavior, gut-microbiome-brain axis and diet: a systematic review for athletes. Int Soc Sports Nutr. (2016) 13:43. doi: 10.1186/s12970-016-0155-6
2. Redondo-Useros N, Nova E, González-Zancada N, Díaz LE, Gómez-Martínez S, Marcos A. Microbiome and lifestyle: a special focus on diet. Nutrients. (2020) 12:1776. doi: 10.3390/nu12061776
3. WHO. Resolutions Prevention and Control of Non-Communicable Diseases. Available online at: https://www.who.int/nmh/events/un_ncd_summit2011/resolutions/en/ (accessed December 8, 2019).
4. West CE, Renz H, Jenmalm MC, Kozyrskyj AL, Allen KJ, Vuillermin P, et al. The gut microbiome and inflammatory noncommunicable diseases: associations and potentials for gut microbiome therapies. J Allergy Clin Immunol. (2015) 135:3–13. doi: 10.1016/j.jaci.2014.11.012
5. McGrattan AM, McGuinness B, McKinley MC, Kee F, Passmore P, Woodside JV, et al. Diet and inflammation in cognitive ageing and Alzheimer's Disease. Curr Nutr Rep. (2019) 8:53–65. doi: 10.1007/s13668-019-0271-4
6. Mohajeri MH, Brummer RJM, Rastall RA, Weersma RK, Harmsen HJM, Faas M, et al. The role of the microbiome for human health: from basic science to clinical applications. Euro J Nutr. (2018) 57:1–14. doi: 10.1007/s00394-018-1703-4
7. Yu E, Malik VS, Hu FB. Reprint of: cardiovascular disease prevention by diet modification: JACC health promotion series. J Am Coll Cardiol. (2018) 72:2951–63. doi: 10.1016/j.jacc.2018.10.019
8. Milani C, Duranti S, Bottacini F, Casey E, Turroni F, Mahony J, et al. The first microbial colonizers of the human gut: composition, activities, and health implications of the infant gut microbiome. Microbiol Mol Biol Rev. (2017) 81:e00036–e00017. doi: 10.1128/MMBR.00036-17
9. Hunt KM, Foster JA, Forney LJ, Schütte UM, Beck DL, Abdo Z, et al. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS ONE. (2011) 6:e21313. doi: 10.1371/journal.pone.0021313
10. Fujimura KE, Sitarik AR, Havstad S, Lin DL, Levan S, Fadrosh D, et al. Neonatal gut microbiome associates with childhood multisensitized atopy and T cell differentiation. Nat Med. (2016) 22:1187–91. doi: 10.1038/nm.4176
11. Moles L, Gómez M, Heilig H, Bustos G, Fuentes S, de Vos W, et al. Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiome during the first month of life. PLoS ONE. (2013) 8:e66986. doi: 10.1371/journal.pone.0066986
12. Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M, Li H, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. (2016) 8:343ra382. doi: 10.1126/scitranslmed.aad7121
13. Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. (2015) 17:852. doi: 10.1016/j.chom.2015.05.012
14. Million M, Diallo A, Raoult D. Gut microbiome and malnutrition. Microb Pathog. (2017) 106:127–38. doi: 10.1016/j.micpath.2016.02.003
15. Mancino W, Duranti S, Mancabelli L, Longhi G, Anzalone R, Milani C, et al. Bifidobacterial transfer from mother to child as examined by an animal model. Microorganisms. (2019) 7:293. doi: 10.3390/microorganisms7090293
16. Lawson MAE, O'Neill IJ, Kujawska M, Gowrinadh JS, Wijeyesekera A, Flegg Z, et al. Breast milk-derived human milk oligosaccharides promote bifidobacterium interactions within a single ecosystem. ISME J. (2020) 14:635–48. doi: 10.1038/s41396-019-0553-2
17. Jagodzinski A, Zielinska E, Laczmanski L, Hirnle L. The early years of life. Are they influenced by our microbiome? Ginekol Pol. (2019) 90:228–32. doi: 10.5603/GP.2019.0041
18. Dinan TG, Cryan JF. Gut instincts: microbiome as a key regulator of brain development, ageing and neurodegeneration. J Physiol. (2017) 595:489–503. doi: 10.1113/JP273106
19. Houghton D, Stewart CJ, Day CP, Trenell M. Gut microbiome and lifestyle interventions in NAFLD. Int J Mol Sci. (2016) 17:447. doi: 10.3390/ijms17040447
20. Nguyen KN, Edward CD, Zhengxiao Z, Mingliang J, Nami B, Maria EPM, et al. Gut microbiome modulation with long-chain corn bran arabinoxylan in adults with overweight and obesity is linked to an individualized temporal increase in fecal propionate. Microbiome. (2020) 8:118. doi: 10.1186/s40168-020-00887-w
21. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf HAL, Goodman JC, et al. The long-term stability of the human gut microbiome. Science. (2013) 341:1237439. doi: 10.1126/science.1237439
22. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. (2014) 505:559–63. doi: 10.1038/nature12820
23. Carmody RN, Gerber GK, Luevano JM, Gatti DM, Somes L, Svenson KL, et al. Diet dominates host genotype in shaping the murine gut microbiome. Cell Host Microbe. (2015) 17:72–84. doi: 10.1016/j.chom.2014.11.010
24. Fragiadakis GK, Smits SA, Sonnenburg ED, Van TW, Reid G, Knight R, et al. Links between environment, diet, and the hunter-gatherer microbiome. Gut Microbes. (2019) 10:216–27. doi: 10.1080/19490976.2018.1494103
25. Smits SA, Leach J, Sonnenburg ED, Gonzalez CG, Lichtman JS, Reid G, et al. Seasonal cycling in the gut microbiome of the hadza hunter-gatherers of Tanzania. Science. (2017) 357:802–806. doi: 10.1126/science.aan4834
26. Noce A, Marrone G, Di DF, Ottaviani E, Wilson JG, Bernini R, et al. Impact of gut microbiome composition on onset and progression of chronic non-communicable diseases. Nutrients. (2019) 11:1073. doi: 10.3390/nu11051073
27. Abbasi A. Are non-communicable diseases chronically communicable: a role for the human microbiome? Med Hypotheses. (2017) 104:126–27. doi: 10.1016/j.mehy.2017.06.002
28. Sirisinha S. The potential impact of gut microbiome on your health: current status and future challenges. Asian Pac J Allergy Immunol. (2016) 34:249–64. doi: 10.12932/AP0803
29. Zinöcker MK, Lindseth IA. The western diet-microbiome-host interaction and its role in metabolic disease. Nutrients. (2018) 10:365. doi: 10.3390/nu10030365
30. Zhu C, Sawrey-Kubicek L, Beals E, Rhodes CH, Houts HE, Sacchi R, et al. Human gut microbiome composition and tryptophan metabolites were changed differently by fast food and Mediterranean diet in 4 days: a pilot study. Nutr Res. (2020) 77:62–72. doi: 10.1016/j.nutres.2020.03.005
31. Bortolin RC, Vargas AR, Gasparotto J, Chaves PR, Schnorr CE, Martinello KB, et al. A new animal diet based on human Western diet is a robust diet-induced obesity model: comparison to high-fat and cafeteria diets in term of metabolic and gut microbiome disruption. Int J Obes. (2018) 42:525–34. doi: 10.1038/ijo.2017.225
32. Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med. (2016) 375:2369–79. doi: 10.1056/NEJMra1600266
33. Zeevi D, Korem T, Zmora N, Israeli D, Rothschild D, Weinberger A, et al. Personalized nutrition by prediction of glycemic responses. Cell. (2015) 163:1079–94. doi: 10.1016/j.cell.2015.11.001
34. Shoaie S, Ghaffari P, Kovatcheva-Datchary P, Mardinoglu A, Sen P, Pujos-Guillot E, et al. Quantifying diet-induced metabolic changes of the human gut microbiome. Cell Metab. (2015) 22:320–31. doi: 10.1016/j.cmet.2015.07.001
35. Torres-Fuentes C, Schellekens H, Dinan TG, Cryan JF. The microbiome-gut-brain axis in obesity. Lancet Gastroenterol Hepatol. (2017) 2:747–56. doi: 10.1016/S2468-1253(17)30147-4
36. Clercq NC, Groen AK, Romijn JA, Nieuwdorp M. Gut microbiome in obesity and undernutrition. Adv Nutr. (2016) 7:1080–9. doi: 10.3945/an.116.012914
37. Maruvada P, Leone V, Kaplan LM, Chang EB. The human microbiome and obesity: moving beyond associations. Cell Host Microbe. (2017) 22:589–99. doi: 10.1016/j.chom.2017.10.005
38. Cryan JF, O'Riordan KJ, Sandhu K, Peterson V, Dinan TG. The gut microbiome in neurological disorders. Lancet Neurol. (2020) 19:179–94. doi: 10.1016/S1474-4422(19)30356-4
39. Peretti S, Mariano M, Mazzocchetti C, Mazza M, Pino MC, Verrotti DPA. Diet: the keystone of autism spectrum disorder? Nutr Neurosci. (2019) 22:825–39. doi: 10.1080/1028415X.2018.1464819
41. Sonnenburg ED, Sonnenburg JL. Starving our microbial self: the deleterious consequences of a diet deficient in microbiome-accessible carbohydrates. Cell Metab. (2014) 20:779–86. doi: 10.1016/j.cmet.2014.07.003
42. Trowell HC. Review dietary-fiber hypothesis of the etiology of diabetes mellitus. Diabetes. (1975) 24:762–5. doi: 10.2337/diab.24.8.762
43. Jenkins DJ, Goff DV, Leeds AR, Alberti KG, Wolever TM, Gassull MA, et al. Unabsorbable carbohydrates and diabetes: decreased post-prandial hyperglycaemia. Lancet. (1976) 2:172–4. doi: 10.1016/S0140-6736(76)92346-1
44. Marcobal A, Barboza M, Froehlich JW, Block DE, German JB, Lebrilla CB, et al. Consumption of human milk oligosaccharides by gut-related microbes. J Agric Food Chem. (2010) 58:5334–40. doi: 10.1021/jf9044205
45. Vandenplas Y, De Greef E, Veereman G. Prebiotics in infant formula. Gut Microbes. (2014) 5:681–9. doi: 10.4161/19490976.2014.972237
46. Macfarlane GT, Gibson GR. Carbohydrate fermentation, energy transduction and gas metabolism in the human large intestine. In: Mackie RI, White BA, eds. Ecology and Physiology of Gastrointestinal Microbes: Gastrointestinal Fermentations and Ecosystems, Vol. 1. New York, NY: Chapman & Hall (1996). p. 269–318. doi: 10.1007/978-1-4615-4111-0_9
47. Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol. (2008) 6:121–31. doi: 10.1038/nrmicro1817
48. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther. (2007) 27:104–19. doi: 10.1111/j.1365-2036.2007.03562.x
49. Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. (2016) 165:1332–45. doi: 10.1016/j.cell.2016.05.041
50. Scott KP, Duncan SH, Flint HJ. Dietary fibre and the gut microbiome. Nutr Bull. (2008) 33:201–11. doi: 10.1111/j.1467-3010.2008.00706.x
51. Duncan SH, Louis P, Thomson JM, Flint HJ. The role of pH in determining the species composition of the human colonic microbiome. Environ Microbiol. (2009) 11:2112–22. doi: 10.1111/j.1462-2920.2009.01931.x
52. Daïen CI, Pinget GV, Tan JK, Macia L. Detrimental impact of microbiome-accessible carbohydrate-deprived diet on gut and immune homeostasis: an overview. Front Immunol. (2017) 8:548. doi: 10.3389/fimmu.2017.00548
53. Desai MS, Seekatz AM, Koropatkin NM, Kamada N, Hickey CA, Wolter M. A dietary fiber-deprived gut microbiome degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell. (2016) 167:1339–53.e21. doi: 10.1016/j.cell.2016.10.043
54. Weickert MO, Pfeiffer AFH. Impact of dietary fiber consumption on insulin resistance and the prevention of type 2 diabetes. J Nutr. (2018) 148:7–12. doi: 10.1093/jn/nxx008
55. Bermudez-Brito M, Faas MM, de Vos P. Modulation of dendritic-epithelial cell responses against sphingomonas paucimobilis by dietary fibers. Sci Rep. (2016) 6:30277. doi: 10.1038/srep30277
56. Simpson HL, Campbell BJ. Review article: dietary fibre–microbiome interactions. Aliment Pharmacol Ther. (2015) 42:158–79. doi: 10.1111/apt.13248
57. Leone V, Gibbons SM, Martinez K, Hutchison AL, Huang EY, Cham CM, et al. Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe. (2015) 17:681–9. doi: 10.1016/j.chom.2015.03.006
58. Semova I, Carten JD, Stombaugh J, Mackey LC, Knight R, Farber SA, et al. Microbiome regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microbe. (2012) 12:277–88. doi: 10.1016/j.chom.2012.08.003
59. Bionaz M, Vargas-Bello-Pérez E, Busato S. Advances in fatty acids nutrition in dairy cows: from gut to cells and effects on performance. J Anim Sci Biotechnol. (2020) 11:110. doi: 10.1186/s40104-020-00512-8
60. Min Y, Ma X, Sankaran K, Ru Y, Chen L, Baiocchi M, et al. Sex-specific association between gut microbiome and fat distribution. Nat Commun. (2019) 10:2408. doi: 10.1038/s41467-019-10440-5
61. Yoshimoto S, Loo TM, Atarashi K, Kanda H, Sato S, Oyadomari S, et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature. (2013) 499:97–101. doi: 10.1038/nature12347
62. Ridlon JM, Kang DJ, Hylemon PB. Bile salt biotransformations by human intestinal bacteria. J Lipid Res. (2006) 47:241–59. doi: 10.1194/jlr.R500013-JLR200
63. Islam KB, Fukiya S, Hagio M, Fujii N, Ishizuka S, Ooka T, et al. Bile acid is a host factor that regulates the composition of the cecal microbiome in rats. Gastroenterology. (2011) 141:1773–81. doi: 10.1053/j.gastro.2011.07.046
64. Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature. (2012) 487:104–8. doi: 10.1038/nature11225
65. Wan Y, Wang F, Yuan J, Li J, Jiang D, Zhang J, et al. Effects of dietary fat on gut microbiome and faecal metabolites, and their relationship with cardiometabolic risk factors: a 6-month randomised controlled-feeding trial. Gut. (2019) 68:1417–29. doi: 10.1136/gutjnl-2018-317609
66. Jenq RR, Taur Y, Devlin SM, Ponce DM, Goldberg JD, Ahr KF, et al. Intestinal blautia is associated with reduced death from graft-versus-host disease. Biol Blood Marrow Transplant. (2015) 21:1373–83. doi: 10.1016/j.bbmt.2015.04.016
67. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiome analysis of crohn disease patients. Proc Natl Acad Sci USA. (2008) 105:16731–6. doi: 10.1073/pnas.0804812105
68. Miquel S, Martín R, Rossi O, Bermúdez-Humarán LG, Chatel JM, Sokol H, et al. Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol. (2013) 16:255–61. doi: 10.1016/j.mib.2013.06.003
69. Chu DM, Antony KM, Ma J, Prince AL, Showalter L, Moller M, et al. The early infant gut microbiome varies in association with a maternal high-fat diet. Genome Med. (2016) 8:77. doi: 10.1186/s13073-016-0330-z
70. Hyoju SK, Adriaansens C, Wienholts K, Sharma A, Keskey R, Arnold W, et al. Low-fat/high-fibre diet prehabilitation improves anastomotic healing via the microbiome: an experimental model. Br J Surg. (2020) 107:743–55. doi: 10.1002/bjs.11388
71. Guerville M, Hamilton MK, Ronveaux CC, Ellero-Simatos S, Raybould HE, Boudry G. Chronic refined low-fat diet consumption reduces cholecystokinin satiation in rats. Eur J Nutr. (2019) 58:2497–510. doi: 10.1007/s00394-018-1802-2
72. Wang J, Ji H. Influence of probiotics on dietary protein digestion and utilization in the gastrointestinal tract. Curr Protein Pept Sci. (2019) 20:125–31. doi: 10.2174/1389203719666180517100339
73. Chen H, Wierenga PA, Hendriks WH, Jansman AJM. In vitro protein digestion kinetics of protein sources for pigs. Animal. (2019) 13:1154–64. doi: 10.1017/S1751731118002811
74. Hughes R, Magee EA, Bingham S. Protein degradation in the large intestine: relevance to colorectal cancer. Curr Issues Intest Microbiol. (2000) 1:51–8.
75. Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters EC, et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sic USA. (2009) 106:3698–703. doi: 10.1073/pnas.0812874106
76. Fan P, Li L, Rezaei A, Eslamfam S, Che D, Ma X. Metabolites of dietary protein and peptides by intestinal microbes and their impacts on gut. Curr Protein Pept Sci. (2015) 16:646–54. doi: 10.2174/1389203716666150630133657
77. Zhao J, Zhang X, Liu H, Brown MA, Qiao S. dietary protein and gut microbiome composition and function. Curr Protein Pept Sci. (2019) 20:145–54. doi: 10.2174/1389203719666180514145437
78. Ma N, Tian Y, Wu Y, Ma X. Contributions of the interaction between dietary protein and gut microbiome to intestinal health. Curr Protein Pept Sci. (2017) 18:795–808. doi: 10.2174/1389203718666170216153505
79. O'Keefe SJ. Diet, microorganisms and their metabolites, colon cancer. Nat Rev Gastroenterol Hepatol. (2016) 13:691–706. doi: 10.1038/nrgastro.2016.165
80. Mehta RS, Nishihara R, Cao Y, Song M, Mima K, Qian ZR, et al. Association of Dietary patterns with risk of colorectal cancer subtypes classified by Fusobacterium nucleatum in tumor tissue. JAMA Oncol. (2017) 3:921–7. doi: 10.1001/jamaoncol.2016.6374
81. Tápparo DC, Rogovski P, Cadamuro RD, Marques Souza DS, Bonatto C, Frumi Camargo A, et al. Nutritional, energy and sanitary aspects of swine manure and carcass co-digestion. Front Bioeng Biotechnol. (2020) 8:333. doi: 10.3389/fbioe.2020.00333
82. Gilbert MS, Ijssennagger N, Kies AK, van Mil SWC. Protein fermentation in the gut; implications for intestinal dysfunction in humans, pigs, and poultry. Am J Physiol Gastrointest Liver Physiol. (2018) 315:G159–70. doi: 10.1152/ajpgi.00319.2017
83. Rideout TC, Fan MZ, Cant JP, Wagner-Riddle C, Stonehouse P. Excretion of major odor-causing and acidifying compounds in response to dietary supplementation of chicory inulin in growing pigs. J Anim Sci. (2004) 82:1678–84. doi: 10.2527/2004.8261678x
84. An C, Kuda T, Yazaki T, Takahashi H, Kimura B. Caecal environment of rats fed far east asian-modelled diets. Appl Microbiol Biotechnol. (2014) 98:4701–9. doi: 10.1007/s00253-014-5535-8
85. Kiilerich P, Myrmel LS, Fjære E, Hao Q, Hugenholtz F, Sonne SB, et al. Effect of a long-term high-protein diet on survival, obesity development, and gut microbiome in mice. Am J Physiol Endocrinol Metab. (2016) 310:E886–99. doi: 10.1152/ajpendo.00363.2015
86. Ko GJ, Rhee CM, Kalantar-Zadeh K, Joshi S. The effects of high-protein diets on kidney health and longevity. J Am Soc Nephrol. (2020) 31:1667–79. doi: 10.1681/ASN.2020010028
87. Pallister T, Spector TD. Food: a new form of personalised (gut microbiome) medicine for chronic diseases? J R Soc Med. (2016) 109:331–6. doi: 10.1177/0141076816658786
88. Kaidar-Person O, Person B, Szomstein S, Rosenthal RJ. Nutritional deficiencies in morbidly obese patients: a new form of malnutrition? Part A: vitamins. Obes Surg. (2008) 18:870–6. doi: 10.1007/s11695-007-9349-y
89. Xanthakos SA. Nutritional deficiencies in obesity and after bariat ric surgery. Pediatr Clin North Am. (2009) 56:1105–21. doi: 10.1016/j.pcl.2009.07.002
90. Signori C, Zalesin KC, Franklin B, Miller WL, McCullough PA. Effect of gastric bypass on vitamin D and secondary hyperparathyroidism. Obes Surg. (2010) 20:949–52. doi: 10.1007/s11695-010-0178-z
91. Enos RT, Davis JM, Velázquez KT, McClellan JL, Day SD, Carnevale KA. Influence of dietary saturated fat content on adiposity, macrophage behavior, inflammation, and metabolism: composition matters. J Lipid Res. (2013) 54:152–63. doi: 10.1194/jlr.M030700
92. Pannu PK, Calton EK, Soares MJ. Calcium and vitamin d in obesity and related chronic disease. Adv Food Nutr Res. (2016) 77:57–100. doi: 10.1016/bs.afnr.2015.11.001
93. Guo C, Sinnott B, Niu B, Lowry MB, Fantacone ML, Gombart AF. Synergistic induction of human cathelicidin antimicrobial peptide gene expression by vitamin D and stilbenoids. Mol Nutr Food Res. (2014) 58:528–36. doi: 10.1002/mnfr.201300266
94. Cantorna MT, McDaniel K, Bora S, Chen J, James J. Vitamin D. immune regulation, the microbiome, and inflammatory bowel disease. Exp Biol Med. (2014) 239:1524–30. doi: 10.1177/1535370214523890
95. Cantorna MT, Munsick C, Bemiss C, Mahon BD. 1,25-Dihydroxycholecalciferol prevents and ameliorates symptoms of experimental murine inflammatory bowel disease. J Nutr. (2000) 130:2648–52. doi: 10.1093/jn/130.11.2648
96. Jørgensen SP, Agnholt J, Glerup H, Lyhne S, Villadsen GE, Hvas CL. Clinical trial: vitamin D3 treatment in Crohn's disease - a randomized double-blind placebo-controlled study. Aliment Pharmacol Ther. (2010) 32:377–83. doi: 10.1111/j.1365-2036.2010.04355.x
97. Guss JD, Taylor E, Rouse Z, Roubert S, Higgins CH, Thomas CJ, et al. The microbial metagenome and bone tissue composition in mice with microbiome-induced reductions in bone strength. Bone. (2019) 127:146–54. doi: 10.1016/j.bone.2019.06.010
98. Ohlsson C, Engdahl C, Fåk F, Andersson A, Windahl SH, Farman HH, et al. Probiotics protect mice from ovariectomy-induced cortical bone loss. PLoS ONE. (2014) 9:e92368. doi: 10.1371/journal.pone.0092368
99. Chaplin A, Parra P, Laraichi S, Serra F, Palou A. Calcium supplementation modulates gut microbiome in a prebiotic manner in dietary obese mice. Mol Nutr Food Res. (2016) 60:468–80. doi: 10.1002/mnfr.201500480
100. Laparra JM, Olivares M, Sanz Y. Oral administration of Bifidobacterium longum CECT 7347 ameliorates gliadin-induced alterations in liver iron mobilisation. Br J Nutr. (2013) 110:1828–36. doi: 10.1017/S0007114513001098
101. González A, Gálvez N, Martín J, Reyes F, Pérez-Victoria I, Dominguez-Vera JM. Identification of the key excreted molecule by Lactobacillus fermentum related to host iron absorption. Food Chem. (2017) 228:374–80. doi: 10.1016/j.foodchem.2017.02.008
102. Winther G, Pyndt Jørgensen BM, Elfving B, Nielsen DS, Kihl P, Lund S, et al. Dietary magnesium deficiency alters gut microbiome and leads to depressive-like behaviour. Acta Neuropsychiatr. (2015) 27:168–76. doi: 10.1017/neu.2015.7
103. Yang Y, Huang S, Wang J, Jan G, Jeantet R, Chen XD. Mg2+ improves the thermotolerance of probiotic Lactobacillus rhamnosus GG. Lactobacillus casei Zhang and Lactobacillus plantarum P-8. Lett Appl Microbiol. (2017) 64:283–8. doi: 10.1111/lam.12716
104. Lavu RVS, Van De Wiele T, Pratti VL, Tack F, Du LG. Selenium bioaccessibility in stomach, small intestine and colon: comparison between pure Se compounds, Se-enriched food crops and food supplements. Food Chem. (2016) 197:382–7. doi: 10.1016/j.foodchem.2015.08.001
105. Pieniz S, Andreazza R, Mann MB, Camargo F, Brandelli A. Bioaccumulation and distribution of selenium in Enterococcus durans. J Trace Elem Med Biol. (2017) 40:37–45. doi: 10.1016/j.jtemb.2016.12.003
106. Agga GE, Scott HM, Vinasco J, Nagaraja TG, Amachawadi RG, Bai J, et al. Effects of chlortetracycline and copper supplementation on the prevalence, distribution, and quantity of antimicrobial resistance genes in the fecal metagenome of weaned pigs. Prev Vet Med. (2015) 119:179–89. doi: 10.1016/j.prevetmed.2015.02.008
107. Reed S, Neuman H, Moscovich S, Glahn RP, Koren O, Tako E. Chronic zinc deficiency alters chick gut microbiome composition and function. Nutrients. (2015) 7:9768–84. doi: 10.3390/nu7125497
108. Zackular JP, Moore JL, Jordan AT, Juttukonda LJ, Noto MJ, Nicholson MR, et al. Dietary zinc alters the microbiome and decreases resistance to Clostridium difficile infection. Nat Med. (2016) 22:1330–4. doi: 10.1038/nm.4174
109. Mogna L, Pane M, Nicola S, Raiteri E. Screening of different probiotic strains for their in vitro ability to metabolise oxalates. J Clin Gastroenterol. (2014) 48:91–5. doi: 10.1097/MCG.0000000000000228
110. Deschemin JC, Noordine ML, Remot A, Willemetz A, Afif C, Canonne-Hergaux F, et al. The microbiome shifts the iron sensing of intestinal cells. FASEB J. (2016) 30:252–61. doi: 10.1096/fj.15-276840
111. Kłobukowski JA, Skibniewska KA, Kowalski IM. Calcium bioavailability from dairy products and its release from food by in vitro digestion. J Elementol. (2014) 277–88. doi: 10.5601/jelem.2014.19.1.436
112. Dostal A, Lacroix C, Bircher L, Pham VT, Follador R, Zimmermann MB, et al. Iron modulates butyrate production by a child gut microbiome in vitro. MBio. (2015) 6:e01453–e01415. doi: 10.1128/mBio.01453-15
113. Saha P, Yeoh BS, Singh R, Chandrasekar B, Vemula PK, Haribabu B, et al. Gut microbiome conversion of dietary ellagic acid into bioactive phytoceutical urolithin A inhibits heme peroxidases. PLoS ONE. (2016) 11:e0156811. doi: 10.1371/journal.pone.0156811
114. Silva B, Faustino P. An overview of molecular basis of iron metabolism regulation and the associated pathologies. BBA Mol Basis Dis. (2015) 1852:1347–59. doi: 10.1016/j.bbadis.2015.03.011
115. Skrypnik K, Suliburska J. Association between the gut microbiome and mineral metabolism. J Sci Food Agric. (2017) 98:2449–60. doi: 10.1002/jsfa.8724
116. EC. Council Directive on the Approximation of the Rules of the Member States Concerning the Colouring Matters Authorized for Use in Foodstuffs Intended for Human Consumption. Available online at: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A31962L2645 (accessed September 10, 2019).
117. Chassaing B, Koren O, Goodrich JK, Poole AC, Srinivasan S, Ley RE, et al. Dietary emulsifiers impact the mouse gut microbiome promoting colitis and metabolic syndrome. Nature. (2015) 519:92–6. doi: 10.1038/nature14232
118. Thymann T, Moller HK, Stoll B, Stoy AC, Buddington RK, Bering SB, et al. Carbohydrate maldigestion induces necrotizing enterocolitis in preterm pigs. Am J Physiol Gastrointest Liver Physiol. (2009) 297:G1115–25. doi: 10.1152/ajpgi.00261.2009
119. Nickerson KP, McDonald C. Crohn's disease-associated adherent-invasive Escherichia coli adhesion is enhanced by exposure to the ubiquitous dietary polysaccharide maltodextrin. PLoS ONE. (2012) 7:e52132. doi: 10.1371/journal.pone.0052132
120. Nickerson KP, Homer CR, Kessler SP, Dixon LJ, Kabi A, Gordon IO, et al. The dietary polysaccharide maltodextrin promotes salmonella survival and mucosal colonization in mice. PLoS ONE. (2014) 9:e101789. doi: 10.1371/journal.pone.0101789
121. Laudisi F, Di Fusco D, Dinallo V, Stolfi C, Di Grazia A, Marafini I, et al. The food additive maltodextrin promotes endoplasmic reticulum stress-driven mucus depletion and exacerbates intestinal inflammation. Cell Mol Gastroenterol Hepatol. (2019) 7:457–73. doi: 10.1016/j.jcmgh.2018.09.002
122. Suez J, Korem T, Zeevi D, Zilberman-Schapira G, Thaiss CA, Maza O, et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiome. Nature. (2014) 514:181–6. doi: 10.1038/nature13793
123. Olivier-Van Stichelen S, Rother KI, Hanover JA. Maternal exposure to non-nutritive sweeteners impacts progeny's metabolism and microbiome. Front Microbiol. (2019) 10:1360. doi: 10.3389/fmicb.2019.01360
124. Rodriguez-Palacios A, Harding A, Menghini P, Himmelman C, Retuerto M, Nickerson KP, et al. The artificial sweetener splenda promotes gut proteobacteria, dysbiosis, and myeloperoxidase reactivity in crohn's disease-like ileitis. Inflamm Bowel Dis. (2018) 24:1005–20. doi: 10.1093/ibd/izy060
125. Chi L, Bian X, Gao B, Tu P, Lai Y, Ru H, et al. Effects of the artificial sweetener neotame on the gut microbiome and fecal metabolites in mice. Molecules. (2018) 23:367. doi: 10.3390/molecules23020367
126. Butler M, Boyle JJ, Powell JJ, Playford RJ, Ghosh S. Dietary microparticles implicated in Crohn's disease can impair macrophage phagocytic activity and act as adjuvants in the presence of bacterial stimuli. Inflamm Res Off J Eur Histamine Res Soc. (2007) 56:353–61. doi: 10.1007/s00011-007-7068-4
127. Ruiz PA, Moron B, Becker HM, Lang S, Atrott K, Spalinger MR, et al. Titanium dioxide nanoparticles exacerbate DSS-induced colitis: role of the NLRP3 inflammasome. Gut. (2017) 66:1216–24. doi: 10.1136/gutjnl-2015-310297
128. Bettini S, Boutet-Robinet E, Cartier C, Comera C, Gaultier E, Dupuy J, et al. Food-grade TiO2 impairs intestinal and systemic immune homeostasis, initiates preneoplastic lesions and promotes aberrant crypt development in the rat colon. Sci Rep. (2017) 7:40373. doi: 10.1038/srep40373
129. Javurek AB, Suresh D, Spollen WG, Hart ML, Hansen SA, Ellersieck MR, et al. Gut dysbiosis and neurobehavioral alterations in rats exposed to silver nanoparticles. Sci Rep. (2017) 7:2822. doi: 10.1038/s41598-017-02880-0
130. Marques C, Fernandes I, Meireles M, Faria A, Spencer JPE, Mateus N. Gut microbiome modulation accounts for the neuroprotective properties of anthocyanins. Sci Rep. (2018) 8:11341. doi: 10.1038/s41598-018-29744-5
131. EEC. Council Directive on the Approximation of the Rules of the Member States Concerning the Colouring Matters Authorized for Use in Foodstuffs Intended for Human Consumption. Available online at: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A31962L2645 (accessed September 10, 2019).
132. Commission Regulation: No 1129/2011 of 11 November 2011 amending Annex II to Regulation (EC) No 1333/2008 of the European Parliament and of the Council by Establishing a Union List of Food Additives (Text With EEA Relevance). Available online: https://publications.europa.eu/en/publication-detail/-/publication/28cb4a37-b40e-11e3-86f9-01aa75ed71a1/language-en (accessed September 10, 2019).
133. GRAS Substances Database. Available online at: https://www.fda.gov/food/generally-recognized-safe-gras/gras-substances-scogs-database (accessed September 10, 2019).
134. Carmody RN, Bisanz JE, Bowen BP, Maurice CF, Lyalina S, Louie KB. Cooking shapes the structure and function of the gut microbiome. Nat Microbiol. (2019) 4:2052–63. doi: 10.1038/s41564-019-0569-4
135. Pérez-Burillo S, Pastoriza S, Jiménez-Hernández N, D'Auria G, Francino MP, Rufián-Henares JA. Effect of food thermal processing on the composition of the gut microbiome. J Agric Food Chem. (2018) 66:11500–9. doi: 10.1021/acs.jafc.8b04077
136. Bouvard V, Loomis D, Guyton KZ, Grosse Y, Ghissassi FE, Benbrahim-Tallaa L, et al. International agency for research on cancer monograph working group. Lancet Oncol. (2015) 16:1599–600. doi: 10.1016/S1470-2045(15)00444-1
137. Helmus DS, Thompson CL, Zelenskiy S, Tucker TC, Li L. Red meat-derived heterocyclic amines increase risk of colon cancer: a population-based case-control study. Nutr Cancer. (2013) 65:1141–50. doi: 10.1080/01635581.2013.834945
138. Vignal C, Desreumaux P, Body-Malapel M. Gut: an underestimated target organ for aluminum. Morphologie. (2016) 100:75–84. doi: 10.1016/j.morpho.2016.01.003
139. Miclotte L, Van de Wiele T. Food processing, gut microbiome and the globesity problem. Crit Rev Food Sci Nutr. (2020) 60:1769–82. doi: 10.1080/10408398.2019.1596878
140. Bhabatosh DAS, Nair GB. Homeostasis and dysbiosis of the gut microbiome in health and disease. J Biosci. (2019) 44:117. doi: 10.1007/s12038-019-9926-y
141. Gorkiewicz G, Moschen A. Gut microbiome: a new player in gastrointestinal disease. Virchows Arch. (2018) 472:159–72. doi: 10.1007/s00428-017-2277-x
142. Quach D, Britton RA. Gut microbiome and bone health. Adv Exp Med Biol. (2017) 1033:47–58. doi: 10.1007/978-3-319-66653-2_4
143. Peirce JM, Alviña K. The role of inflammation and the gut microbiome in depression and anxiety. J Neurosci Res. (2019) 97:1223–41. doi: 10.1002/jnr.24476
144. Dinan TG, Cryan JF. Brain-gut-microbiome axis and mental health. Psychosom Med. (2017) 79:920–6. doi: 10.1097/PSY.0000000000000519
145. Buford TW. Trust your gut: the gut microbiome in age-related inflammation, health, and disease. Microbiome. (2017) 5:80. doi: 10.1186/s40168-017-0296-0
146. Li W, Deng Y, Chu Q, Zhang P. Gut microbiome and cancer immunotherapy. Cancer Lett. (2019) 447:41–7. doi: 10.1016/j.canlet.2019.01.015
147. Ahmadmehrabi S, Tang WHW. Gut microbiome and its role in cardiovascular diseases. Curr Opin Cardiol. (2017) 32:761–6. doi: 10.1097/HCO.0000000000000445
148. Kappel BA, Federici M. Gut microbiome and cardiometabolic risk. Rev Endocr Metab Disord. (2019) 20:399–406. doi: 10.1007/s11154-019-09533-9
149. Voigt RM, Forsyth CB, Green SJ, Engen PA, Keshavarzian A. Circadian rhythm and the gut microbiome. Int Rev Neurobiol. (2016) 131:193–205. doi: 10.1016/bs.irn.2016.07.002
150. Sharma S, Tripathi P. Gut microbiome and type 2 diabetes: where we are and where to go? J Nutr Biochem. (2019) 63:101–8. doi: 10.1016/j.jnutbio.2018.10.003
151. Leong KSW, Derraik JGB, Hofman PL, Cutfield WS. Antibiotics, gut microbiome and obesity. Clin Endocrinol. (2018) 88:185–200. doi: 10.1111/cen.13495
152. Magnúsdóttir S, Thiele I. Modeling metabolism of the human gut microbiome. Curr Opin Biotechnol. (2018) 51:90–6. doi: 10.1016/j.copbio.2017.12.005
153. Shi N, Li N, Duan X, Niu H. Interaction between the gut microbiome and mucosal immune system. Mil Med Res. (2017) 4:14. doi: 10.1186/s40779-017-0122-9
154. Takiishi T, Fenero CIM, Câmara NOS. Intestinal barrier and gut microbiome: shaping our immune responses throughout life. Tissue Barriers. (2017) 5:e1373208. doi: 10.1080/21688370.2017.1373208
155. Thaiss CA, Zmora N, Levy M, Elinav E. The microbiome and innate immunity. Nature. (2016) 535:65–74. doi: 10.1038/nature18847
156. Zhao Q, Elson CO. Adaptive immune education by gut microbiome antigens. Immunology. (2018) 154:28–37. doi: 10.1111/imm.12896
157. Sethi V, Kurtom S, Tarique M, Lavania S, Malchiodi Z, Hellmund L, et al. Gut microbiome promotes tumor growth in mice by modulating immune response. Gastroenterology. (2018) 155:33–7.e6. doi: 10.1053/j.gastro.2018.04.001
158. Belkaid Y, Hand TW. Role of the microbiome in immunity and inflammation. Cell. (2014) 157:121–41. doi: 10.1016/j.cell.2014.03.011
159. Baker JM, Al-Nakkash L, Herbst-Kralovetz MM. Estrogen-gut microbiome axis: physiological and clinical implications. Maturitas. (2017) 103:45–53. doi: 10.1016/j.maturitas.2017.06.025
160. Ang Z, Xiong D, Wu M, Ding JL. FFAR2-FFAR3 receptor heteromerization modulates short-chain fatty acid sensing. FASEB J. (2018) 32:289–303. doi: 10.1096/fj.201700252RR
161. Alex S, Lange K, Amolo T, Grinstead JS, Haakonsson AK, et al. Short-chain fatty acids stimulate angiopoietin-like 4 synthesis in human colon adenocarcinoma cells by activating peroxisome proliferator-activated receptor. Mol Cell Biol. (2013) 33:1303–16. doi: 10.1128/MCB.00858-12
162. Kelly CJ, Zheng L, Campbell EL, Saeedi B, Scholz CC, Bayless AJ, et al. Crosstalk between microbiome-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host Microbe. (2015) 17:662–71. doi: 10.1016/j.chom.2015.03.005
163. Ridlon JM, Kang DJ, Hylemon PB, Bajaj JS. Bile acids and the gut microbiome. Curr Opin Gastroenterol. (2014) 30:332–8. doi: 10.1097/MOG.0000000000000057
164. Ma C, Han M, Heinrich B, Fu Q, Zhang Q, Sandhu M. Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells. Science. (2018) 360:eaan5931. doi: 10.1126/science.aan5931
165. Song X, Sun X, Oh SF, Wu M, Zhang Y, Zheng W, et al. Microbial bile acid metabolites modulate gut RORgamma(+) regulatory T cell homeostasis. Nature. (2020) 577:410–5. doi: 10.1038/s41586-019-1865-0
166. Liu T, Song X, Khan S, Li Y, Guo Z, Li C, et al. The gut microbiome at the intersection of bile acids and intestinal carcinogenesis: an old story, yet mesmerizing. Int J Cancer. (2020) 146:1780–90. doi: 10.1002/ijc.32563
167. Wang Z, Zhao Y. Gut microbiome derived metabolites in cardiovascular health and disease. Protein Cell. (2018) 9:416–31. doi: 10.1007/s13238-018-0549-0
168. Dao MC, Everard A, Aron-Wisnewsky J, Sokolovska N, Prifti E, Verger EO, et al. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut. (2016) 65:426–36. doi: 10.1136/gutjnl-2014-308778
169. So D, Whelan K, Rossi M, Morrison M, Holtmann G, Kelly JT, et al. Dietary fiber intervention on gut microbiome composition in healthy adults: a systematic review and meta-analysis. Am J Clin Nutr. (2018) 107:965–83. doi: 10.1093/ajcn/nqy041
170. Medina-Vera I, Sanchez-Tapia M, Noriega-López L, Granados-Portillo O, Guevara-Cruz M, Flores-López A, et al. A dietary intervention with functional foods reduces metabolic endotoxaemia and attenuates biochemical abnormalities by modifying faecal microbiome in people with type 2 diabetes. Diabetes Metab. (2019) 45:122–31. doi: 10.1016/j.diabet.2018.09.004
171. Houghton D, Hardy T, Stewart C, Errington L, Day CP, Trenell MI, et al. Systematic review assessing the effectiveness of dietary intervention on gut microbiome in adults with type 2 diabetes. Diabetologia. (2018) 61:1700–11. doi: 10.1007/s00125-018-4632-0
172. Matt SM, Allen JM, Lawson MA, Mailing LJ, Woods JA, Johnson RW. Butyrate and soluble fiber improve neuroinflammation associated with aging in mice. Front Immunol. (2018) 9:1832. doi: 10.3389/fimmu.2018.01832 Dietary
173. Thaiss CA, Itav S, Rothschild D, Meijer MT, Levy M, Moresi C, et al. Persistent microbiome alterations modulate the rate of post-dieting weight regain. Nature. (2016) 540:544–51. doi: 10.1038/nature20796
174. Gubert C, Kong G, Renoir T, Hannan AJ. Exercise, diet and stress as modulators of gut microbiota: implications for neurodegenerative diseases. Neurobiol Dis. (2020) 134:104621. doi: 10.1016/j.nbd.2019.104621
175. Vitale K, Getzin A. Nutrition and supplement update for the endurance athlete: review and recommendations. Nutrients. (2019) 11:1289. doi: 10.3390/nu11061289
176. Greene DA, Varley BJ, Hartwig TB, Chapman P, Rigney MJ. A low-carbohydrate ketogenic diet reduces body mass without compromising performance in powerlifting and olympic weightlifting athletes. Strength Cond Res. (2018) 32:3373–82. doi: 10.1519/JSC.0000000000002904
177. Royston KJ, Adedokun B, Olopade OI. Race, the microbiome and colorectal cancer. World J Gastrointest Oncol. (2019) 15:11:773–87. doi: 10.4251/wjgo.v11.i10.773
Keywords: additives, cooking, diet, food ingredients, gut microbiome, processing
Citation: Su Q and Liu Q (2021) Factors Affecting Gut Microbiome in Daily Diet. Front. Nutr. 8:644138. doi: 10.3389/fnut.2021.644138
Received: 20 December 2020; Accepted: 16 April 2021;
Published: 10 May 2021.
Edited by:
Xi Yu, Macau University of Science and Technology, MacauReviewed by:
Chiara Devirgiliis, Council for Agricultural Research and Economics, ItalyXinyi Pang, Nanjing University of Finance and Economics, China
Copyright © 2021 Su and Liu. 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) and the copyright owner(s) 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.
*Correspondence: Qin Liu, qinliu@cuhk.edu.hk