22 May The Human Gut Microbiome (and Beyond): Drivers of Health or Disease?
Gut Microbiome…From head to toe, inside and outside our body, we carry countless microorganisms that influence almost every aspect of our health.
Microbes are found everywhere on Earth, in every surface, crevice or hole, and our body is no exception. We are home to a vast microbial network, composed of trillions of microorganisms living in our skin, oral cavity, gastrointestinal tract, respiratory tract, and reproductive system. In the past decades the gut flora, for example, has been the focus of thousands of research studies, revealing amazing links between the composition of human microbiota and health1.
For example, reductions in the patterns of microbial diversity have been associated with conditions like eczema2, asthma and inflammatory diseases3, diabetes and obesity4, food intolerance or sensitivity, allergy to food or environmental biotoxins5, digestive tract disorders such as IBD (inflammatory bowel disease)6 and increased changes of acquiring infectious diseases1. Likewise, dysbiosis, when a microbial disbalances occurs that leads to the overgrowth of particular microbial groups, has been associated with conditions like chronic fatigue syndrome7, cancer8, colitis9 bacterial vaginosis10, anxiety and depression11 as well as other neurological conditions like Parkinson’s and Alzheimer’s disease12.
Hence, it is important to understand the basics of the human microbiota and how it can affect our health.
THE HUMAN GUT MICROBIOME: A BRIEF DEFINITION
Although originally intended to have different meanings, the terms “microbiota” (referring to the different microorganisms) and “microbiome” (referring to the genome content of the microbiota and their products) are currently used interchangeably to refer to the diversity of microbes living in our bodies. Herein, we employ both terms, microbiome and microbiota, to refer to the total composition of microbes in a given part of the body.
What are they?
The human microbiome is composed of vast communities of bacteria, archaea, fungi and viruses, found across the whole body, inside and out. This microbiome or microbiota is a weird ménage of commensal, symbiotic and pathogenic microorganisms, all living together in peaceful co-existence.
What do they do?
Their primary function, besides living in peace among themselves, is to maintain equilibrium or homeostasis between the local environment and the immune system of the host. These challenging tasks are amazingly executed in multiple sites of the body, including the oral cavity, gastrointestinal tract, vagina and skin1. These microbes have been found to influence multiple aspects of our body functions and health.
Below we give an overview of the human microbiome diversity, focusing on bacteria and the gut flora, describing the most important roles played by these microorganisms in different parts of our body, including our nose, lungs, gut, and skin.
The nasal cavity is a complex area of our body, composed of multiple sections, including crevices, holes, different textures, and some sections with significantly lower temperatures, compared to other parts of the body. Multiple factors have been shown to affect the composition of the nasal microbiota, including mode of birth, breastfeeding, environmental exposures, antibiotics, and smoking13.
The unique anatomical features of the nasal cavity influence the diversity and distribution of nasal microbes, known to harbour as many as 141 bacterial species14-15.
Anterior nares (the outside of the nose)
Studies have shown that this region is predominantly colonised by bacteria of the Actinobacteria, Firmicutes, and Proteobacteria families15.
A study that examined the middle meatus of healthy adults found a rich bacterial community, with Staphylococcus aureus, S. epidermidis, and Propionibacterium acnes standing as the most abundant bacterial species16.
Roles in disease
The diversity of nasal microbes has been associated with multiple diseases. Nasal dysbiosis, which is characterised by a reduction in the nasal microbiota diversity (number of species), has been associated with conditions like chronic rhinosinusitis, asthma, allergic rhinitis, bronchiolitis, the flu, and otitis media17-18.
- Bronchiolitis or pneumonia – In children, early colonization by the bacteria Haemophilus influenzae, Streptococcus pneumoniae and Moraxella catarrhalis, has been associated with increased chances of developing these conditions19.
- Viral infections – Reduced bacterial microbiome diversity in the respiratory tract has been shown to influence the development and severity of viral infections caused by respiratory syncytial virus, influenza and human rhinovirus20-21.
- Chronic rhinosinusitis (CR) – Multiple studies have shown that people suffering from CR often harbour certain bacteria in their nasal tract, including Staphylococcus, Pseudomonas aeruginosa, and S. aureus22- 23 as well as Streptococcus, Haemophilus, and Fusobacterium, and reduced overall diversity, according to another study24.
- Asthma – Recent studies have linked the nasal microbiota with the onset, development, and severity of asthma25-29. One study, for example, found that the nasal microbiota of asthma patients had an abundance of bacterial taxa Prevotella buccalis and Gardnerella, compared to healthy individuals. Another study found that the risk of developing asthma during the first year of life was strongly associated with early colonization by Streptococcus30.
LUNG AND PHARYNX MICROBIOME
The lungs and pharynx, despite their close proximity, are home to a distinct microbiota and are colonized by different pathogenic microorganisms. The pharynx, more commonly known as the throat, is divided into three sections: the nasopharynx (the upper region of the throat behind the nose), the oropharynx (located behind the mouth) and the laryngopharynx.
A study that employed a genomic approach to measuring the bacterial microbiota diversity of the oropharynx of seven individuals found that as many as 778 different species, mostly belonging to the Firmicutes, Proteobacteria, and Bacteroidetes group31. Studies have determined that the distribution of these three bacterial groups is more similar to that found in the saliva, compared to other body parts, including species like Staphylococcus aureus, Streptococcus mitis, Staphylococcus epidermidis, Enterobacter aerogenes and Aerococcus viridians. Another study reported that bacteria of the genus Prevotella, Capnocytophaga, Campylobacter, Veillonella, Streptococcus, Neisseria, where most commonly found throughout the human pharynx32.
Traditionally considered sterile, the lungs are now thought to serve as a host of a diverse microbiota, present during health or disease. Bacteria belonging to the Proteobacteria, Bacteroidetes, Firmicutes, Fusobacterium and Actinobacteria phylum have been identified in healthy lungs46, closely resembling the oral microbiome. This observation has led to the hypothesis that the oral microbiome may be the main source of bacteria colonizing the lungs47-48.
Role in disease
Different microbial compositions in the pharynx or lungs have been associated with a wide range of conditions, from cancer to microbial infections, bronchiectasis, and cystic fibrosis.
Various forms of cancer have been associated with an altered pharynx microbiome. For example:
One study, which analysed the pharyngeal microbiome of 68 individuals with laryngeal carcinoma, found a significant abundance of bacteria of the Firmicutes group of bacteria, representing more than half of the total bacterial diversity. Within this group, the genus Streptococcus was the most abundant43.
A study found that the bacteria Actinomyces oris and Veillonella denticariosi were associated with a reduced risk of developing pharynx cancer44.
Respiratory tract infections
Alterations to the optimal balance or homeostasis of bacterial species living the pharynx, including loss of diversity or loss of protective species, has been associated with disease45.
Microbes found in the lungs have been associated with conditions like bronchiectasis and cystic fibrosis, rheumatoid arthritis, autoimmunity and asthma26.
Bacterial taxa like Pseudomonas aeruginosa, Haemophilus influenzae, Prevotella, and Veillonella have been found at high abundance in the lungs of people suffering from bronchiectasis27.
Inflammatory airway diseases
Studies have linked lung microbiota composition with conditions like asthma or chronic obstructive pulmonary disease (COPD). Patients with COPD, for example, have been shown to harbour high levels of bacteria from the Proteobacteria and Firmicutes group, particularly species of Lactobacillus28.
People suffering from asthma have an overrepresentation of certain bacterial taxa in their airways, including pathogenic members of the Proteobacteria group, such as Haemophilus, Moraxella and Neisseria In contrast, there is an underrepresentation of other bacterial species, such as Prevotella spp, a member of the Bacteroidetes group29-30.
The lungs of adults and children with cystic fibrosis host a core microbiota characterised by bacterial species like Streptococcus, Prevotella, Rothia, Veillonella and Actinomyces, according to a study that used genomic tools to identify the microbes31. The study also found an inverse correlation between bacterial diversity and lung function, such that there was decreased lung function associated low bacterial community diversity and overgrowth of bacteria from the genus Pseudomonas31
The skin is our body’s largest and heaviest organ, responsible for protecting us from pathogens and other environmental threats. The skin also helps regulate temperature and allows us to feel the touch sensation.
But skin cells are not alone. In multiple sites across the body, the skin is covered with millions of microorganisms. The skin microbiome is composed of bacteria, fungi and viruses that help protect our body against invading pathogens, interact with our immune system and produce chemicals needed by our body. These roles influence our health in different ways, ultimately, affecting the development of skin and systemic diseases32.
The composition of the skin microbiome is mostly shaped by the type of skin where the microbes live and whether it is moist, dry or oily skin (Figure 2).
This includes the bits of skin in the middle of your forehead, called glabella, your cheeks, and several other regions. These regions of the skin are characterised by bacteria from the Propionibacterium (mostly) and Staphylococcus genera, but non-bacterial groups can also be present (Table 1).
The skin found in the middle of your arm, opposite to your elbow (called the antecubital fossa), is considered moist skin. Also, your nare and the bit of skin in between your fingers and the back of your knee are considered moist, as well as a few other places (Figure 2). In these bits of moist skin, you are also likely to find, mostly, species of Propionibacterium, but also species of Corynebacterium and Staphylococcus and a few other bacterial groups (Table 1).
Skin regions like your palms and the underside of the forearms are dominated by species of Corynebacterium, followed by members of Staphylococcus, and several other bacterial genera (Table 1)
Role in disease
Like with other microbiomes of the human body, the skin microbiome thrives in balance, and in keeping a careful composition of different species. Alterations to this balance can result in dysbiosis, where specific species overgrow, altering microbial dynamics and affecting the skin’s protective function, potentially allowing the entrance of pathogens.
In general, dysbiosis of microbial communities can be defined as a state of altered or impaired composition of a microbial community, compared to a normal/healthy state. Skin conditions like dandruff, acne, eczema and poor wound healing have been associated with dysbiosis33.
One study found that healthy scalps are characterised by a microbiome dominated by the bacteria Propionibacterium acnes, whereas a scalp affected by dandruff is mostly dominated by Staphylococcus epidermidis33.
This well-known condition affecting teenager (and some adults) is primarily driven by the bacterium Propionibacterium acnes, a normal inhabitant of healthy skin. In people with acne, research suggest that certain strains of this bacterium are associated with the development of this condition34.
Table 1. Diversity of bacteria, fungi and viruses present in the human skin.
Better known as eczema, this chronic condition is a type of inflammatory disease characterised by red, scaly and itchy skin. Skin barrier dysfunction, altered immune function and skin microbial dysbiosis are among the contributing factors driving this condition. Different bacterial species have been associated with dermatitis, including species within the genus Staphylococcus, like S. aureus and S. epidermidis, which are more commonly found in severe stages of this disease35. Another study identified an overrepresentation of Streptococcus and Gemella bacterial species, and a depletion of species from the genus Dermacoccus in people suffering from atopic dermatitis36.
Multiple species of bacteria and fungi inhabit the male and female urogenital systems. These organs are home to important communities of microorganism that help fight off infections and influence the development of local as well as systemic disease.
Bacterial diversity in the urogenital tract is distinct for males and females, characterised by specific bacterial and fungal species.
- In women, a healthy vaginal microbiome may be dominated by species of the bacterial genus Lactobacillus37. However, other bacterial species have also been identified in healthy individuals, including species of the bacterial genera Prevotella, Sneathia, Megasphaera, or Streptococcus. This suggests that there is significant diversity in terms of a healthy vaginal microbiota. Studies have also shown that the composition of the vaginal microbiota drastically changes over a woman’s life cycle38.
- During childhood, the vaginal microbiota is primarily composed of y Gram-negative anaerobe bacteria, like Bacteroides, Fusobacterium, Veillonella, Gram-positive anaerobic bacteria, including Actinomyces, Bifidobacterium, Peptococcus, Peptostreptococcus, and Propionibacterium, as well as some aerobic bacteria such as Staphylococcus aureus, Staphylococccus epidermidis, Streptococcus viridans, and Enterococcus faecalis.
- During pre-puberty, the vaginal microbiota changes to an environment characterised by reduced numbers of lactobacilli, Gardnerella vaginalis, and Prevotella Bivia.
- During puberty, influenced by the presence of estrogen, the vaginal microbiome becomes dominated by Lactobacillus crispatus, Lactobacillus gasseri, Lactobacillus iners, and Lactobacillus jensenii, similar to the microbiome of adult women.
- During menopause, when estrogen levels decrease, the vaginal microbiome is characterised by an abundance of Lactobacillus crispatus, L. iners, Gardnerella vaginalis, and Prevotella. There is also a reduction in the levels of certain groups, like Candida, Mobiluncus, Staphylococcus, Bifidobacterium, and Gemella.
Another important aspect of a woman’s vaginal microbiome concerns how it influences the makeup of newborns. Multiple factors influence the makeup of a baby’s microbiota, but the role of the mother is, by far, the most important (Figure 2). For an in-depth review of how the microbiome influence’s women’s health and the health of newborns, please see this recent review.
Figure 2. Different factors affecting the process of birth, from conception to childbirth and beyond.
- In men, microorganisms can be found inside and outside their genitals.
- For example, species belonging to as many as 42 bacterial families have been identified in the base of the penis alone, with members of the Pseudomonadaceae and Oxalobacteraceae families being the most common39.
- Whether or not you are circumcised also affects the diversity of bacteria. A circumcised penis has been shown to host significant lower diversity of anaerobic bacteria (bacteria that don’t need oxygen), and a higher diversity of bacteria capable of alternating between using oxygen or not, known as facultative bacteria, which may influence the function of the immune system40.
- Semen – One recent study identified three different microbiome profiles in semen: Prevotella-enriched, Lactobacillus-enriched, and polymicrobial, meaning they hosted a wide range of microbes41. Another study identified Lactobacillus, Pseudomonas, Prevotella and Gardnerella as the most abundant bacterial groups. This study, also established links between semen microbiome and quality, showing that low-quality semen had a higher level of Prevotella, compared to normal samples42. In recent years, research studies have established links between the seminal microbiome and men’s reproductive health, the health of their partners and even the health of their offspring.
- Seminal microbiome dysbiosis has been linked to disorders like infertility and poor semen quality, prostatitis and HIV infection
- Sexual intercourse can lead to the exchange of microbes between partners, and part of this exchange involves the seminal microbiome.
- The transfer of microbes to the female partners may involve commensal and potentially pathogenic species, which might influence the development of bacterial vaginosis.
- Likewise, female to male transfer of microbes has been observed, with studies showing that semen can harbour vaginal bacterial taxa and that sexually active men can host unique bacterial species in their semen43.
For a good and recent review on the seminal microbiome and its role in health, check this Nature research review43.
Role in disease
In females, the vaginal microbiota is associated with the development of conditions like vaginosis, yeast infections, sexually transmitted infections (STI) (including HIV), cancer and urinary tract infections44-45. In males, similar associations have been made for conditions like STIs, cancer and infections.
This is a complex condition most commonly affecting fertile, pre-menopausal and pregnant women. It is characterised by a disruption of the vaginal microbiome, resulting in a reduction of Lactobacillus, which is the dominant group in health, and an overgrowth of other bacterial groups. So far studies have identified bacterial genera like Gardnerella, Atopobium, Prevotella, Peptostreptococcus, Mobiluncus, Sneathia, Leptotrichia, Mycoplasma, as being associated with the development of the disease. Furthermore, studies suggest that the response of the immune system to these bacteria is also an important factor to consider46. A significant finding regarding vaginosis and microbes is that sexual intercourse has been identified as an important factor affecting the vaginal microbiota and disease. For example, regular sexual activity between a couple can lead to similar penile and vaginal microbiomes, which has been linked to increased chances of developing vaginosis in the female partner47.
The microbes inhabiting the male and female genital tracts have an important role in protecting our body from infections and this includes sexually transmitted infections. For example:
- In females, multiple studies have linked bacterial vaginosis to herpes simplex virus (HSV). For example, one study found that HSV-positive women had an increased risk of developing bacterial vaginosis48-49.
- Human Papillomavirus (HPV)
This is the most common sexually transmitted viral infection affecting both men and women. While it can be asymptomatic in a lot of cases, some HPV types are associated with cancer. Cancers of the anus, vulva, vagina, penis, cervix and oropharynx have been linked to different types of HPV. Among these, cervical cancer is one of the most clinically important, affecting half a million people worldwide. Multiple studies have linked HPV infection with bacterial vaginosis, with some studies showing that women who are HPV positive have a lower proportion of Lactobacillus, the dominant bacterial taxa in healthy vaginal microbiomes50-51.
- Human Papillomavirus (HPV)
Urinary incontinence (UI)
Studies report that women with UI show reduced levels of Lactobacillus and elevated levels of the bacterial genus Gardnerella52-53. Likewise, other studies have identified differences in the composition of the urinary tract microbiome of patients suffering from urgency urinary incontinence (UUI). One study found differences in abundance in as many as 14 bacterial taxa between UUI patients and healthy controls54.
Multiple lines of evidence support a link between the human microbiome and certain urogenital cancers in both males and females. For example, microbes have been associated with colorectal adenoma, adenocarcinoma, as well as in gastric, colorectal, and hepatobiliary cancer55. In these cancers, bacteria have been shown to affect a biochemical pathway involving a protein called beta-catenin, involved in cell development56. Bacteria have also been shown to influence cancer risk through their role in the metabolism and production of certain carcinogenic chemicals, like nitrosamines and acetaldehyde57.
The gastrointestinal Tract (GIT), commonly known as the gut, is a large organ system that includes your mouth and tongue, pharynx, oesophagus, stomach, duodenum, plus the small and large intestines. Two of the most studied microbiomes of the gut are those of the mouth and the small intestine.
The mouth is home to 700-1000 different bacterial species, amounting to up to 10 billion microorganisms58-59. In any one individual, a healthy mouth may contain as many as 50 species in each of different locations, like your tongue, teeth, saliva and the inner linings of the mouth60-61 (Figure 1).
Figure 1. Oral microbiome: diversity of genera identified in the mouth.
The diversity (how many species) of these microorganisms varies from person to person, from site to site within your mouth and according to your health status.
The mouth is colonised by a diverse flora of microorganisms, most prominently by bacteria, but also by viruses and fungi. Among these, bacteria represent the most common and best-studied group. The bacterium Streptococcus mutans, for example, is found in the saliva, teeth and tongue. Other bacterial species are restricted to specific regions.
- For example, a study analysing the tongue bacterial microbiota in healthy individuals identified members of the bacterial families Proteobacteria, Bacteroidetes, Firmicutes, Fusobacteria, Actinobacteria, as is common among all participants58.
- Other studies have identified distinct bacterial composition in the teeth, localised in three key regions: the keratinized gingiva, the subgingival plaque and the supragingival plaque59-61 (Figure 1). Bacterial groups from the genus Streptococcus are found in all three sites of the teeth.
Role in disease
Multiple oral conditions have been associated with the composition of the oral bacterial microbiota, including caries, gingivitis, stomatitis, and periodontitis. Beyond the mouth, the oral microbiota has also been linked to conditions like cancer, diabetes, cardiovascular diseases, bacteraemia, and pre-term birth61-63.
The bacterial species Streptococcus mutans is a common inhabitant of the teeth and other parts of the mouth (Figure 1), found in healthy mouths. But, under certain circumstances, overgrowth of this and other species can influence the development of caries64.
Multiple studies have linked changes in the composition of the oral microbiota with different forms of cancer. For example, bacterial taxa of the Fusobacterium, Dialister, Peptostreptococcus, Filifactor, Peptococcus, Catonella and Parvimonas groups are more abundant in people suffering from oral squamous cell carcinoma, compared to healthy controls65. Similar findings with other forms of oral cancer have been reviewed elsewhere66-68.
Studies have linked a role for oral pathogenic bacteria like Fusobacterium nucleatum, Porphyromonas gingivalis, Filifactor alocis, Campylobacter rectus, among others, in pregnancy outcomes. Possible mechanisms involved in this link include bacteremia, originated from periodontal pathogens, host or fetal immune responses, or oral to vaginal transmission of pathogens due to some sexual practices69-70.
INTESTINAL GUT MICROBIOME
The small intestine is home to the vast majority of microorganisms that make up the gut microbiome. Most of these microorganisms are found in the large intestine, where they are responsible for the digestion of certain fibres that are not digestible elsewhere in the body.
Estimates suggest that billions of microorganisms make up the intestinal gut microbiome. Taking together the diversity found across different people, thousands of gut microbial species have been identified. Studies suggest that a single person can harbour over 160 different bacterial species in their guts71.
In the past decades, studies have identified intriguing links between the composition of the gut microbiome and an amazing range of diseases, from IBD, IBS and other gut dysfunctions, to Alzheimer’s and Parkinson’s disease, obesity, heart disease, diabetes and cancer72.
FOCUS ON THE INTESTINAL GUT MICROBIOME
Where did it all begin?
From Primate to Humans
The origins of the gut microbiome go back before our own species evolved into human beings. Chimpanzees, humans’ closest evolutionary relatives, also host a gut microbiome. One study found that compared to chimpanzees, human host a gut microbiome with reduced ancestral diversity. That is, our gut microbiome has reduced microbial groups similar to those found in chimps. The study also found differences in the microbial composition: humans had an increase in the number of gut bacteria involved with animal-based diets73.
From Mother to Child
The composition of the intestinal gut microbiome, as well as the rest of the baby’s microbiome, is shaped during the first months of life, starting from the day we are born74 and, likely, even before75-77. Babies who are born through vaginal delivery, are exposed to the maternal microbiome when they pass through the birth canal and into the world. This first exposure to bacteria and other microbes from the mother serves as an inoculum that will grow and develop into a mature microbiome across multiple sites of the baby’s body78.
In contrast, babies born from Caesarean Section (C-section) are not exposed to the same set of maternal microbes. Rather than their mother’s gut microbiota, they are exposed to skin microbes as well as environmental microbes found in their surroundings. Studies have shown that these two different modes of delivery have significant effects on the composition of the baby’s microbiota, as well as with their health in the short and long term. Babies delivered through C-section have been associated with an increased risk of developing chronic immune disorders such as asthma, systemic connective tissue disorders, juvenile arthritis, inflammatory bowel disease, and obesity79.
After birth, the composition of a baby’s microbiome is influenced by multiple factors. Some of these factors are intrinsic, like genetics or immune and gut function, but others, the vast majority, are external and include our mother’s diet, diet during our early and adult years, presence of environmental toxins, sleeping patterns, exercise levels, antibiotic use and use of prescription and over the counter drugs, stress levels, among others80-82.
How do we define an optimal gut microbiome?
A difficult question to address concerns what actually makes a healthy gut flora. So far, studies conclude that there is no ideal combination of gut microbes that would benefit everyone. When the Human Microbiome Project sequenced the gut microbiome of multiple healthy individuals, they found that everyone had different microbes in their guts83. These findings suggest that there is no ideal gut flora or microbiome that is common to everyone. Just like our genomic signature is unique, the composition of our gut microbiome seems to be a unique feature of each person84.
Despite the marked differences between healthy individuals in terms of microbial species, it has been possible to identify certain groups of bacteria that seem to dominate the gut microbiome of healthy individuals. For example, studies have shown that two phyla of bacteria, Firmicutes and Bacteroidetes, represent about 90% of all the gut microbiome85.
Furthermore, researchers have identified specific bacterial taxa that consistently seem associated with beneficial outcomes. For example,
The primary function of this species is process mucus into sugars and other chemicals that are used by others but microbes. Influence on Health: promotes mucosal health. Low levels of this species have been associated with obesity, regulation of blood sugar levels, and metabolic problems, whereas overgrowth is linked to multiple sclerosis.
Involved with multiple functions in the gut, including regulation of immune function, gut barrier integrity and microbial balance. Influence on Health: Low levels of this bacteria have been associated with reduced anti-inflammatory function in the gut.
Species of this bacterial genus are commonly found in breast milk and in probiotic supplements. It is a common gut inhabitant of the gut, vagina and mouth microbiome. Influence on Health: Studies have suggested that Bifidobacterium bifidum may help reduce the symptoms of IBS and might improve immune function.
This is a broad group of bacteria that include multiple species of bacteria known to produce short-chain fatty acids, like butyrate. Influence on Health: Through the production of SCFAs, these bacteria have been linked to multiple functions, including the maintenance of a healthy intestinal mucosal barrier, immune function and protection against pathogens.
This is a common member of the Firmicutes phylum of gut bacteria. There are more than 16 known species of this genus. Influence on Health: Alterations to the optimal levels of this bacteria have been associated with conditions like altered digestive capacity, constipation or bacterial overgrowth.
A common gut inhabitant, member of the Proteobacteria phylum. The species E. coli is the most common species in this genus, commonly found in healthy guts. However, there are many pathogenic strains of this species that can affect our health. Influence on Health: High levels of coli can be indicative of inflammation-related disorders in the gut, whereas low levels of E. coli have been associated with decreased gut mucosal function and reduced protection against pathogenic strains of E. coli.
While there is no ideal gut microbiome composition that fits everyone, there are key signatures that are present in a healthy gut, and this key is balance. Every person may have a distinct gut microbiome, made of different combinations of species. But the signature of a healthy gut is a balanced gut microbiome86 and one with optimal intestinal permeability.
In simple terms, gut dysbiosis is defined as an imbalance in the composition of the gut microbiome, in relation to a healthy/normal state. Gut dysbiosis can lead to an overgrowth of potentially pathogenic species, can reduce our capacity to fight off infections from invading pathogens, like Blastocystis hominis or Dientamoeba fragilis, can alter the function of some immune cells or cause excessive intestinal permeability. Dysbiosis has been associated with multiple ailments and symptoms87-92 (Table 2).
Table 2. Example of conditions associated with gut dysbiosis, and typical symptoms
Drivers of gut dysbiosis
Alterations to the composition of the gut microbiome can be due to multiple factors, such as genetics, diet, exercise and sleeping patterns, infections, environmental factors, among others. Understanding the cause and consequences of these factors can help you understand how to best improve your health. Some key factors associated with gut dysbiosis include:
- Environmental toxins
- Chronic Stress
- Refined carbohydrates
- Industrial seed oils
- Parasite infections
- Bacterial infections
- Fungal and yeast infections
Among these, diet is one of the most important factors affecting our gut microbiome.
This is one of the most important factors affecting the composition of the gut microbiome, and one you can control. The type and quantity of food you eat have a direct impact on what microbes thrive in your gut, through the complex interaction that occurs between nutrients and microorganisms. One of the most important examples of dietary components that affect the gut microbiome is fibre.
There are various types of fibre, but one that interacts with the gut microbiome is called fermentable fibre. This type of fibre includes pectins, beta-glucans, guar gum, inulin and oligofructose and is found in beans and legumes. Another important type of fibre that also feeds your gut microbiome is resistant starch. Sources of resistant starch include green bananas, cooked and cooled rice and pasta, cashews, raw oats, and many others.
How much is enough?
The most likely answer is as much as you can handle, granted you have consulted with a health professional first. It is quite likely that you are not eating enough fibre. Even if you follow the recommended amounts of 30 grams per day, you are not eating enough. According to different studies, the amount of fibre we consume today is significantly low, compared to what our ancestors ate before the dawn of the agricultural revolution. The recommended fibre intake (30g / day) is about a third of the 100g our ancestors consumed every day93. Modern rural communities that consume high levels of fibre (about 50g / day) have been shown to be free of chronic inflammatory diseases94-96, hinting at the health benefit of a fibre-rich diet.
Role of Fibre
Fermentation of dietary fibre is a key mechanism that affects our health through the formation of special chemicals called Short Chain Fatty Acids, or SCFAs. SCFAs, like butyrate, are an important source of energy for colonic cells, influencing their growth and function. SCFAs have also been involved with some types of cancers, obesity and insulin sensitivity, among other conditions.
Other factors, like stress, exposure to environmental biotoxins, lack of exercise, and many others have been linked to gut dysbiosis. Classic experiments, for example, have shown that separating rat pups from their mum (a source of stress) leads to changes in the pups’ microbiota, their stress system and their behaviour97. Other studies have shown comparable effects of stress on the human microbiome98.
Figure 3. Main factors driving gut dysbiosis
FUNGI AND VIRUSES: THE OTHER MICROBIOME
While the bacterial gut microbiome has received most of the attention of researchers, there are other microbes that also live in our body. Studies have identified fungal and viral species inhabiting the mouth, lungs, gut, skin and urogenital tracts. These microorganisms are diverse and have been associated with multiple diseases.
Fungal species are the next most studied microbiome in the human body. Studies have shown that fungal species live alongside bacteria on the same body sites, like your skin (Table 1), gut, mouth (Figure 4). To learn more about the human mycobiome you can jump to our article on this topic.
Compared to other microbial groups, the viral microbiome has not been so extensively studied, partly due to the difficulty cultivating viruses or in gathering the required data to identify them. In the oral cavity, for example, the viral microbiota is characterised by a group of viruses that target bacteria, called bacteriophages. Little is known, so far, about the function of these viruses, but researchers think they might influence the diversity and function of some oral bacteria21-22. The skin has also been found to host a large number of different viruses (see Table 1). However, further research is needed to gain a better understanding of the diversity of function of viruses in the oral cavity and beyond.
Figure 4. Diversity and distribution of the human mycobiota and associations with disease.
The gut microbiome and the microbiome living in the rest of your body can influence your health in many ways, influencing a wide range of conditions, from obesity and diabetes to digestive disorders, skin disorders, fungal infections, parasite infections, autoimmune disorders and neurological disorders. The role of external factors like diet or stress on the composition of the gut microbiome is well supported by research and should be considered on any treatment plan.
At the Australian Centre for Functional Medicine, we are up to date on the scientific literature of the gut microbiome and its link to health. We employ advanced diagnostic testing technology, including blood, breath, stools, urine, and skin swabs tests, to uncover information about your body’s health and about the health of your microbiome. With this information at hand, we can get a better understanding of the underlying problems causing your symptoms and design a personalised and effective treatment plan.
Register to become a patient today and you will be one step closer in your pathway to optimal health.
- Malla MA, Dubey A, Kumar A, Yadav S, Hashem A, Abd_Allah EF. Exploring the human microbiome: The potential future role of next-generation sequencing in disease diagnosis and treatment. Frontiers in immunology. 2019 Jan 7;9:2868. Read it!
- Wang M, Karlsson C, Olsson C, Adlerberth I, Wold AE, Strachan DP, Martricardi PM, Åberg N, Perkin MR, Tripodi S, Coates AR. Reduced diversity in the early fecal microbiota of infants with atopic eczema. Journal of Allergy and Clinical Immunology. 2008 Jan 1;121(1):129-34. Read it!
- Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC. Low gut microbiota diversity in early infancy precedes asthma at school age. Clinical & Experimental Allergy. 2014 Jun;44(6):842-50. Read it!
- Karlsson F, Tremaroli V, Nielsen J, Bäckhed F. Assessing the human gut microbiota in metabolic diseases. Diabetes. 2013 Oct 1;62(10):3341-9. Read it!
- Bisgaard H, Li N, Bonnelykke K, Chawes BL, Skov T, Paludan-Müller G, Stokholm J, Smith B, Krogfelt KA. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. Journal of Allergy and Clinical Immunology. 2011 Sep 1;128(3):646-52. Read it!
- Ferreira CM, Vieira AT, Vinolo MA, Oliveira FA, Curi R, Martins FD. The central role of the gut microbiota in chronic inflammatory diseases. Journal of immunology research. 2014;2014. Read it!
- Lakhan SE, Kirchgessner A. Gut inflammation in chronic fatigue syndrome. Nutrition & metabolism. 2010 Dec 1;7(1):79. Read it!
- Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, Barnes R, Watson P, Allen-Vercoe E, Moore RA, Holt RA. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome research. 2012 Feb 1;22(2):299-306. Read it!
- Duranti S, Gaiani F, Mancabelli L, Milani C, Grandi A, Bolchi A, Santoni A, Lugli GA, Ferrario C, Mangifesta M, Viappiani A. Elucidating the gut microbiome of ulcerative colitis: bifidobacteria as novel microbial biomarkers. FEMS microbiology ecology. 2016 Dec 1;92(12):fiw191. Read it!
- Africa CW, Nel J, Stemmet M. Anaerobes and bacterial vaginosis in pregnancy: virulence factors contributing to vaginal colonisation. International journal of environmental research and public health. 2014 Jul;11(7):6979-7000. Read it!
- Lach G, Schellekens H, Dinan TG, Cryan JF. Anxiety, depression, and the microbiome: a role for gut peptides. Neurotherapeutics. 2018 Jan 1;15(1):36-59. Read it!
- Tremlett H, Bauer KC, Appel‐Cresswell S, Finlay BB, Waubant E. The gut microbiome in human neurological disease: a review. Annals of neurology. 2017 Mar;81(3):369-82. Read it!
- Kaspar U, Kriegeskorte A, Schubert T, Peters G, Rudack C, Pieper DH, Wos‐Oxley M, Becker K. The culturome of the human nose habitats reveals individual bacterial fingerprint patterns. Environmental microbiology. 2016 Jul;18(7):2130-42. Read it!
- Proctor DM, Relman DA. The landscape ecology and microbiota of the human nose, mouth, and throat. Cell host & microbe. 2017 Apr 12;21(4):421-32. Read it!
- Bassis CM, Tang AL, Young VB, Pynnonen MA. The nasal cavity microbiota of healthy adults. Microbiome. 2014 Dec;2(1):1-5. Read it!
- Ramakrishnan VR, Feazel LM, Gitomer SA, Ir D, Robertson CE, Frank DN. The microbiome of the middle meatus in healthy adults. PloS one. 2013;8(12). Read it!
- Esposito S, Principi N. Impact of nasopharyngeal microbiota on the development of respiratory tract diseases. European Journal of Clinical Microbiology & Infectious Diseases. 2018 Jan 1;37(1):1-7. Read it!
- Huang YJ. Nasopharyngeal microbiota: gatekeepers or fortune tellers of susceptibility to respiratory tract infections? Read it!
- Vissing NH, Chawes BL, Bisgaard H. Increased risk of pneumonia and bronchiolitis after bacterial colonization of the airways as neonates. American journal of respiratory and critical care medicine. 2013 Nov 15;188(10):1246-52. Read it!
- Ederveen TH, Ferwerda G, Ahout IM, Vissers M, de Groot R, Boekhorst J, Timmerman HM, Huynen MA, van Hijum SA, de Jonge MI. Haemophilus is overrepresented in the nasopharynx of infants hospitalized with RSV infection and associated with increased viral load and enhanced mucosal CXCL8 responses. Microbiome. 2018 Dec;6(1):10. Read it!
- Lee KH, Gordon A, Shedden K, Kuan G, Ng S, Balmaseda A, Foxman B. The respiratory microbiome and susceptibility to influenza virus infection. PloS one. 2019 Jan 9;14(1):e0207898. Read it!
- Allen EK, Koeppel AF, Hendley JO, Turner SD, Winther B, Sale MM. Characterization of the nasopharyngeal microbiota in health and during rhinovirus challenge. Microbiome. 2014 Dec;2(1):22. Read it!
- Lemon KP, Klepac-Ceraj V, Schiffer HK, Brodie EL, Lynch SV, Kolter R. Comparative analyses of the bacterial microbiota of the human nostril and oropharynx. MBio. 2010 Aug 31;1(3):e00129-10. Read it!
- Gong H, Wang B, Shi Y, Shi Y, Xiao X, Cao P, Tao L, Wang Y, Zhou L. Composition and abundance of microbiota in the pharynx in patients with laryngeal carcinoma and vocal cord polyps. Journal of Microbiology. 2017 Aug 1;55(8):648-54. Read it!
- Hayes RB, Ahn J, Fan X, Peters BA, Ma Y, Yang L, Agalliu I, Burk RD, Ganly I, Purdue MP, Freedman ND. Association of oral microbiome with risk for incident head and neck squamous cell cancer. JAMA oncology. 2018 Mar 1;4(3):358-65. Read it!
- Gao Z, Kang Y, Yu J, Ren L. Human pharyngeal microbiome may play a protective role in respiratory tract infections. Genomics, proteomics & bioinformatics. 2014 Jun 1;12(3):144-50. Read it!
- Lanaspa M, Bassat Q, Medeiros MM, Muñoz-Almagro C. Respiratory microbiota and lower respiratory tract disease. Expert review of anti-infective therapy. 2017 Jul 3;15(7):703-11. Read it!
- Tunney MM, Einarsson GG, Wei L, Drain M, Klem ER, Cardwell C, Ennis M, Boucher RC, Wolfgang MC, Elborn JS. Lung microbiota and bacterial abundance in patients with bronchiectasis when clinically stable and during exacerbation. American journal of respiratory and critical care medicine. 2013 May 15;187(10):1118-26. Read it!
- Gollwitzer ES, Marsland BJ. Microbiota abnormalities in inflammatory airway diseases—Potential for therapy. Pharmacology & therapeutics. 2014 Jan 1;141(1):32-9. Read it!
- Hilty M, Burke C, Pedro H, Cardenas P, Bush A, Bossley C, Davies J, Ervine A, Poulter L, Pachter L, Moffatt MF. Disordered microbial communities in asthmatic airways. PloS one. 2010 Jan 5;5(1):e8578. Read it!
- Coburn B, Wang PW, Caballero JD, Clark ST, Brahma V, Donaldson S, Zhang Y, Surendra A, Gong Y, Tullis DE, Yau YC. Lung microbiota across age and disease stage in cystic fibrosis. Scientific reports. 2015 May 14;5:10241. Read it!
- Byrd AL, Belkaid Y, Segre JA. The human skin microbiome. Nature Reviews Microbiology. 2018 Mar;16(3):143. Read it!
- Saxena R, Mittal P, Clavaud C, Dhakan DB, Hegde P, Veeranagaiah MM, Saha S, Souverain L, Roy N, Breton L, Misra N. Comparison of healthy and dandruff scalp microbiome reveals the role of commensals in scalp health. Frontiers in cellular and infection microbiology. 2018 Oct 4;8:346. Read it!
- Fitz-Gibbon S, Tomida S, Chiu BH, Nguyen L, Du C, Liu M, Elashoff D, Erfe MC, Loncaric A, Kim J, Modlin RL. Propionibacterium acnes strain populations in the human skin microbiome associated with acne. Journal of investigative dermatology. 2013 Sep 1;133(9):2152-60. Read it!
- Byrd AL, Deming C, Cassidy SK, Harrison OJ, Ng WI, Conlan S, Belkaid Y, Segre JA, Kong HH, NISC Comparative Sequencing Program. Staphylococcus aureus and Staphylococcus epidermidis strain diversity underlying pediatric atopic dermatitis. Science translational medicine. 2017 Jul 5;9(397):eaal4651. Read it!
- Chng KR, Tay AS, Li C, Ng AH, Wang J, Suri BK, Matta SA, McGovern N, Janela B, Wong XF, Sio YY. Whole metagenome profiling reveals skin microbiome-dependent susceptibility to atopic dermatitis flare. Nature microbiology. 2016 Sep;1(9):16106. Read it!
- Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM. Vaginal microbiome of reproductive-age women. Proceedings of the National Academy of Sciences. 2011 Mar 15;108(Supplement 1):4680-7.Read it!
- Younes JA, Lievens E, Hummelen R, van der Westen R, Reid G, Petrova MI. Women and their microbes: the unexpected friendship. Trends in microbiology. 2018 Jan 1;26(1):16-32. Read it!
- Mändar R. Microbiota of male genital tract: impact on the health of man and his partner. Pharmacological research. 2013 Mar 1;69(1):32-41.Read it!
- Price LB, Liu CM, Johnson KE, Aziz M, Lau MK, Bowers J, Ravel J, Keim PS, Serwadda D, Wawer MJ, Gray RH. The effects of circumcision on the penis microbiome. PloS one. 2010 Jan 6;5(1):e8422. Read it!
- Baud D, Pattaroni C, Vulliemoz N, Castella V, Marsland B, Stojanov M. Sperm microbiota and its impact on semen parameters. Frontiers in microbiology. 2019;10:234. Read it!
- Weng SL, Chiu CM, Lin FM, Huang WC, Liang C, Yang T, Yang TL, Liu CY, Wu WY, Chang YA, Chang TH. Bacterial communities in semen from men of infertile couples: metagenomic sequencing reveals relationships of seminal microbiota to semen quality. PloS one. 2014;9(10). Read it!
- Altmäe S, Franasiak JM, Mändar R. The seminal microbiome in health and disease. Nature Reviews Urology. 2019 Nov 15:1-9. Read it!
- Bing M, Forney LJ, Ravel J. The vaginal microbiome: rethinking health and diseases. Annu Rev Microbiol. 2012;66:371-89. Read it!
- Petrova MI, van den Broek M, Balzarini J, Vanderleyden J, Lebeer S. Vaginal microbiota and its role in HIV transmission and infection. FEMS microbiology reviews. 2013 Sep 1;37(5):762-92. Read it!
- Onderdonk AB, Delaney ML, Fichorova RN. The human microbiome during bacterial vaginosis. Clinical microbiology reviews. 2016 Apr 1;29(2):223-38. Read it!
- Zozaya M, Ferris MJ, Siren JD, Lillis R, Myers L, Nsuami MJ, Eren AM, Brown J, Taylor CM, Martin DH. Bacterial communities in penile skin, male urethra, and vaginas of heterosexual couples with and without bacterial vaginosis. Microbiome. 2016 Dec;4(1):16. Read it!
- Nagot N, Ouedraogo A, Defer MC, Vallo R, Mayaud P, Van de Perre P. Association between bacterial vaginosis and Herpes simplex virus type-2 infection: implications for HIV acquisition studies. Sexually transmitted infections. 2007 Aug 1;83(5):365-8. Read it!
- Lewis FM, Bernstein KT, Aral SO. Vaginal microbiome and its relationship to behavior, sexual health, and sexually transmitted diseases. Obstetrics and gynecology. 2017 Apr;129(4):643. Read it!
- Brotman RM, Shardell MD, Gajer P, Tracy JK, Zenilman JM, Ravel J, Gravitt PE. Interplay between the temporal dynamics of the vaginal microbiota and human papillomavirus detection. The Journal of infectious diseases. 2014 Dec 1;210(11):1723-33. Read it!
- King CC, Jamieson DJ, Wiener J, Cu-Uvin S, Klein RS, Rompalo AM, Shah KV, Sobel JD. Bacterial vaginosis and the natural history of human papillomavirus. Infectious diseases in obstetrics and gynecology. 2011;2011. Read it!
- Karstens L, Asquith M, Davin S, Stauffer P, Fair D, Gregory WT, Rosenbaum JT, McWeeney SK, Nardos R. Does the urinary microbiome play a role in urgency urinary incontinence and its severity?. Frontiers in cellular and infection microbiology. 2016 Jul 27;6:78. Read it!
- Pearce MM, Hilt EE, Rosenfeld AB, Zilliox MJ, Thomas-White K, Fok C, Kliethermes S, Schreckenberger PC, Brubaker L, Gai X, Wolfe AJ. The female urinary microbiome: a comparison of women with and without urgency urinary incontinence. MBio. 2014 Aug 29;5(4):e01283-14. Read it!
- Karstens L, Asquith M, Davin S, Stauffer P, Fair D, Gregory WT, Rosenbaum JT, McWeeney SK, Nardos R. Does the urinary microbiome play a role in urgency urinary incontinence and its severity?. Frontiers in cellular and infection microbiology. 2016 Jul 27;6:78. Read it!
- Neto AG, Bradshaw AD, Pei Z. Microbiome, a new dimension in cancer research. Annals of translational medicine. 2015 Sep;3(16). Read it!
- Clevers H, Nusse R. Wnt/β-catenin signaling and disease. Cell. 2012 Jun 8;149(6):1192-205. Read it!
- Xu W, Yang L, Lee P, Huang WC, Nossa C, Ma Y, Deng FM, Zhou M, Melamed J, Pei Z. Mini-review: perspective of the microbiome in the pathogenesis of urothelial carcinoma. American journal of clinical and experimental urology. 2014;2(1):57. Read it!
- Tribble GD, Angelov N, Weltman R, Wang BY, Eswaran SV, Gay IC, Parthasarathy K, Dao DH, Richardson KN, Ismail NM, Sharina IG. Frequency of tongue cleaning impacts the human tongue microbiome composition and enterosalivary circulation of nitrate. Frontiers in cellular and infection microbiology. 2019;9:39. Read it!
- Wade, W.G., 2013. The oral microbiome in health and disease. Pharmacological research, 69(1), pp.137-143. Read it!
- Wade WG. Detection and culture of novel oral bacteria. Oral Microbial Ecology: Current Research and New Perspectives. 2013 Feb 15:27. Read it!
- Aas, J.A., Paster, B.J., Stokes, L.N., Olsen, I. and Dewhirst, F.E., 2005. Defining the normal bacterial flora of the oral cavity. Journal of clinical microbiology, 43(11), pp.5721-5732. Read it!
- Babu, N.C. and Gomes, A.J., 2011. Systemic manifestations of oral diseases. Journal of oral and maxillofacial pathology: JOMFP, 15(2), p.144. Read it!
- Sampaio-Maia B, Caldas IM, Pereira ML, Perez-Mongiovi D, Araujo R. The oral microbiome in health and its implication in oral and systemic diseases. In Advances in applied microbiology 2016 Jan 1 (Vol. 97, pp. 171-210). Academic Press. Read it!
- Tanner AC, Kent Jr RL, Holgerson PL, Hughes CV, Loo CY, Kanasi E, Chalmers NI, Johansson I. Microbiota of severe early childhood caries before and after therapy. Journal of dental research. 2011 Nov;90(11):1298-305. Read it!
- Farrell JJ, Zhang L, Zhou H, Chia D, Elashoff D, Akin D, Paster BJ, Joshipura K, Wong DT. Variations of oral microbiota are associated with pancreatic diseases including pancreatic cancer. Gut. 2012 Apr 1;61(4):582-8. Read it!
- Gholizadeh P, Eslami H, Yousefi M, Asgharzadeh M, Aghazadeh M, Kafil HS. Role of oral microbiome on oral cancers, a review. Biomedicine & Pharmacotherapy. 2016 Dec 1;84:552-8. Read it!
- Zhao H, Chu M, Huang Z, Yang X, Ran S, Hu B, Zhang C, Liang J. Variations in oral microbiota associated with oral cancer. Scientific reports. 2017 Sep 18;7(1):1-0. Read it!
- Karpiński TM. Role of oral microbiota in cancer development. Microorganisms. 2019 Jan;7(1):20. Read it!
- Mitchell‐Lewis D, Engebretson SP, Chen J, Lamster IB, Papapanou PN. Periodontal infections and pre‐term birth: early findings from a cohort of young minority women in New York. European journal of oral sciences. 2001 Feb;109(1):34-9.
- Offenbacher S, Lin D, Strauss R, McKaig R, Irving J, Barros SP, Moss K, Barrow DA, Hefti A, Beck JD. Effects of periodontal therapy during pregnancy on periodontal status, biologic parameters, and pregnancy outcomes: a pilot study. Journal of periodontology. 2006 Dec;77(12):2011-24.
- Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR. A human gut microbial gene catalogue established by metagenomic sequencing. nature. 2010 Mar;464(7285):59-65. Read it!
- Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. Dysbiosis of the gut microbiota in disease. Microbial ecology in health and disease. 2015 Dec 1;26(1):26191. Read it!
- Moeller AH, Li Y, Ngole EM, Ahuka-Mundeke S, Lonsdorf EV, Pusey AE, Peeters M, Hahn BH, Ochman H. Rapid changes in the gut microbiome during human evolution. Proceedings of the National Academy of Sciences. 2014 Nov 18;111(46):16431-5. Read it!
- Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009 Dec 18;326(5960):1694-7. Read it!
- Del Chierico F, Vernocchi P, Petrucca A, Paci P, Fuentes S, Praticò G, Capuani G, Masotti A, Reddel S, Russo A, Vallone C. Phylogenetic and metabolic tracking of gut microbiota during perinatal development. PloS one. 2015 Sep 2;10(9):e0137347. Read it!
- Aagaard, K., Ma, J., Antony, K.M., Ganu, R., Petrosino, J. and Versalovic, J., 2014. The placenta harbors a unique microbiome. Science translational medicine, 6(237), pp.237ra65-237ra65. Read it!
- Collado, M.C., Rautava, S., Aakko, J., Isolauri, E. and Salminen, S., 2016. Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Scientific reports, 6, p.23129. Read it!
- Rodríguez, J.M., Murphy, K., Stanton, C., Ross, R.P., Kober, O.I., Juge, N., Avershina, E., Rudi, K., Narbad, A., Jenmalm, M.C. and Marchesi, J.R., 2015. The composition of the gut microbiota throughout life, with an emphasis on early life. Microbial ecology in health and disease, 26(1), p.26050. Read it!
- Jakobsson, H.E., Abrahamsson, T.R., Jenmalm, M.C., Harris, K., Quince, C., Jernberg, C., Björkstén, B., Engstrand, L. and Andersson, A.F., 2014. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut, 63(4), pp.559-566. Read it!
- Chen G, Chiang WL, Shu BC, Guo YL, Chiou ST, Chiang TL. Associations of caesarean delivery and the occurrence of neurodevelopmental disorders, asthma or obesity in childhood based on Taiwan birth cohort study. BMJ open. 2017 Sep 1;7(9):e017086. Read it!
- Sevelsted A, Stokholm J, Bønnelykke K, Bisgaard H. Cesarean section and chronic immune disorders. Pediatrics. 2015 Jan 1;135(1):e92-8. Read it!
- Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proceedings of the National Academy of Sciences. 2010 Jun 29;107(26):11971-5. Read it!
- Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature. 2007 Oct;449(7164):804-10. Read it!
- Rinninella E, Raoul P, Cintoni M, Franceschi F, Miggiano GA, Gasbarrini A, Mele MC. What is the healthy gut microbiota composition? a changing ecosystem across age, environment, diet, and diseases. Microorganisms. 2019 Jan;7(1):14. Read it!
- Morten KJ, Staines-Urias E, Kenyon J. Potential clinical usefulness of gut microbiome testing in a variety of clinical conditions. Human Microbiome Journal. 2018 Oct 1;10. Read it!
- Yang T, Santisteban MM, Rodriguez V, Li E, Ahmari N, Carvajal JM, Zadeh M, Gong M, Qi Y, Zubcevic J, Sahay B. Gut dysbiosis is linked to hypertension. Hypertension. 2015 Jun;65(6):1331-40. Read it!
- Ni J, Shen TC, Chen EZ, Bittinger K, Bailey A, Roggiani M, Sirota-Madi A, Friedman ES, Chau L, Lin A, Nissim I. A role for bacterial urease in gut dysbiosis and Crohn’s disease. Science translational medicine. 2017 Nov 15;9(416):eaah6888. Read it!
- Martinez KB, Leone V, Chang EB. Western diets, gut dysbiosis, and metabolic diseases: Are they linked?. Gut microbes. 2017 Mar 4;8(2):130-42. Read it!
- Inoue T, Nakayama J, Moriya K, Kawaratani H, Momoda R, Ito K, Iio E, Nojiri S, Fujiwara K, Yoneda M, Yoshiji H. Gut dysbiosis associated with hepatitis C virus infection. Clinical Infectious Diseases. 2018 Aug 31;67(6):869-77. Read it!
- Almeida C, Oliveira R, Soares R, Barata P. Influence of gut microbiota dysbiosis on brain function: a systematic review. Porto Biomedical Journal. 2020 Mar 1;5(2):1. Read it!
- Wang L, Alammar N, Singh R, Nanavati J, Song Y, Chaudhary R, Mullin GE. Gut microbial dysbiosis in the irritable bowel syndrome: A systematic review and meta-analysis of case-control studies. Journal of the Academy of Nutrition and Dietetics. 2020 Apr 1;120(4):565-86. Read it!
- Toor D, Wsson MK, Kumar P, Karthikeyan G, Kaushik NK, Goel C, Singh S, Kumar A, Prakash H. Dysbiosis disrupts gut immune homeostasis and promotes gastric diseases. International journal of molecular sciences. 2019 Jan;20(10):2432. Read it!
- Eaton SB, Konner MJ. Review paleolithic nutrition revisited: a twelve-year retrospective on its nature and implications. European journal of clinical nutrition. 1997 Apr;51(4):207-16. Read it!
- O’Keefe SJ. The need to reassess dietary fiber requirements in healthy and critically ill patients. Gastroenterology Clinics. 2018 Mar 1;47(1):219-29. Read it!
- O’Keefe SJ, Li JV, Lahti L, Ou J, Carbonero F, Mohammed K, Posma JM, Kinross J, Wahl E, Ruder E, Vipperla K. Fat, fibre and cancer risk in African Americans and rural Africans. Nature communications. 2015 Apr 28;6:6342. Read it!
- Makki K, Deehan EC, Walter J, Bäckhed F. The impact of dietary fiber on gut microbiota in host health and disease. Cell host & microbe. 2018 Jun 13;23(6):705-15. Read it!
- De Palma G, Blennerhassett P, Lu J, Deng Y, Park AJ, Green W, Denou E, Silva MA, Santacruz A, Sanz Y, Surette MG. Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nature communications. 2015 Jul 28;6(1):1-3.Read it!
- Rea K, Dinan TG, Cryan JF. The microbiome: a key regulator of stress and neuroinflammation. Neurobiology of stress. 2016 Oct 1;4:23-33. Read it!