This special issue of Psychosomatic Medicine focuses on brain-gut interactions and the intestinal microenvironment. Guest Editors Emeran Mayer andElaine Hsiao provide an overview of the issue, which was inspired by a symposium on the topic convened by the American Psychosomatic Society (APS) and the American Gastroenterological Association (AGA).
A perspective on brain-gut communication is provided by Aroniadis, Drossman, andSimrén. This white paper presents a summary of the APS/AGA symposium. A characterization of the intestinal microbial functioning is presented as well as evidence for the interactions between the intestinal microbiome, the host, and the environment. The role of the intestinal microbiome in medical and neuropsychiatric diseases and psychological disorders is reviewed as well as the treatment effects of manipulation of the intestinal microbiome.
Recent studies of microbiota composition have raised the question of whether there are disease-specific intestinal microbiota signatures in inflammatory bowel disease (IBD) and irritable bowel syndrome (IBS). In this review, Sundin et al. summarize the current knowledge of microbial dysbiosis in IBS and IBD and review intrinsic factors (e.g., genetic factors and the host immune system) and extrinsic factors (early life diet, method of infant delivery) as important contributors to the variations in findings in IBD and IBS.
Fecal microbiota transplant (FMT) has been used to treat a wide range of diseases, but results have been mixed. Lawrence J. Brandt provides an overview of this literature in which the use of FMT has been consistent only in the treatment of Clostridium difficile colitis Conclusions about FMT efficacy in other GI diseases still await well-designed trials.
In a review, de Clercq et al. document that obesity and metabolic dysregulation are associated with reduced microbial diversity. A major challenge in this research is interindividual variability of the microbiome. The microbial metabolites, short chain fatty acids (SCFAs), may play an important role in dysregulated metabolic processes. Advanced mapping of the human microbiome is necessary to develop targeted interventions for obesity and metabolic syndrome.
Sanmiguel et al. explored whether changes in gut microbiota after weight-loss surgery are associated with weight loss and changes in appetite and hedonic eating. In women who underwent laparoscopic sleeve gastrectomy, a microbial signature comprised of five bacterial genera discriminated between pre- and post-surgery status. Gut microbial profiles were associated with surgically induced reductions in appetite and in food addiction measures.
The weaning of infants from the mother and increased social contact with peers is a developmental stage that is likely to affect the gut microbiome. Amaral et al. evaluated the bacterial profiles of young monkeys, prospectively investigating them on day 1 and again 2 weeks after rehousing away from the mother and group formation. Combining weaned infants into small social groups led to a microbial convergence by 2 weeks. Diversity analyses indicated a more similar microbiota community structure within peer groups than across groups.
The association between individual differences in temperament traits with microbiome enterotypes in healthy adults was examined by Kim andPark. Results showed that the level of novelty seeking and reward dependence was related to two enterotype groups, one predominantly characterized by Bacteroidaceae and the other by Prevotellaceae. This association between psychological traits and the gut microbiome may develop early in life.
In a study of 40 women, Tillisch et al. identified brain and behavioral characteristics clustered by gut microbiota profiles. Two bacterial genus-based clusters were identified, one with greater Bacteroides abundance, and one with greater Prevotella abundance. The groups differed in hippocampal activity during the viewing of negative valence images. Differences in emotional, attentional, and sensory processing regions were observed in the Prevotella cluster. The Bacteroides cluster was associated with greater gray matter volumes of the cerebellum and hippocampus.
Probiotic supplementation has been associated with cardiovascular health benefits. Möller et al. conducted a clinical trial to examine probiotic influence on resting cardiovascular activity and cardiovascular and psychological responses to acute cognitive stress. Results showed that supplemental intake of mixed-species, mixed-strain probiotics over 2 weeks did not change measures of cardiovascular or psychological responsivity to stress in healthy young adults. Additional research varying strains, species, and dosage is needed to further understand the link between microbiota and cardiovascular health.
In a literature review, Dinan andCryan assess the potential usefulness and limitations of the brain-gut-microbiota axis paradigm as related to psychiatric and psychological disorders. There is now a large preclinical literature on psychobiotics—bacteria shown to have a positive mental health benefit when ingested by healthy volunteers. A cocktail of probiotics has been shown to alter brain activity as monitored by functional magnetic resonance imaging. Major clinical studies are needed to examine whether mediating the communication between the brain and microbes in the gut may be a therapeutic target for managing psychiatric illness.
In an exploration of the microbiota-brain-gut axis in children, Michels et al. examined the association of chronic stress with levels of the intestinal inflammation marker fecal calprotectin and levels of fecal short-chain fatty acids, independent of BMI and diet. Higher stress (emotional problems) and low parasympathetic activity were associated with higher levels of the short-chain fatty acids butyrate, valerate, isovalerate, and isobutyrate, but not with the inflammation marker of fecal calprotectin. This is the first preliminary evidence for the stress–gut communication in children.
The microbiome is an important determinant of immunoregulation. Inadequate immunoregulation and elevated levels of inflammation may be risk factors for posttraumatic stress disorder (PTSD). Hemmings et al. investigated the gut microbiome in a sample of individuals with PTSD and a trauma-exposed (TE) comparison group. Measures of overall microbial diversity were similar among individuals with PTSD and TE; however, decreased total abundance of Actinobacteria, Lentisphaerae, and Verrucomicrobia was associated with PTSD status.
In a cross-disciplinary review, Maier andal’Absi outline an ecological framework of the human microbiome that extends the general biopsychosocial model. This perspective integrates the potential theoretical and clinical implications of the articles in this Special Issue of Psychosomatic Medicine. The microbiota appears to be integrated with health and is connected to systems across biological/physical, psychological/behavioral, and social domains that extend far beyond the individual. In order to advance basic and clinical microbiome research, an ecological paradigm encompassing distal factors and environmental health is suggested.