The influence of cecal microbiota transplantation on chicken injurious behavior: Perspective in human neuropsychiatric research

Authors: FU, YEUCHI - Purdue University; Cheng, Heng-Wei

Submitted to: Biomedicines
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/13/2024
Publication Date: 8/16/2024
Citation: Fu, Y., Cheng, H. 2024. The influence of cecal microbiota transplantation on chicken injurious behavior: Perspective in human neuropsychiatric research. Biomedicines. https://doi.org/10.3390/biom14081017.
DOI: https://doi.org/10.3390/biom14081017

Interpretive Summary: Social stress-induced injurious behaviors (such as aggressive pecking, feather pecking, and cannibalism) have been recognized as one of the most important unsolved health and welfare issues facing the egg industry worldwide. Recent studies have revealed that gut microbiota plays a critical role in early programming and later responsivity of the stress systems in both humans and animals including chickens. In this study, the effects of modification of gut microbiota on aggressiveness and related injurious behaviors in chickens were investigated. Cecal bacteria of two divergently selected inbred genetic lines (donors) were analyzed, and then orally transferred separately into newly hatched male chicks of a commercial layer strain (recipients). The results indicate that social stress and related abnormal behaviors in chickens can be reduced by modification of gut microbiota composition and brain function. The results provide a novel strategy for reducing injurious behaviors and improving welfare in chickens.

Technical Abstract: Mental disorders (psychiatric disorders) with aggression (or violence) pose a significant challenge to public health and contribute to a substantial economic burden worldwide. Especially, social disorganization (or social inequality) associated with childhood adversity has long-lasting effects on mental health, increasing the risk of developing neuropsychiatric disorders. Intestinal bacteria, functionally as an endocrine organ, release various immunomodulators and neuroactive compounds directly or indirectly regulating a host’s physiological and behavioral homeostasis. Under various social challenges, stress-induced dysbiosis increases gut permeability causing a serial reaction: sequentially releasing neurotoxic compounds, leading to neuroinflammation and neuronal injury, and eventually neuropsychiatric disorders associated with aggressive, violent, or impulsive behavior in humans and animals via the microbiota-gut-brain (MGB) axis. The dysregulation of the MGB axis has also been recognized as one of reasons for the prevalence of social stress-induced injurious behaviors (aggressive pecking, feather pecking, and cannibalism) in laying hens. However, existing knowledge of preventing and treating those disorders in both humans and chickens is not well understood. Recently, we have developed a non-mammal model to rationalize the effects of gut microbiota on injurious behaviors in chickens. This perspective article outlines the possibility of reducing stress-induced injurious behaviors through modifying gut microbiota via cecal microbiota transplantation (CMT). In this multi-year study, the cecal contents were collected from two divergently selected inbred chicken lines (donors: lines 63 and 72 selected for resistance or susceptibility to Marek’s disease) with nonaggressive and aggressive behaviors, respectively, then orally transferred to day-old chicks of a commercial layer strain (recipients). An important discovery of this investigation is that CMT at an early age affects the development of the gut microbiota composition and stress-induced injurious behaviors in recipient chickens with long-lasting effects via regulating the activity of brain serotonergic system through the MGB axis, without donor-recipient genetic effects. Non-aggressive donors’ recipients (63-CMT birds, received cecal contents from 63 donors) showed less aggressive pecking behavior under stress condition with higher brain serotonergic activities than aggressive donors’ recipients (72-CMT birds, received cecal contents from 72 donors). The results provide novel insights into developing intervention strategies to prevent injurious behaviors in laying hens. It may also provide biotherapeutic rationale for preventing injurious behavior among individuals with mental disorders via restoring gut microbiota diversity and function.