Stress and the gut-brain axis: Cognitive performance, mood state, and biomarkers of blood-brain barrier and intestinal permeability following severe physical and psychological stress.

Autor: Varanoske AN; Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine (USARIEM), Natick, MA, USA; Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN, USA., McClung HL; Biophysics and Biomedical Modeling Division, USARIEM, Natick, MA, USA., Sepowitz JJ; Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine (USARIEM), Natick, MA, USA., Halagarda CJ; U.S. Marine Forces Special Operations Command, Camp Lejeune, NC, USA., Farina EK; Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine (USARIEM), Natick, MA, USA., Berryman CE; Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine (USARIEM), Natick, MA, USA; Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN, USA; Department of Nutrition, Food and Exercise Sciences, Florida State University, Tallahassee, FL, USA., Lieberman HR; Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine (USARIEM), Natick, MA, USA., McClung JP; Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine (USARIEM), Natick, MA, USA., Pasiakos SM; Military Performance Division, USARIEM, Natick, MA, USA., Philip Karl J; Military Nutrition Division, U.S. Army Research Institute of Environmental Medicine (USARIEM), Natick, MA, USA. Electronic address: james.p.karl.civ@mail.mil.
Jazyk: angličtina
Zdroj: Brain, behavior, and immunity [Brain Behav Immun] 2022 Mar; Vol. 101, pp. 383-393. Date of Electronic Publication: 2022 Feb 05.
DOI: 10.1016/j.bbi.2022.02.002
Abstrakt: Background: Physical and psychological stress alter gut-brain axis activity, potentially causing intestinal barrier dysfunction that may, in turn, induce cognitive and mood impairments through exacerbated inflammation and blood brain barrier (BBB) permeability. These interactions are commonly studied in animals or artificial laboratory environments. However, military survival training provides an alternative and unique human model for studying the impacts of severe physical and psychological stress on the gut-brain axis in a realistic environment.
Purpose: To determine changes in intestinal barrier and BBB permeability during stressful military survival training and identify relationships between those changes and markers of stress, inflammation, cognitive performance, and mood state.
Materials and Methods: Seventy-one male U.S. Marines (25.2 ± 2.6 years) were studied during Survival, Evasion, Resistance, and Escape (SERE) training. Measurements were conducted on day 2 of the 10-day classroom phase of training (PRE), following completion of the 7.5-day field-based simulation phase of the training (POST), and following a 27-day recovery period (REC). Fat-free mass (FFM) was measured to assess the overall physiologic impact of the training. Biomarkers of intestinal permeability (liposaccharide-binding protein [LBP]) and BBB permeability (S100 calcium-binding protein B [S100B]), stress (cortisol, dehydroepiandrosterone sulfate [DHEA-S] epinephrine, norepinephrine) and inflammation (interleukin-6 [IL-6], high-sensitivity C-reactive protein [hsCRP]) were measured in blood. Cognitive performance was assessed by psychomotor vigilance (PVT) and grammatical reasoning (GR) tests, and mood state by the Profile of Mood States (total mood disturbance; TMD), General Anxiety Disorder-7 (GAD-7), and Patient Health (PHQ-9) questionnaires.
Results: FFM, psychomotor vigilance, and LBP decreased from PRE to POST, while TMD, anxiety, and depression scores, and S100B, DHEA-S, IL-6, norepinephrine, and epinephrine concentrations all increased (all p ≤ 0.01). Increases in DHEA-S were associated with decreases in body mass (p = 0.015). Decreases in FFM were associated with decreases in LBP concentrations (p = 0.015), and both decreases in FFM and LBP were associated with increases in TMD and depression scores (all p < 0.05) but not with changes in cognitive performance. Conversely, increases in S100B concentrations were associated with decreases in psychomotor vigilance (p < 0.05) but not with changes in mood state or LBP concentrations.
Conclusions: Evidence of increased intestinal permeability was not observed in this military survival training-based model of severe physical and psychological stress. However, increased BBB permeability was associated with stress and cognitive decline, while FFM loss was associated with mood disturbance, suggesting that distinct mechanisms may contribute to decrements in cognitive performance and mood state during the severe physical and psychological stress experienced during military survival training.
(Published by Elsevier Inc.)
Databáze: MEDLINE
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