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.

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.

Testosterone status following short-term, severe energy deficit is associated with fat-free mass loss in U.S. Marines.

The objective of this study was to determine metabolic and physiological differences between males with low testosterone (LT) versus those with normal testosterone (NT) following a period of severe energy deficit. In this secondary analysis, 68 male US Marines (mean ± SD, 24.6 ± 2.4 y) were dichotomized by testosterone concentration (< or ≥ 10.5 nmol/L as determined from a single blood sample collected between 0600-0630 after an 8-10 h overnight fast by automated immunoassay) following 7 days of near complete starvation (~300 kcal consumed/d, ~85% energy deficit) during Survival, Evasion, Resistance, and Escape (SERE) training. Dietary intake was assessed before (PRE) SERE. Body composition (dual-energy x-ray absorptiometry and peripheral quantitative computed tomography) and whole-body protein turnover (15 N alanine) were assessed before (PRE) and after (POST) SERE. Mean testosterone concentrations decreased PRE (17.5 ± 4.7 nmol/L) to POST (9.8 ± 4.0 nmol/L, p < 0.0001). When volunteers were dichotomized by POST testosterone concentrations [NT (n = 24) 14.1 ± 3.4 vs. LT (n = 44): 7.5 ± 1.8 nmol/L, p < 0.0001], PRE BMI, total fat mass, trunk fat mass, and testosterone were greater and the diet quality score and total carbohydrate intake were lower in NT compared to LT (p ≤ 0.05). LT lost more fat-free mass and less fat mass, particularly in the trunk region, compared to NT following SERE (p-interaction≤0.044). Whole-body protein synthesis, net balance, and flux decreased and whole-body protein breakdown increased from PRE to POST in both groups (p-time ≤0.025). Following short-term, severe energy deficit, Marines who exhibited low testosterone had greater fat-free mass loss than those who maintained normal testosterone concentrations. Altering body composition and dietary strategies prior to physical training that elicits severe energy deficit may provide an opportunity to attenuate post-training decrements in testosterone and its associated effects (e.g., loss of lean mass, performance declines, fatigue).

Energy Balance and Diet Quality During the US Marine Corps Forces Special Operations Command Individual Training Course.

METHODS: This study characterized the total daily energy expenditure (TDEE), energy intake (EI), body weight, and diet quality (using the Healthy Eating Index-2010 [HEI]) of 20 male US Marines participating in the 9-month US Marine Corps Forces Special Operations Command Individual Training Course (ITC). RESULTS: TDEE was highest (ρ < .05) during Raider Spirit (RS; 6,376 ± 712kcal/d) compared with Survival, Evasion, Resistance, and Escape (SERE; 4,011 ± 475kcal/d) School, Close-Quarters Battle (CQB; 4,189 ± 476kcal/d), and Derna Bridge (DB; 3,754 ± 314kcal/d). Body mass was lost (ρ < .05) during SERE, RS, and DB because EI was less than TDEE (SERE, -3,665kcal/d ± 475kcal/d; RS, -3,966 ± 776kcal/d; and DB, -1,027 ± 740kcal/d; p < .05). However, body mass was restored before the start of each subsequent phase and was not different between the start (86.4 ± 9.8kg) and end of ITC (86.7 ± 9.0kg). HEI score declined during ITC (before, 65.6 ± 11.2 versus after, 60.9 ± 9.7; p < .05) because less greens or beans and more empty calories were consumed (ρ < .05). Dietary protein intake was lowest during RS (0.9 ± 0.4g/kg) compared with all other phases, and carbohydrate intake during RS (3.6 ± 1g/kg), CQB (3.6 ± 1.0g/kg), and DB (3.7 ± 1.0g/kg) was lower than during the academic phase of SERE (5.1 ± 1.0g/kg; p < .05). CONCLUSION: These data suggest that ITC students, on average, adequately restore body mass between intermittent periods of negative energy balance. Education regarding the importance of maintaining healthy eating patterns while in garrison, consuming more carbohydrate and protein, and better matching EI with TDEE during strenuous training exercises may be warranted.

US Military Dietary Protein Recommendations: A Simple But Often Confused Topic.

Military recommendations for dietary protein are based on the recommended dietary allowance (RDA) of 0.8 g of protein per kilogram of body mass (BM) established by the Food and Nutrition Board, Institute of Medicine (IOM) of the National Academies. The RDA is likely adequate for most military personnel, particularly when activity levels are low and energy intake is sufficient to maintain a healthy body weight. However, military recommendations account for periods of increased metabolic demand during training and real-world operations, especially those that produce an energy deficit. Under those conditions, protein requirements are higher (1.5-2.0 g/kg BM) in an attempt to attenuate the unavoidable loss of muscle mass that occurs during prolonged or repeated exposure to energy deficits. Whole foods are recommended as the primary method to consume more protein, although there are likely operational scenarios where whole foods are not available and consuming supplemental protein at effective, not excessive, doses (20-25 g or 0.25-0.3 g/kg BM per meal) is recommended. Despite these evidence-based, condition-specific recommendations, the necessity of protein supplements and the requirements and rationale for consuming higher-protein diets are often misunderstood, resulting in an overconsumption of dietary protein and unsubstantiated health-related concerns. This review will provide the basis of the US military dietary protein requirements and highlight common misconceptions associated with the amount and safety of protein in military diets.

Supplemental genistein, quercetin, and resveratrol intake in active duty army soldiers.

Previous reports indicate that the majority of U.S. Army soldiers consume dietary supplements (DSs) > 1 time/wk. However, these studies did not evaluate phytonutrient supplementation. A growing literature suggests inclusion of phytonutrients in DSs may pose a risk for toxicity, which could impact the performance of soldier duties, as well as long-term health and wellness. This study was conducted to assess and understand soldiers' motivations to consume phytonutrient-containing DSs, specifically genistein, quercetin, and resveratrol. The study was a cross-sectional, descriptive mixed-methods design using a survey and semistructured interviews. There were 436 soldiers stationed at Joint Base Lewis-McChord, Washington who completed the survey, from which 36 soldiers completed an interview. Overall, 34% of soldiers reported taking a single or multicomponent phytonutrient DS > 1 time/wk, from which 41 soldiers took >1 supplement/wk. Soldiers' reasons for use included unsure (54%), weight loss (12%), and other, unspecified (24%). The majority of interviewees did not consume DSs based on inclusion of genistein, quercetin, or resveratrol. The majority of soldiers, in our study, appear unable to rationalize their phytonutrient DS choices. Findings from this study illuminate the need for future research to further explore DS practices within military populations and encourage informed use of DSs.