Susceptibility to stress and nature exposure: Unveiling differential susceptibility to physical environments; a randomized controlled trial

Abstract

Background: Emerging epidemiological evidence indicates nature exposure could be associated with greater health benefits among groups in lower versus higher socioeconomic positions. One possible mechanism underpinning this evidence is described by our framework: (susceptibility) adults in low socioeconomic positions face higher exposure to persistent psychosocial stressors in early life, inducing a pro-inflammatory phenotype as a lifelong susceptibility to stress; (differential susceptibility) susceptible adults are more sensitive to the health risks of adverse (stress-promoting) environments, but also to the health benefits of protective (stress-buffering) environments.

Objective: Experimental investigation of a pro-inflammatory phenotype as a mechanism facilitating greater stress recovery from nature exposure.

Methods: We determined differences in stress recovery (via heart rate variability) caused by exposure to a nature or office virtual reality environment (10 min) after an acute stressor among 64 healthy college-age males with varying levels of susceptibility (socioeconomic status, early life stress, and a pro-inflammatory state [inflammatory reactivity and glucocorticoid resistance to an in vitro bacterial challenge]).

Results: Findings for inflammatory reactivity and glucocorticoid resistance were modest but consistently trended towards better recovery in the nature condition. Differences in recovery were not observed for socioeconomic status or early life stress.

Discussion: Among healthy college-age males, we observed expected trends according to their differential susceptibility when assessed as inflammatory reactivity and glucocorticoid resistance, suggesting these biological correlates of susceptibility could be more proximal indicators than self-reported assessments of socioeconomic status and early life stress. If future research in more diverse populations aligns with these trends, this could support an alternative conceptualization of susceptibility as increased environmental sensitivity, reflecting heightened responses to adverse, but also protective environments. With this knowledge, future investigators could examine how individual differences in environmental sensitivity could provide an opportunity for those who are the most susceptible to experience the greatest health benefits from nature exposure.

Fig 1. Theoretical framework.

Emerging epidemiological evidence indicates that nature exposure could be associated with cardiovascular health among individuals in low socioeconomic positions to a greater degree than among more privileged groups. One possible mechanism underpinning this evidence is described by our theoretical framework: (Panel A; Susceptibility [Measures]) individuals in low socioeconomic positions^A, compared to those in higher positions, are at risk for higher exposure to stressors in early life^B and a pro-inflammatory phenotype^C induced by early life stress; (Panel B; Differential Susceptibility [Outcomes]) susceptible individuals are more sensitive to the health risks of adverse environments (e.g., worse recovery from stress), relative to less susceptible individuals, but also are more sensitive to the health benefits of protective environments (e.g., better recovery from stress), relative to less susceptible individuals. (A) Socioeconomic status is defined as the position of an individual in their society which is determined by both social and economic factors that impact exposure to and experiences with psychosocial stressors [63]. (B) Early life stress is defined as persistent exposure to stressors during childhood, with ranging degrees of perceived severity, that induce psychobiological responses and could promote neurodevelopmental alterations over time [64]. (C) A pro-inflammatory phenotype is defined as increased neuro-immune reactivity to psychological and biological stressors combined with resistance to anti-inflammatory signals [27, 28]. Panel B was adapted from “For Better and For Worse: Differential Susceptibility to Environmental Influences” by Jay Belsky, Marian J. Bakermans-Kranenburg, and Marinus H. van IJzendoorn, 2007, Current Directions in Psychological Science, 16(6), 300–304. Copyright 2007 by Association for Psychological Science. Adapted with permission.

Fig 2. Flow diagram of exposure experiment.

Stress recovery was assessed using heart rate variability to index changes in autonomic activation (sympathetic and parasympathetic) from baseline to the recovery period. Susceptibility indicators (socioeconomic status, early life stress, inflammatory reactivity, and glucocorticoid resistance) were assessed at various time points. Socioeconomic status (MacArthur Scale of Subjective Social Status) and early life stress (Adverse Childhood Experience Questionnaire) were measured during an initial visit to the laboratory within three days of the exposure experiment. Inflammatory reactivity and glucocorticoid resistance (in vitro bacterial challenge) were assessed using serum collected before the start of the exposure experiment.

Fig 3. Virtual reality environments.

Equirectangular depictions of the 360-degree 8k stationary recordings (Insta360 Pro™, Insta360.Inc, Shenzhen, Hong Kong) delivered in virtual reality using a commercial headset (VIVE Pro™, HTC Corporation, Taoyuan, Taiwan) after participants experienced an acute stressor. The virtual greenspace environment (nature) was recorded at a public park within the same county as the university where the exposure experiment was conducted. The virtual indoor environment (office) was recorded at the same university office used for the experiment. Participants were seated in a chair for the duration of the exposure (10 min).

Fig 4. Forest plots of standardized effects (Continuous interaction terms).

Forest plots visualizing interaction terms (standardized coefficients and confidence intervals [95%]) across all multiple regression models. Within these plots, all models were specified so that among participants with higher susceptibility (continuous), positive interaction terms indicate greater stress recovery (increased parasympathetic and reduced sympathetic activation) in the nature versus office condition while negative terms indicate greater stress recovery in the office versus nature condition. Interaction terms at zero indicate no differences in the association between susceptibility and stress recovery (autonomic activation) by condition group. * p < .05.

Fig 5. Interaction plots: Susceptibility by condition on autonomic activation (Recovery).

Interaction plots visualizing significant associations (slopes) between susceptibility and stress recovery (autonomic activation) by condition group (nature [solid black line] versus office [dashed gray line]). Y-axes present sympathetic or parasympathetic activation using fitted values (unstandardized) from the corresponding regression model (baseline adjusted metric of autonomic activity [log] during the recovery period [40 min]). X-axes present susceptibility indicators using log-values. P-values (beta weights) represent the interaction term.