Focusing attention on biological markers of acute stressor intensity: Empirical evidence and limitations

ARMARIO, A, J. Labad and R. Nadal. Focusing attention on biological markers of acute stressor intensity: empirical evidence and limitations. NEUROSCIENCE AND BIOBEHAVIORAL REVIEWS. The availability of biological markers that objectively quantify stress is a highly relevant issue. However, experimental evidence suggests that most physiological changes elicited by emotional stressors do not reflect their intensity and are not useful for this purpose. Thus, we review experimental evidence in animals and humans about the putative validity of neuroendocrine and sympathetic/parasympathetic variables to measure stress. Plasma levels of some hormones (e.g. ACTH, glucocorticoids, prolactin and catecholamines) have been found to reflect, at least under certain conditions, the intensity of emotional stressors in animals and probably in humans. However, the temporal resolution of hormone changes is insufficient to reflect the very dynamic psychological processes taking place while experiencing stressors. Cardiovascular parameters (e.g. heart rate and blood pressure) have much better temporal resolution but their validity as markers of stressor intensity either in animals or humans is problematic. Skin conductance and pupil dilation appear to be promising. Additional and more systematic studies are needed to demonstrate the actual validity of stress-induced physiological changes to quantify stress.

[1]  D. Jezova,et al.  High trait anxiety in healthy subjects is associated with low neuroendocrine activity during psychosocial stress , 2004, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[2]  D. Siddle,et al.  Effects of stimulus intensity on cardiovascular activity. , 1983 .

[3]  G. Yadid,et al.  Heterogeneous neurochemical responses to different stressors: a test of Selye's doctrine of nonspecificity. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[4]  J. Meyerhoff,et al.  Graded footshock stress elevates pituitary cyclic AMP and plasma β-endorphin, β-LPH, corticosterone and prolactin , 1983 .

[5]  S. Southwick,et al.  The Science of Resilience: Implications for the Prevention and Treatment of Depression , 2012, Science.

[6]  J. Sluiter,et al.  Medical staff in emergency situations: severity of patient status predicts stress hormone reactivity and recovery , 2003, Occupational and environmental medicine.

[7]  M. Palkovits,et al.  Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. , 2001, Endocrine reviews.

[8]  Charles A Morgan,et al.  Hormone profiles in humans experiencing military survival training , 2000, Biological Psychiatry.

[9]  S. McDougall,et al.  Differential cardiovascular responses to stressors in hypertensive and normotensive rats , 2005, Experimental physiology.

[10]  W Linden,et al.  Physiological stress reactivity and recovery: conceptual siblings separated at birth? , 1997, Journal of psychosomatic research.

[11]  Postural changes associated with public speech tests lead to mild and selective activation of stress hormone release. , 2007, Journal of physiology and pharmacology : an official journal of the Polish Physiological Society.

[12]  R. Deinzer,et al.  Endocrine and psychological stress responses in a simulated emergency situation , 2011, Psychoneuroendocrinology.

[13]  C. Ring,et al.  Mental stress-induced hemoconcentration: Sex differences and mechanisms. , 2004, Psychophysiology.

[14]  Wolfgang Ellermeier,et al.  Gender differences in pain ratings and pupil reactions to painful pressure stimuli , 1995, Pain.

[15]  H. Ursin,et al.  Modulatory effects of defense and coping on stress-induced changes in endocrine and immune parameters , 1995, International journal of behavioral medicine.

[16]  Warren D. Smith,et al.  Performing laparoscopic surgery is significantly more stressful for the surgeon than open surgery , 2001, Surgical Endoscopy.

[17]  A. Der-Avakian,et al.  Current Status of Animal Models of Posttraumatic Stress Disorder: Behavioral and Biological Phenotypes, and Future Challenges in Improving Translation , 2017, Biological Psychiatry.

[18]  Norman Miller,et al.  Cognitive appraisals and emotions predict cortisol and immune responses: a meta-analysis of acute laboratory social stressors and emotion inductions. , 2009, Psychological bulletin.

[19]  A. Armario,et al.  Anterior pituitary response to stress : time-related changes and adaptation , 1998, International Journal of Developmental Neuroscience.

[20]  Jan M. van Ree,et al.  Endocrine and cardiovascular responses to a series of graded physical and psychological stress stimuli in healthy volunteers , 1995, European Neuropsychopharmacology.

[21]  I. Kopin,et al.  Effect of handling and forced immobilization on rat plasma levels of epinephrine, norepinephrine, and dopamine-beta-hydroxylase. , 1978, Endocrinology.

[22]  D. Roberts,et al.  Adrenal demedullation blocks and brain norepinephrine depletion potentiates the hyperglycemic response to a variety of stressors , 1989, Brain Research.

[23]  M. Nijsen,et al.  Conditioned fear-induced tachycardia in the rat: vagal involvement. , 1998, European journal of pharmacology.

[24]  P. Sawchenko,et al.  Circuits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms. , 2000, Progress in brain research.

[25]  Ulrike Ehlert,et al.  Effects of orthostasis on endocrine responses to psychosocial stress. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[26]  M. Schedlowski,et al.  Time kinetics of the endocrine response to acute psychological stress. , 1996, The Journal of clinical endocrinology and metabolism.

[27]  D Carroll,et al.  The effects of level of difficulty of mental arithmetic challenge on heart rate and oxygen consumption. , 1986, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[28]  Antonio Armario,et al.  What can We Know from Pituitary–Adrenal Hormones About the Nature and Consequences of Exposure to Emotional Stressors? , 2012, Cellular and Molecular Neurobiology.

[29]  I. Jonsdottir,et al.  Prolactin in response to acute psychosocial stress in healthy men and women , 2011, Psychoneuroendocrinology.

[30]  P Hjemdahl,et al.  Cardiovascular and sympathoadrenal responses to mental stress: a study of sensory intake and rejection reactions. , 1990, Acta physiologica Scandinavica.

[31]  A. Armario,et al.  Post-stress recovery of pituitary–adrenal hormones and glucose, but not the response during exposure to the stressor, is a marker of stress intensity in highly stressful situations , 2002, Brain Research.

[32]  S. Campeau,et al.  A detailed characterization of loud noise stress: Intensity analysis of hypothalamo–pituitary–adrenocortical axis and brain activation , 2005, Brain Research.

[33]  Rudy E. Ballieux,et al.  Cardiovascular and endocrine responses to experimental stress: Effects of mental effort and controllability , 1998, Psychoneuroendocrinology.

[34]  J. Gugten,et al.  Mouse strain differences in autonomic responses to stress , 2006, Genes, brain, and behavior.

[35]  M. Palkovits,et al.  Catecholaminergic systems in stress: structural and molecular genetic approaches. , 2009, Physiological reviews.

[36]  J. Herman,et al.  Neural regulation of endocrine and autonomic stress responses , 2009, Nature Reviews Neuroscience.

[37]  E. Katkin,et al.  Vagal Rebound and Recovery From Psychological Stress , 2001, Psychosomatic medicine.

[38]  M. Nattrass,et al.  Physiological response to parachute jumping. , 1987, British medical journal.

[39]  M. Konarska,et al.  Differential plasma catecholamine and neuropeptide Y responses to acute stress in rats. , 1988, Life sciences.

[40]  A. Armario.  The hypothalamic-pituitary-adrenal axis: what can it tell us about stressors? , 2006, CNS & neurological disorders drug targets.

[41]  J. A. Häusser,et al.  The Trier Social Stress Test as a paradigm to study how people respond to threat in social interactions , 2015, Front. Psychol..

[42]  F Boomsma,et al.  Cardiovascular control and plasma catecholamines during rest and mental stress: effects of posture. , 1999, Clinical science.

[43]  Zhenhong Wang,et al.  Extraversion and cardiovascular responses to recurrent social stress: Effect of stress intensity. , 2017, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[44]  B. Natelson,et al.  Humoral indices of stress in rats , 1981, Physiology & Behavior.

[45]  K. Eliasson,et al.  Pace variation and control of work pace as related to cardiovascular, neuroendocrine, and subjective responses , 1986, Biological Psychology.

[46]  J. Slangen,et al.  Plasma catecholamine and corticosterone levels during active and passive shock-prod avoidance behavior in rats: Effects of chlordiazepoxide , 1990, Physiology & Behavior.

[47]  Jun Liu,et al.  Heart Rate and Heart Rate Variability Assessment Identifies Individual Differences in Fear Response Magnitudes to Earthquake, Free Fall, and Air Puff in Mice , 2014, PloS one.

[48]  Bruce S. McEwen,et al.  Allostasis and the Epigenetics of Brain and Body Health Over the Life Course: The Brain on Stress , 2017, JAMA psychiatry.

[49]  R. Callister,et al.  Sympathetic activity is influenced by task difficulty and stress perception during mental challenge in humans. , 1992, The Journal of physiology.

[50]  D. Goldstein,et al.  Evolution of concepts of stress , 2007, Stress.

[51]  M. Dallman,et al.  Integral as well as proportional adrenal responses to ACTH. , 1983, The American journal of physiology.

[52]  E. D. de Geus,et al.  Differential effects of active versus passive coping on secretory immunity. , 2001, Psychophysiology.

[53]  R. Hauger,et al.  Corticotropin-releasing factor receptors and pituitary adrenal responses during immobilization stress. , 1988, Endocrinology.

[54]  Clemens Kirschbaum,et al.  Persistent High Cortisol Responses to Repeated Psychological Stress in a Subpopulation of Healthy Men , 1995, Psychosomatic medicine.

[55]  J. M. Castellanos,et al.  Sensitivity of anterior pituitary hormones to graded levels of psychological stress. , 1986, Life sciences.

[56]  A. Armario,et al.  Stress-induced sensitization: the hypothalamic–pituitary–adrenal axis and beyond , 2015, Stress.

[57]  Sylvia D. Kreibig,et al.  Autonomic nervous system activity in emotion: A review , 2010, Biological Psychology.

[58]  R. M. Escorihuela,et al.  Long-term neuroendocrine and behavioural effects of a single exposure to stress in adult animals , 2008, Neuroscience & Biobehavioral Reviews.

[59]  G. Chrousos,et al.  Clinical review 104: Adrenocorticotropin (ACTH)- and non-ACTH-mediated regulation of the adrenal cortex: neural and immune inputs. , 1999, The Journal of clinical endocrinology and metabolism.

[60]  O. Wolkowitz,et al.  Controllable and uncontrollable stress in humans: alterations in mood and neuroendocrine and psychophysiological function. , 1987, The American journal of psychiatry.

[61]  A. Armario,et al.  Sensitivity of corticosterone and some metabolic variables to graded levels of low intensity stresses in adult male rats , 1986, Physiology & Behavior.

[62]  Clemens Kirschbaum,et al.  Dissociation Between Reactivity of the Hypothalamus-Pituitary-Adrenal Axis and the Sympathetic-Adrenal-Medullary System to Repeated Psychosocial Stress , 2003, Psychosomatic medicine.

[63]  M Frankenhaeuser,et al.  Behavior and circulating catecholamines. , 1971, Brain research.

[64]  A. Armario,et al.  Recovery of the Hypothalamic-Pituitary-Adrenal Response to Stress , 2000, Neuroendocrinology.

[65]  D. Carroll,et al.  A General Enhancement of Autonomic and Cortisol Responses During Social Evaluative Threat , 2009, Psychosomatic medicine.

[66]  Ahmad R. Hariri,et al.  Experiential, autonomic, and neural responses during threat anticipation vary as a function of threat intensity and neuroticism , 2011, NeuroImage.

[67]  Antonio Armario,et al.  Adaptation of the hypothalamus–pituitary–adrenal axis to daily repeated stress does not follow the rules of habituation: A new perspective , 2015, Neuroscience & Biobehavioral Reviews.

[68]  A. Hupbach,et al.  Beyond the Stress Concept: Allostatic Load—A Developmental Biological and Cognitive Perspective , 2015 .

[69]  P. Brazeau,et al.  Pattern of adenohypophyseal hormone changes induced by various stressors in female and male rats. , 1978, Neuroendocrinology.

[70]  W. Vale,et al.  Diminished responsiveness of the hypothalamic-pituitary-adrenal axis of the rat during exposure to prolonged stress: a pituitary-mediated mechanism. , 1987, Endocrinology.

[71]  P. Carrive,et al.  Hypocretin /orexin contributes to the expression of some but not all forms of stress and arousal , 2009, The European journal of neuroscience.

[72]  C. Chapman,et al.  Central noradrenergic mechanisms and the acute stress response during painful stimulation , 2014, Journal of psychopharmacology.

[73]  A. Armario.  Studying Chronic Stress in Animals: Purposes, Models and Consequences , 2015 .

[74]  C. Kirschbaum,et al.  Human hypothalamus–pituitary–adrenal axis responses to acute psychosocial stress in laboratory settings , 2010, Neuroscience & Biobehavioral Reviews.

[75]  S. Levine,et al.  Sensitive pituitary-adrenal responsiveness to varying intensities of psychological stimulation , 1978, Physiology & Behavior.

[76]  D. Jezova,et al.  Psychosocial stress based on public speech in humans: is there a real life/laboratory setting cross-adaptation? , 2016, Stress.

[77]  Konstantina Zougkou,et al.  Preconscious Processing Biases Predict Emotional Reactivity to Stress , 2010, Biological Psychiatry.

[78]  S. Dickerson,et al.  Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. , 2004, Psychological bulletin.

[79]  A. Armario,et al.  Critical features of acute stress-induced cross-sensitization identified through the hypothalamic-pituitary-adrenal axis output , 2016, Scientific Reports.

[80]  F M Kopacz,et al.  Sex differences in skin conductance measures as a function of shock threat. , 1971, Psychophysiology.

[81]  J. Koolhaas,et al.  Different Sympathovagal Modulation of Heart Rate During Social and Nonsocial Stress Episodes in Wild-Type Rats , 1999, Physiology & Behavior.

[82]  Michael D. Robinson,et al.  Measures of emotion: A review , 2009, Cognition & emotion.

[83]  G. Croiset,et al.  Shock-prod burying test in rats: Autonomic and behavioral responses , 1991, Physiology & Behavior.

[84]  Pascal Carrive,et al.  Changes in cutaneous and body temperature during and after conditioned fear to context in the rat , 2005, The European journal of neuroscience.

[85]  J. Thayer,et al.  Physiological concomitants of perseverative cognition: A systematic review and meta-analysis. , 2016, Psychological bulletin.

[86]  P. Alboni,et al.  Typical vasovagal syncope as a “defense mechanism” for the heart by contrasting sympathetic overactivity , 2017, Clinical Autonomic Research.

[87]  Mark Hamer,et al.  Chronic psychosocial factors and acute physiological responses to laboratory-induced stress in healthy populations: a quantitative review of 30 years of investigations. , 2008, Psychological bulletin.

[88]  Susanne Fischer,et al.  Intra-individual psychological and physiological responses to acute laboratory stressors of different intensity , 2015, Psychoneuroendocrinology.

[89]  N. Schneiderman,et al.  Stress and health: psychological, behavioral, and biological determinants. , 2005, Annual review of clinical psychology.

[90]  Eva Walther,et al.  Virtually stressed? A refined virtual reality adaptation of the Trier Social Stress Test (TSST) induces robust endocrine responses , 2019, Psychoneuroendocrinology.

[91]  R. Sapolsky,et al.  How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. , 2000, Endocrine reviews.

[92]  Joris C Verster,et al.  The effect of stress on core and peripheral body temperature in humans , 2013, Stress.

[93]  J. Herman,et al.  Dissociation of ACTH and glucocorticoids , 2008, Trends in Endocrinology & Metabolism.

[94]  D. Hellhammer,et al.  Habituation of cortisol responses to repeated psychosocial stress—further characterization and impact of genetic factors , 2005, Psychoneuroendocrinology.

[95]  Punishment shock intensity and basal skin resistance. , 1965, Journal of the experimental analysis of behavior.

[96]  M. Lachman,et al.  Cortisol response to challenge involving low controllability: The role of control beliefs and age , 2013, Biological Psychology.

[97]  S. Dickerson,et al.  Assessing the relationship between rumination and cortisol: a review. , 2012, Journal of psychosomatic research.

[98]  P. Netter,et al.  Cortisol reaction in success and failure condition in endogenous depressed patients and controls , 1993, Psychoneuroendocrinology.

[99]  W. Lovallo,et al.  Cardiovascular reactivity: mechanisms and pathways to cardiovascular disease. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[100]  G. Chrousos,et al.  The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. , 1992, JAMA.

[101]  Cristina M. Alberini,et al.  Stress and glucocorticoid receptor-dependent mechanisms in long-term memory: From adaptive responses to psychopathologies , 2014, Neurobiology of Learning and Memory.

[102]  A. Armario,et al.  Acute stress markers in humans: Response of plasma glucose, cortisol and prolactin to two examinations differing in the anxiety they provoke , 1996, Psychoneuroendocrinology.

[103]  F. López,et al.  Estimation of endogenous adrenocorticotropin half-life using pulsatility patterns: a physiological approach to the evaluation of secretory episodes. , 1988, Endocrinology.