Named Series/Harrison: Neuroimaging, Inflammation and Behaviour Mind-body interactions in the regulation of airway inflammation in asthma: A PET study of acute and chronic stress

Background: Psychological stress has long been recognized as a contributing factor to asthma symptom expression and disease progression. Yet, the neural mechanisms that underlie this relationship have been largely unexplored in research addressing the pathophysiology and management of asthma. Studies that have examined the mechanisms of this relationship in the periphery suggest that it is the superimposition of acute stress on top of chronic stress that is of greatest concern for airway inflammation. Methods: We compared asthmatic individuals with high and low levels of chronic life stress in their neural and peripheral physiological responses to the Trier Social Stress Test and a matched control task. We used FDG-PET to measure neural activity during performance of the two tasks. We used both circulating and airway-specific markers of asthma-related inflammation to assess the impact of acute stress in these two groups. Results: Asthmatics under chronic stress had a larger HPA-axis response to an acute stressor, which failed to show the suppressive effects on inflammatory markers observed in those with low chronic stress. Moreover, our PET data suggest that greater activity in the anterior insula during acute stress may reflect regulation of the effect of stress on inflammation. In contrast, greater activity in the mid-insula and perigenual anterior cingulate seems to reflect greater reactivity and was associated with greater airway inflammation, a more robust alpha amylase response, and a greater stress-induced increase in proinflammatory cytokine mRNA expression in airway cells. Conclusions: Acute stress is associated with increases in markers of airway inflammation in asthmatics under chronic stress. This relationship may be mediated by interactions between the insula and anterior cingulate cortex, that determine the salience of environmental cues, as well as descending regulatory influence of inflammatory pathways in the periphery.

[1]  T. Ritz,et al.  Exhaled Nitric Oxide Decreases during Academic Examination Stress in Asthma. , 2015, Annals of the American Thoracic Society.

[2]  W. K. Simmons,et al.  A common gustatory and interoceptive representation in the human mid‐insula , 2015, Human brain mapping.

[3]  M. Kraft,et al.  Update in Asthma 2014. , 2015, American journal of respiratory and critical care medicine.

[4]  M. Bonsignore,et al.  Advances in asthma pathophysiology: stepping forward from the Maurizio Vignola experience , 2015, European Respiratory Review.

[5]  A. Waisman,et al.  The role of IL-17 in CNS diseases , 2015, Acta Neuropathologica.

[6]  J. Cavanagh,et al.  Frontal midline theta reflects anxiety and cognitive control: Meta-analytic evidence , 2015, Journal of Physiology-Paris.

[7]  T. Ritz,et al.  Increases in Exhaled Nitric Oxide After Acute Stress: Association With Measures of Negative Affect and Depressive Mood , 2014, Psychosomatic medicine.

[8]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[9]  Peter Kirsch,et al.  Neuroimaging evidence for a role of neural social stress processing in ethnic minority-associated environmental risk. , 2014, JAMA psychiatry.

[10]  Stephen M. Smith,et al.  Permutation inference for the general linear model , 2014, NeuroImage.

[11]  T. Ritz,et al.  Airway nitric oxide and psychological processes in asthma and health: a review. , 2014, Annals of allergy, asthma & immunology : official publication of the American College of Allergy, Asthma, & Immunology.

[12]  R. Louis,et al.  Importance of concomitant local and systemic eosinophilia in uncontrolled asthma , 2014, European Respiratory Journal.

[13]  Joshua H. Balsters,et al.  The role of the midcingulate cortex in monitoring others' decisions , 2013, Front. Neurosci..

[14]  W. K. Simmons,et al.  Keeping the body in mind: Insula functional organization and functional connectivity integrate interoceptive, exteroceptive, and emotional awareness , 2013, Human brain mapping.

[15]  S. Cole,et al.  Social stress up-regulates inflammatory gene expression in the leukocyte transcriptome via β-adrenergic induction of myelopoiesis , 2013, Proceedings of the National Academy of Sciences.

[16]  C. Pariante,et al.  The role of immune genes in the association between depression and inflammation: A review of recent clinical studies , 2013, Brain, Behavior, and Immunity.

[17]  Cheree James,et al.  Real-time imaging of cortical and subcortical control of muscle sympathetic nerve activity in awake human subjects , 2013, NeuroImage.

[18]  L. Harrington,et al.  Inflammatory T Helper 17 Cells Promote Depression-like Behavior in Mice , 2013, Biological Psychiatry.

[19]  T. Ritz,et al.  Academic exam stress and depressive mood are associated with reductions in exhaled nitric oxide in healthy individuals , 2013, Biological Psychology.

[20]  Q. Hamid,et al.  Glucocorticoid Receptor-Beta Up-Regulation and Steroid Resistance Induction by IL-17 and IL-23 Cytokine Stimulation in Peripheral Mononuclear Cells , 2013, Journal of Clinical Immunology.

[21]  N. Jarjour,et al.  Human eosinophils release IL‐1ß and increase expression of IL‐17A in activated CD4+ T lymphocytes , 2012, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[22]  D. Centonze,et al.  Interleukin-1β Causes Anxiety by Interacting with the Endocannabinoid System , 2012, The Journal of Neuroscience.

[23]  W. Busse,et al.  Are There Neurophenotypes for Asthma? Functional Brain Imaging of the Interaction between Emotion and Inflammation in Asthma , 2012, PloS one.

[24]  S. Wenzel,et al.  Nitric oxide and related enzymes in asthma: relation to severity, enzyme function and inflammation , 2012, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[25]  R. Dweik,et al.  Nitric oxide and asthma severity: towards a better understanding of asthma phenotypes , 2012, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[26]  R. Ho,et al.  The role of interleukin (IL)‐17 in anxiety and depression of patients with rheumatoid arthritis , 2012, International journal of rheumatic diseases.

[27]  Richard E Carson,et al.  Glucose Metabolism in the Insula and Cingulate Is Affected by Systemic Inflammation in Humans , 2012, The Journal of Nuclear Medicine.

[28]  Peisong Chen,et al.  Emerging tendency towards autoimmune process in major depressive patients: A novel insight from Th17 cells , 2011, Psychiatry Research.

[29]  A. Kijlstra,et al.  The Effects of Th17 Cytokines on the Inflammatory Mediator Production and Barrier Function of ARPE-19 Cells , 2011, PloS one.

[30]  R. Davidson,et al.  The integration of negative affect, pain and cognitive control in the cingulate cortex , 2011, Nature Reviews Neuroscience.

[31]  Frank Seifert,et al.  Activation of central sympathetic networks during innocuous and noxious somatosensory stimulation , 2011, NeuroImage.

[32]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

[33]  S. Park,et al.  Interleukin-17 regulation: an attractive therapeutic approach for asthma , 2010, Respiratory research.

[34]  W. Busse,et al.  Use of exhaled nitric oxide measurement to identify a reactive, at-risk phenotype among patients with asthma. , 2010, American journal of respiratory and critical care medicine.

[35]  Volker Arolt,et al.  The Interleukin 1 Beta (IL1B) Gene Is Associated with Failure to Achieve Remission and Impaired Emotion Processing in Major Depression , 2010, Biological Psychiatry.

[36]  L. Bacharier,et al.  Socioeconomic status associated with exhaled nitric oxide responses to acute stress in children with asthma , 2010, Brain, Behavior, and Immunity.

[37]  J. Sheridan,et al.  Social disruption induces lung inflammation , 2010, Brain, Behavior, and Immunity.

[38]  Christian Büchel,et al.  Dyspnea and pain share emotion-related brain network , 2009, NeuroImage.

[39]  H. Critchley,et al.  Inflammation Causes Mood Changes Through Alterations in Subgenual Cingulate Activity and Mesolimbic Connectivity , 2009, Biological Psychiatry.

[40]  H. Critchley,et al.  Neural Origins of Human Sickness in Interoceptive Responses to Inflammation , 2009, Biological Psychiatry.

[41]  J. Sheridan,et al.  Social Stress Enhances Allergen-Induced Airway Inflammation in Mice and Inhibits Corticosteroid Responsiveness of Cytokine Production1 , 2009, The Journal of Immunology.

[42]  Nicolas Rohleder,et al.  Determinants of salivary α-amylase in humans and methodological considerations , 2009, Psychoneuroendocrinology.

[43]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[44]  G. Miller,et al.  Double-Exposure to Acute Stress and Chronic Family Stress is Associated With Immune Changes in Children With Asthma , 2009, Psychosomatic medicine.

[45]  T. Brüning,et al.  Exhaled breath condensate and airway inflammation , 2009, Current opinion in allergy and clinical immunology.

[46]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[47]  G. Canino,et al.  Violence, abuse, and asthma in Puerto Rican children. , 2008, American journal of respiratory and critical care medicine.

[48]  Jamil Zaki,et al.  Your pain or mine? Common and distinct neural systems supporting the perception of pain in self and other. , 2008, Social cognitive and affective neuroscience.

[49]  Richard J. Davidson,et al.  Glucose metabolic changes in the prefrontal cortex are associated with HPA axis response to a psychosocial stressor , 2008, Psychoneuroendocrinology.

[50]  B. Kuehn.  Asthma linked to psychiatric disorders. , 2008, JAMA.

[51]  Ali H Mokdad,et al.  Impact of Depression and Anxiety on Quality of Life, Health Behaviors, and Asthma Control Among Adults in the United States with Asthma, 2006 , 2008, The Journal of asthma : official journal of the Association for the Care of Asthma.

[52]  G. Miller,et al.  Stress and inflammation in exacerbations of asthma , 2007, Brain, Behavior, and Immunity.

[53]  G. Miller,et al.  Socioeconomic status and inflammatory processes in childhood asthma: the role of psychological stress. , 2006, The Journal of allergy and clinical immunology.

[54]  V. Bagaev,et al.  Visceral-related area in the rat insular cortex , 2006, Autonomic Neuroscience.

[55]  P. Frenette,et al.  Signals from the Sympathetic Nervous System Regulate Hematopoietic Stem Cell Egress from Bone Marrow , 2006, Cell.

[56]  James P. Herman,et al.  Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis , 2005, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[57]  A. Steptoe,et al.  Psychological stress activates interleukin-1β gene expression in human mononuclear cells , 2005, Brain, Behavior, and Immunity.

[58]  Tom Johnstone,et al.  Neural circuitry underlying the interaction between emotion and asthma symptom exacerbation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  B. McEwen,et al.  Protection and Damage from Acute and Chronic Stress: Allostasis and Allostatic Overload and Relevance to the Pathophysiology of Psychiatric Disorders , 2004, Annals of the New York Academy of Sciences.

[60]  S. Szefler,et al.  The Aerocrine exhaled nitric oxide monitoring system NIOX is cleared by the US Food and Drug Administration for monitoring therapy in asthma. , 2004, The Journal of allergy and clinical immunology.

[61]  J. Gordon,et al.  Opposing effects of short- and long-term stress on airway inflammation. , 2004, American journal of respiratory and critical care medicine.

[62]  C. Kirschbaum,et al.  Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change , 2003, Psychoneuroendocrinology.

[63]  T. Shallice,et al.  Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. , 2003, Brain : a journal of neurology.

[64]  A. Caspi,et al.  Influence of Life Stress on Depression: Moderation by a Polymorphism in the 5-HTT Gene , 2003, Science.

[65]  Lin Ying Liu,et al.  School examinations enhance airway inflammation to antigen challenge. , 2002, American journal of respiratory and critical care medicine.

[66]  Rosalind J Wright,et al.  Violence: an unrecognized environmental exposure that may contribute to greater asthma morbidity in high risk inner-city populations. , 2001, Environmental health perspectives.

[67]  A. Buist,et al.  Validation of a standardized version of the Asthma Quality of Life Questionnaire. , 1999, Chest.

[68]  G Brix,et al.  Performance evaluation of a whole-body PET scanner using the NEMA protocol. National Electrical Manufacturers Association. , 1997, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[69]  J. R. Augustine.  Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[70]  C. Kirschbaum,et al.  The 'Trier Social Stress Test'--a tool for investigating psychobiological stress responses in a laboratory setting. , 1993, Neuropsychobiology.

[71]  C. Hammen,et al.  Generation of stress in the course of unipolar depression. , 1991, Journal of abnormal psychology.

[72]  D. Cechetto,et al.  Autonomic responses and efferent pathways from the insular cortex in the rat , 1991, The Journal of comparative neurology.

[73]  D. Watson,et al.  Development and validation of brief measures of positive and negative affect: the PANAS scales. , 1988, Journal of personality and social psychology.

[74]  Buist As.  Standardization of spirometry. , 1987 .

[75]  T. Kamarck,et al.  A global measure of perceived stress. , 1983, Journal of health and social behavior.

[76]  M. Mesulam,et al.  Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum , 1982, The Journal of comparative neurology.

[77]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[78]  A. Beck,et al.  An inventory for measuring depression. , 1961, Archives of general psychiatry.

[79]  T. Ritz,et al.  Acute stress-induced increases in exhaled nitric oxide in asthma and their association with endogenous cortisol. , 2011, American journal of respiratory and critical care medicine.

[80]  I. Sora,et al.  The distinctive effects of acute and chronic psychological stress on airway inflammation in a murine model of allergic asthma. , 2007, Allergology international : official journal of the Japanese Society of Allergology.

[81]  Arthur S Slutsky,et al.  Marked flow-dependence of exhaled nitric oxide using a new technique to exclude nasal nitric oxide. , 1997, American journal of respiratory and critical care medicine.

[82]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .