Conceptual endophenotypes: A strategy to advance the impact of psychoneuroendocrinology in precision medicine

Psychobiological research has generated a tremendous amount of findings on the psychological, neuroendocrine, molecular and environmental processes that are directly relevant for mental and physical health, but have overwhelmed our capacity to meaningfully absorb, integrate, and utilize this knowledge base. Here, we reflect about suitable strategies to improve the translational success of psychoneuroendocrinological research in the era of precision medicine. Following a strategy advocated by the National Research Council and the tradition of endophenotype-based research, we advance here a new approach, termed "conceptual endophenotypes". We define the contextual and formal criteria of conceptual endophenotypes, outline criteria for filtering and selecting information, and describe how conceptual endophenotypes can be validated and implemented at the bedside. As proof-of-concept, we describe some of our findings from research that has adopted this approach in the context of stress-related disorders. We argue that conceptual endophenotypes engineer a bridge between the bench and the bedside. This approach readily lends itself to being continuously developed and implemented. Recent methodological advances, including digital phenotyping, machine learning, grassroots collaboration, and a learning healthcare system, may accelerate the development and implementation of this conceptual endophenotype approach.

[1]  John Blangero,et al.  Arguments for the sake of endophenotypes: Examining common misconceptions about the use of endophenotypes in psychiatric genetics , 2014, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[2]  A. Chekroud,et al.  Bigger Data, Harder Questions-Opportunities Throughout Mental Health Care. , 2017, JAMA psychiatry.

[3]  John P. A. Ioannidis,et al.  What does research reproducibility mean? , 2016, Science Translational Medicine.

[4]  James Shields,et al.  Etiology of Psychosis. (Book Reviews: Schizophrenia and Genetics. A Twin Study Vantage Point) , 1972 .

[5]  G. Chrousos,et al.  Glucocorticoid action networks and complex psychiatric and/or somatic disorders , 2007, Stress.

[6]  J. Moncrieff,et al.  Psychiatry beyond the current paradigm , 2012, British Journal of Psychiatry.

[7]  C. Nemeroff,et al.  Personalized Medicine and Mood Disorders. , 2015, The Psychiatric clinics of North America.

[8]  R. Tandon,et al.  Psychiatry is a clinical neuroscience, but how do we move the field? , 2015, Asian journal of psychiatry.

[9]  Alexandre Pouget,et al.  A better way to crack the brain , 2016, Nature.

[10]  Sarah M. Greene,et al.  Implementing the Learning Health System: From Concept to Action , 2012, Annals of Internal Medicine.

[11]  B. McEwen Allostasis and Allostatic Load: Implications for Neuropsychopharmacology , 2000, Neuropsychopharmacology.

[12]  C. Wild,et al.  The exposome: from concept to utility. , 2012, International journal of epidemiology.

[13]  J. Westfall,et al.  Practice-based research--"Blue Highways" on the NIH roadmap. , 2007, JAMA.

[14]  N. Schork Personalized medicine: Time for one-person trials , 2015, Nature.

[15]  V. Rauh,et al.  Research Review: Environmental exposures, neurodevelopment, and child mental health - new paradigms for the study of brain and behavioral effects. , 2016, Journal of child psychology and psychiatry, and allied disciplines.

[16]  G. Elmer,et al.  Engaging Research Domain Criteria (RDoC): Neurocircuitry in Search of Meaning. , 2016, Schizophrenia bulletin.

[17]  R. Iniesta,et al.  Machine learning, statistical learning and the future of biological research in psychiatry , 2016, Psychological Medicine.

[18]  T. Seeman,et al.  Modeling Multisystem Physiological Dysregulation , 2016, Psychosomatic medicine.

[19]  E. Fries 5. Hypocortisolemic Disorders , 2008 .

[20]  B. McEwen,et al.  Lifetime experiences, the brain and personalized medicine: an integrative perspective. , 2013, Metabolism: Clinical and Experimental.

[21]  A. Jablensky,et al.  Revisiting the suitability of antisaccade performance as an endophenotype in schizophrenia , 2011, Brain and Cognition.

[22]  A. Steptoe Handbook of Behavioral Medicine , 2010 .

[23]  John P A Ioannidis,et al.  The Reproducibility Wars: Successful, Unsuccessful, Uninterpretable, Exact, Conceptual, Triangulated, Contested Replication. , 2017, Clinical chemistry.

[24]  Albert A. Rizzo,et al.  Allostatic load as a complex clinical construct: A case-based computational modeling approach , 2015, Complex..

[25]  R. Joober On the simple and the complex in psychiatry, with reference to DSM 5 and research domain criteria. , 2013, Journal of psychiatry & neuroscience : JPN.

[26]  R. Dantzer Neuroimmune Interactions: From the Brain to the Immune System and Vice Versa. , 2018, Physiological reviews.

[27]  Bruce Mcewen,et al.  Stress, Adaptation, and Disease: Allostasis and Allostatic Load , 1998, Annals of the New York Academy of Sciences.

[28]  M. Chakravarty,et al.  Dynamic endophenotypes and longitudinal trajectories: capturing changing aspects of development in early psychosis. , 2016, Journal of psychiatry & neuroscience : JPN.

[29]  Thomas R. Insel,et al.  Endophenotypes: Bridging Genomic Complexity and Disorder Heterogeneity , 2009, Biological Psychiatry.

[30]  Carla Nasca,et al.  Mechanisms of stress in the brain , 2015, Nature Neuroscience.

[31]  M C Neale,et al.  Endophenotype: a conceptual analysis , 2010, Molecular Psychiatry.

[32]  T. White,et al.  Brain connectivity and gyrification as endophenotypes for schizophrenia: weight of the evidence. , 2012, Current topics in medicinal chemistry.

[33]  G. Lewis,et al.  Detection of depression and anxiety in primary care: follow up study , 2002, BMJ : British Medical Journal.

[34]  F. Collins,et al.  A new initiative on precision medicine. , 2015, The New England journal of medicine.

[35]  D. Borsboom A network theory of mental disorders , 2017, World psychiatry : official journal of the World Psychiatric Association.

[36]  Albert Y Xue,et al.  A support vector machine model provides an accurate transcript-level-based diagnostic for major depressive disorder , 2016, Translational Psychiatry.

[37]  I. Gottesman,et al.  Human development: biological and genetic processes. , 2005, Annual review of psychology.

[38]  J. Wakefield Wittgenstein's nightmare: why the RDoC grid needs a conceptual dimension , 2014, World psychiatry : official journal of the World Psychiatric Association.

[39]  J. Panksepp Emotional endophenotypes in evolutionary psychiatry , 2006, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[40]  J. Ioannidis Acknowledging and Overcoming Nonreproducibility in Basic and Preclinical Research. , 2017, JAMA.

[41]  B. John,et al.  Chromosome variability and geographic distribution in insects. , 1966, Science.

[42]  A. Baum,et al.  The Handbook of Stress Science: Biology, Psychology, and Health , 2010 .

[43]  Kenneth D. Mandl,et al.  The Evolution of Patient Diagnosis: From Art to Digital Data-Driven Science , 2017, JAMA.

[44]  M. Munafo,et al.  The endophenotype concept in psychiatric genetics , 2006, Psychological Medicine.

[45]  D. Hellhammer,et al.  7. Serotonergic and Parasympathetic Disorders , 2008 .

[46]  Daniel R Weinberger,et al.  Intermediate phenotypes in psychiatric disorders. , 2011, Current opinion in genetics & development.

[47]  Leon Eisenberg,et al.  Bridging Disciplines in the Brain, Behavioral, and Clinical Sciences , 2000 .

[48]  A. Prange,et al.  Use of TSH response to TRH as an independent variable. , 1983, The American journal of psychiatry.

[49]  Issa J Dahabreh,et al.  Can the learning health care system be educated with observational data? , 2014, JAMA.

[50]  C. Tacket,et al.  Translation of clinical research into practice: defining the clinician scientist. , 2009, Family medicine.

[51]  B. McEwen Neurobiological and Systemic Effects of Chronic Stress , 2017, Chronic stress.

[52]  Hyejung Won,et al.  The road to precision psychiatry: translating genetics into disease mechanisms , 2016, Nature Neuroscience.

[53]  W. Glannon Research domain criteria: a final paradigm for psychiatry? , 2015, Front. Hum. Neurosci..

[54]  R. Murison,et al.  Pavlovian conditioning of corticotropin-releasing factor-induced increase of blood pressure and corticosterone secretion in the rat. , 1992, Acta physiologica Scandinavica.

[55]  Robert L Phillips,et al.  Family medicine, the NIH, and the medical-research roadmap: perspectives from inside the NIH. , 2009, Family medicine.

[56]  B. McEwen,et al.  Insulin resistance—a missing link no more , 2016, Molecular Psychiatry.

[57]  I. Gottesman,et al.  The endophenotype concept in psychiatry: etymology and strategic intentions. , 2003, The American journal of psychiatry.

[58]  Francesco Vallania,et al.  Methods to increase reproducibility in differential gene expression via meta-analysis , 2016, Nucleic acids research.

[59]  D. Dorr,et al.  Can Personalized Care Planning Improve Primary Care? , 2017, JAMA.

[60]  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.

[61]  D. Hellhammer 3. Principles of the Crosstalk between Brain and Body – Glandotropy, Ergotropy, and Trophotropy , 2008 .

[62]  E. Walker,et al.  The neural diathesis-stress model of schizophrenia revisited: An update on recent findings considering illness stage and neurobiological and methodological complexities , 2017, Neuroscience & Biobehavioral Reviews.

[63]  R. Phillips,et al.  Off the Roadmap? Family Medicine’s Grant Funding and Committee Representation at NIH , 2008, The Annals of Family Medicine.

[64]  Raquel E Gur,et al.  The Consortium on the Genetics of Schizophrenia: neurocognitive endophenotypes. , 2006, Schizophrenia bulletin.

[65]  C. Nemeroff,et al.  Personalized medicine: Prediction of disease vulnerability in mood disorders , 2016, Neuroscience Letters.

[66]  Brigitte Rockstroh,et al.  Endophenotypes in psychopathology research: where do we stand? , 2013, Annual review of clinical psychology.

[67]  J. Gray,et al.  The psychology of fear and stress , 1971 .

[68]  D. Hellhammer,et al.  Neuropattern: A new translational tool to detect and treat stress pathology I. Strategical consideration , 2012, Stress.

[69]  Bruce N Cuthbert,et al.  The NIMH Research Domain Criteria Initiative: Background, Issues, and Pragmatics. , 2016, Psychophysiology.

[70]  S. Goodman,et al.  Using Design Thinking to Differentiate Useful From Misleading Evidence in Observational Research. , 2017, JAMA.

[71]  T. Lidz,et al.  Adolf Meyer and the development of American psychiatry. , 1966, The American journal of psychiatry.

[72]  J. Ioannidis,et al.  What Happens When Underperforming Big Ideas in Research Become Entrenched? , 2016, JAMA.

[73]  D. Hellhammer,et al.  6. Noradrenergic and Sympathetic Disorders , 2008 .

[74]  M. Buchsbaum,et al.  Psychopathology: biological approaches. , 1983, Annual review of psychology.

[75]  B. Kudielka,et al.  Salivary cortisol as a biomarker in stress research , 2009, Psychoneuroendocrinology.

[76]  Derek C Angus,et al.  Fusing Randomized Trials With Big Data: The Key to Self-learning Health Care Systems? , 2015, JAMA.

[77]  Mario Maj,et al.  The need for a conceptual framework in psychiatry acknowledging complexity while avoiding defeatism , 2016, World psychiatry : official journal of the World Psychiatric Association.

[78]  Fiona Godlee,et al.  Data Sharing Statements for Clinical Trials: A Requirement of the International Committee of Medical Journal Editors , 2017, Ethiopian journal of health sciences.

[79]  B. Turetsky,et al.  Neurophysiological endophenotypes of schizophrenia: the viability of selected candidate measures. , 2006, Schizophrenia bulletin.

[80]  R. Tuomela Explanation and Understanding of Human Behavior , 1976 .

[81]  R. Kahn,et al.  Cortisol stress reactivity across psychiatric disorders: A systematic review and meta-analysis , 2017, Psychoneuroendocrinology.

[82]  J. Loscalzo,et al.  Precision Psychiatry Meets Network Medicine: Network Psychiatry , 2017, JAMA psychiatry.

[83]  Lutz Bornmann,et al.  Growth rates of modern science: A bibliometric analysis based on the number of publications and cited references , 2014, J. Assoc. Inf. Sci. Technol..

[84]  Ranga R. Krishnan,et al.  A knowledge network for a dynamic taxonomy of psychiatric disease , 2015, Dialogues in clinical neuroscience.

[85]  D. Longo,et al.  Precision medicine--personalized, problematic, and promising. , 2015, The New England journal of medicine.

[86]  S. Zipfel,et al.  Screening psychischer Störungen mit dem "Gesundheitsfragebogen für Patienten (PHQ-D)" Ergebnisse der deutschen Validierungsstudie , 2004 .

[87]  Muin J Khoury,et al.  Convergence of Implementation Science, Precision Medicine, and the Learning Health Care System: A New Model for Biomedical Research. , 2016, JAMA.

[88]  M. Tonelli,et al.  To realize the goals of precision medicine , the hierarchy of evidence pyramidmust yield to amore horizontal conception ofmedical knowledge , 2017 .

[89]  Bartha M Knoppers,et al.  Data Sharing - Is the Juice Worth the Squeeze? , 2016, The New England journal of medicine.

[90]  J. Pruessner,et al.  Reflections on the interaction of psychogenic stress systems in humans: The stress coherence/compensation model , 2013, Psychoneuroendocrinology.

[91]  B. Cuthbert Translating intermediate phenotypes to psychopathology: the NIMH Research Domain Criteria. , 2014, Psychophysiology.

[92]  C. Patrick,et al.  RDoC: Translating promise into progress. , 2016, Psychophysiology.

[93]  Scott O Lilienfeld,et al.  Clashing Diagnostic Approaches: DSM-ICD Versus RDoC. , 2016, Annual review of clinical psychology.

[94]  W. Mandel,et al.  Calcium for myocardial depression from verapamil. , 1982, The New England journal of medicine.

[95]  D. Hellhammer,et al.  Neuropattern: A new translational tool to detect and treat stress pathology. II. The Teltow study , 2012, Stress.

[96]  J. Shields,et al.  Genetic Theorizing and Schizophrenia , 1973, British Journal of Psychiatry.

[97]  Daniel S Pine,et al.  Biomarkers With a Mechanistic Focus. , 2015, JAMA psychiatry.

[98]  Claes Wahlestedt,et al.  Personalized medicine in psychiatry: problems and promises , 2013, BMC Medicine.

[99]  M. Maj Narrowing the gap between ICD/DSM and RDoC constructs: possible steps and caveats , 2016, World psychiatry : official journal of the World Psychiatric Association.

[100]  Patrick F Sullivan,et al.  The Psychiatric GWAS Consortium: Big Science Comes to Psychiatry , 2010, Neuron.

[101]  Nicolas Rohleder,et al.  Stimulation of Systemic Low-Grade Inflammation by Psychosocial Stress , 2014, Psychosomatic medicine.

[102]  Andrew H. Miller,et al.  Psychoneuroimmunology Meets Neuropsychopharmacology: Translational Implications of the Impact of Inflammation on Behavior , 2012, Neuropsychopharmacology.

[103]  E. Zorrilla,et al.  Don’t stress about CRF: assessing the translational failures of CRF1antagonists , 2017, Psychopharmacology.

[104]  Catherine Milne,et al.  Understanding and Explanation , 2011 .

[105]  T. Jay,et al.  The neurobiological properties of Tianeptine (Stablon): from monoamine hypothesis to glutamatergic modulation , 2009, Molecular Psychiatry.

[106]  B. Carroll Clinical science and biomarkers: against RDoC , 2015, Acta psychiatrica Scandinavica.

[107]  G. Chrousos,et al.  Glucocorticoid Signaling in the Cell , 2009, Annals of the New York Academy of Sciences.

[108]  M. Keshavan,et al.  The journey from RDC/DSM diagnoses toward RDoC dimensions , 2014, World psychiatry : official journal of the World Psychiatric Association.

[109]  B. McEwen Epigenetic Interactions and the Brain-Body Communication , 2016, Psychotherapy and Psychosomatics.

[110]  T. Insel Digital Phenotyping: Technology for a New Science of Behavior. , 2017, JAMA.