The three-hit concept of vulnerability and resilience: toward understanding adaptation to early-life adversity outcome

Daskalakis, Nikolaos P.; Bagot, Rosemary C.; Parker, Karen J.; Vinkers, Christiaan H.; de Kloet, E.R.

doi:10.1016/j.psyneuen.2013.06.008

Cited by 582Stress Responses and CortisolResilience and Mental HealthChild Abuse and Trauma

The three-hit concept of vulnerability and resilience: toward understanding adaptation to early-life adversity outcome

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Daskalakis, Nikolaos P., Bagot, Rosemary C., Parker, Karen J., Vinkers, Christiaan H., de Kloet, E.R.·2013·Psychoneuroendocrinology

DOI 10.1016/j.psyneuen.2013.06.008PMC PMC3773020

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Abstract

Stressful experiences during early-life can modulate the genetic programming of specific brain circuits underlying emotional and cognitive aspects of behavioral adaptation to stressful experiences later in life. Although this programming effect exerted by experience-related factors is an important determinant of mental health, its outcome depends on cognitive inputs and hence the valence an individual assigns to a given environmental context. From this perspective we will highlight, with studies in rodents, non-human primates and humans, the three-hit concept of vulnerability and resilience to stress-related mental disorders, which is based on gene-environment interactions during critical phases of perinatal and juvenile brain development. The three-hit (i.e., hit-1: genetic predisposition, hit-2: early-life environment, and hit-3: later-life environment) concept accommodates the cumulative stress hypothesis stating that in a given context vulnerability is enhanced when failure to cope with adversity accumulates. Alternatively, the concept also points to the individual’s predictive adaptive capacity, which underlies the stress inoculation and match/mismatch hypotheses. The latter hypotheses propose that the experience of relatively mild early-life adversity prepares for the future and promotes resilience to similar challenges in later-life; when a mismatch occurs between early and later-life experience, coping is compromised and vulnerability is enhanced. The three-hit concept is fundamental for understanding how individuals can either be prepared for coping with life to come and remain resilient or are unable to do so and succumb to a stress-related mental disorder, under seemingly identical circumstances.

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The shift from a hyper- to a hypo-responsive stress axis in the first 5 years of life may represent a particularly crucial stress-sensitive period, especially in the absence of a nurturing caregiver.
“Accordingly, this shift from a hyper- to a hypo-responsive stress axis in the first 5 years in life may be represent an particularly crucial stress-sensitive period, especially in the absence of a nurturing caregiver (104).”
From Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation (2019) · cites this paper as [104]
Section 2.1 describes a hypo-responsive period in human infants during postnatal months 6–12 and says caregiver quality can attenuate stress-induced cortisol secretion. It does not describe a shift from hyper- to hypo-responsiveness across the first five years of human life, so the claimed timing and transition are unsupported. (LLM, conf=0.86)
Experimental — accuracy not yet measured
After an initial hyper-responsive period, the HPA axis may later transition into a stress hypo-responsive period with lower basal cortisol levels and blunted stress-induced cortisol reactivity.
“After an initial hyper-responsive period, the HPA axis may later transition into a stress hypo-responsive period (SHRP) with lower basal cortisol levels and blunted stress-induced cortisol reactivity (101, 104–106).”
From Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation (2019) · cites this paper as [104]
Section 2.1 (page unavailable) describes a stress hypo-responsive developmental period with attenuated CORT responses, including a comparable period in human infants. It does not describe a general transition from an initial hyper-responsive period to lower basal cortisol and blunted stress reactivity; its account of repeated maternal separation says basal CORT remains low while pups retain the ability to respond to stress. (LLM, conf=0.85)
Experimental — accuracy not yet measured
The classical vulnerability-stress model and conceptually similar approaches such as the 'allostatic load', 'double-hit' or 'three-hit' hypotheses predominantly focus on risk-increasing factors that, assuming a cumulative effect, will lead to manifestation of disease.
“The classical vulnerabilitystress model of mental disorders, arguably one of the most influential models of disorder development, as well as conceptually similar approaches such as the”
From The applied implications of epigenetics in anxiety, affective and stress-related disorders - A review and synthesis on psychosocial stress, psychotherapy and prevention (2020) · cites this paper as Daskalakis, Bagot, Parker, Vinkers, & de Kloet, 2013
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
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Enduring changes in the transcriptome may facilitate the response to early developmental challenges and play a central role in the long-term (and sometimes transgenerational) biological trajectories of stress-related disease through programming effects for stress reactivity after ELS/CT exposure.
“Taken together, enduring changes in the transcriptome may facilitate the response to early developmental challenges and thus play a central role in the long-term (and sometimes transgenerational) biological trajectories of stress-related disease through programming effects for stress reactivity after ELS/CT exposure (104, 413, 414).”
From Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation (2019) · cites this paper as [104]
Daskalakis et al. expanded this model suggesting a three-hit concept for vulnerability and resilience.
“Recently, Daskalakis et al. (104) have expanded this model suggesting a three-hit concept for vulnerability and resilience.”
From Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation (2019) · cites this paper as [104]

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“promoter in the adrenal and pituitary (Witzmann et al., 2012).”
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Trauma and PTSD in the WHO World Mental Health Surveys
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Modulation of the Hypothalamic-Pituitary-Adrenal Axis by Early Life Stress Exposure
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Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation
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“Taken together, enduring changes in the transcriptome may facilitate the response to early developmental challenges and thus play a central role in the long-term (and sometimes transgenerational) biological trajectories of stress-related disease through programming effects for stress reactivity after ELS/CT exposure (…”
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Early-life stress, HPA axis adaptation, and mechanisms contributing to later health outcomes
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STRESS EXPOSURE ACROSS THE LIFE SPAN CUMULATIVELY INCREASES DEPRESSION RISK AND IS MODERATED BY NEUROTICISM
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Early life stress in fathers improves behavioural flexibility in their offspring
Gapp, K., Soldado-Magraner, S., Álvarez-Sánchez, M., Bohacek, J., Vernaz, G., Shu, H., Franklin, T. B., Wolfer, D. P., & Mansuy, I. M. (2014) · Nature Communications · doi:10.1038/ncomms6466 · Cited by 170 · see citing works
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Early life epigenetic programming and transmission of stress‐induced traits in mammals: How and when can environmental factors influence traits and their transgenerational inheritance?
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Conceptualizing Puberty as a Window of Opportunity for Impacting Health and Well‐Being Across the Life Span
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Resilience
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Early Life Stress Effects on Glucocorticoid—BDNF Interplay in the Hippocampus
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Epigenetic programming of the neuroendocrine stress response by adult life stress
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Early life adversity: Lasting consequences for emotional learning
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The Microbiome-Gut-Brain Axis and Resilience to Developing Anxiety or Depression under Stress
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Epigenetic and Neurological Impairments Associated with Early Life Exposure to Persistent Organic Pollutants
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Resilience: A psychobiological construct for psychiatric disorders
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Functional urological disorders: a sensitized defence response in the bladder–gut–brain axis
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Early life stress and trauma: developmental neuroendocrine aspects of prolonged stress system dysregulation
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Glucocorticoids as regulatory signals during intrauterine development
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The intersection of gender and resilience
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Developmental origins of cardiovascular disease: Impact of early life stress in humans and rodents
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Resilience as Regulation of Developmental and Family Processes
MacPhee, D., Lunkenheimer, E. S., & Riggs, N. R. (2015) · Family Relations · doi:10.1111/fare.12100 · Cited by 117 · see citing works
Allostatic Load and Preterm Birth
Olson, D., Severson, E., Verstraeten, B. S. E., Ng, J. W. Y., McCreary, J., & Metz, G. A. S. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161226209 · Cited by 115 · see citing works
The longitudinal influences of adverse childhood experiences and positive childhood experiences at family, school, and neighborhood on adolescent depression and anxiety
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Mancini, G. F., & Campolongo, P. (2026) · IRIS Research product catalog (Sapienza University of Rome)

Authors: Daskalakis, N. P., Bagot, R. C., Parker, K. J., Vinkers, C. H., & de Kloet, E. R.
Affiliations: Leiden University (NL)
Douglas Mental Health University Institute (CA)
Stanford Medicine (US)
Utrecht University (NL)
Corresponding author: Daskalakis, Nikolaos P.
ORCID: Daskalakis, Nikolaos P.
Bagot, Rosemary C.
Parker, Karen J.
Vinkers, Christiaan H.
Venue: Psychoneuroendocrinology
Publisher: Elsevier BV
Published: 2013-09
Volume: 38
Issue: 9
Pages: 1858-1873
ISSN: 0306-4530 (ISSN-L)
DOI: 10.1016/j.psyneuen.2013.06.008
PMC: PMC3773020
OpenAlex: W2150581383
Semantic Scholar: 803eaa44fe6fdff1f9eccd7886ac5a72114899e7
Cited by: 579
References: 202
Citations by year: 2026: 34 · 2025: 29 · 2024: 62 · 2023: 49 · 2022: 52 · 2021: 58 · 2020: 54 · 2019: 50 · 2018: 45 · 2017: 44 · 2016: 41 · 2015: 34 · 2014: 22 · 2013: 4
FWCI: 14.94
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Psychoneuroendocrinology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Leiden Repository (Leiden University) (submittedVersion)
Funders: Dutch Top-Institute Pharma T5-209
NIH-R01HD67175
Royal Netherlands Academy for Sciences
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Clinical Psychology › Resilience and Mental Health
Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
Keywords: vulnerability and resilience, childhood adversity, stress-related disorders, gene-environment interaction, match-mismatch hypothesis, coping
MeSH terms: Adaptation, Psychological, Animals, Avoidance Learning, Disease Models, Animal, Female, Glucocorticoids, Humans, Hypothalamo-Hypophyseal System, Maternal Behavior, Maternal Deprivation, Models, Neurological, Models, Psychological, Neuronal Plasticity, Pituitary-Adrenal System, Pregnancy, Prenatal Exposure Delayed Effects, Primates, Stress Disorders, Post-Traumatic, Stress, Psychological, Genetic Predisposition to Disease, Vulnerable Populations, Epigenesis, Genetic, Rats, Resilience, Psychological, Gene-Environment Interaction

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The three-hit concept of vulnerability and resilience: toward understanding adaptation to early-life adversity outcome

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