Association between Hpa Axis Functioning and Mental Health in Maltreated Children and Adolescents: A Systematic Literature Review
Abstract
:1. Introduction
Connection with the Hypothalamo–Hypophyseal System
2. Materials and Methods
2.1. Search Strategy
2.2. Eligibility Criteria
2.3. Data Collection
3. Results
3.1. Search Results
3.2. Characteristics of the Studies
3.2.1. Populations Studied
3.2.2. Design and Methodology of the Studies
3.2.3. Maltreatment Assessment
- Maltreatment was investigated differently depending on the studies included: social service records, in most cases [27,29,42], mostly using the “maltreatment classification system” (MCS) [37,39,41,43]. In two studies, standardized questionnaires for the foster family were used: the studies that included children who had suffered early maltreatment [30] used these questionnaires, one of which was completed using the social services file [27]. Several studies used questionnaires designed for children: Childhood Trauma Questionnaire (CTQ) [34,35,38,40], Screen for Adolescent Violence Exposure (SAVE) [35], Adverse Childhood Experiences Scale (International Questionnaire) (ACE-IQ) [33], and Childhood Experiences of Violence Questionnaire (CEVQ) [38]. Finally, two other studies used Questionnaires for biological parents: The Early Trauma Inventory by Bremner (Bremner JD et al., 2000) [32], Unspecified Standardized Questionnaire [36], and one study also used, in addition to the child questionnaire, a prenatal stress questionnaire for the mother: the Prenatal Psychosocial Profile [33].
3.2.4. Psycho-Behavioral Assessment
- For categorical assessment, the Mini-International Neuropsychiatric Interview for Children and Adolescents (MINI kid), and the Schedule for Affective Disorders and Schizophrenia for school-aged children (K-SADS-E), both exploring child and adolescent psychiatric disorders (DSM IV), were used. For dimensional assessment, the Children’s Depression Inventory (CDI) (scale for assessing the severity of depressive symptoms), the Adolescent Personality Disorder (APD) (Personality Disorder Symptoms Rating Scale), the Impulsiveness Venturesomeness and Empathy (IVE) Questionnaire (Evaluation of empathy and impulsivity), and the Adolescent Delinquency Questionnaire (ADQ) scales were used. Five out of 15 studies used the TRF scale [36,37,39,41,43]; four studies used the CBCL scale [27,32,35,36] and three studies used the CDI [29,37,41].
- One study used, in addition to the TRF and the Dissociation Sub-scale, two cognitive assessment scales: California Verbal Learning Test for Children (CVLT-C) and Peabody Picture Vocabulary Test 3 (PPVT3): assessment of memory for verbal comprehension and learning [43]. Several studies used sub-scores or composite scores to more specifically assess interpersonal and social difficulties, better characterize emotional and behavioral problems (particularly fear and aggression) as well as symptomatology (internalizing or externalizing), and measure resilience capacities.
3.2.5. HPA Axis Functioning Assessment
- Eight studies measured spontaneous cortisol levels by taking saliva samples at different times of the day. In three studies, the aim was to measure the circadian rhythm of cortisol [27,30,42], with three samples taken per day, in the morning, at midday, and in the afternoon or at bedtime, following practical sampling instructions to avoid disturbing the salivary cortisol (e.g., no food or toothbrushing just before sampling). One study assessed morning cortisol only [43] and followed practical sampling instructions. One study assessed the reactivity of the hypothalamic–pituitary axis upon awakening [34], using the cortisol awakening response (CAR) protocol with the measurement of cortisol by salivary sampling (3 samples per day over 2 days: upon awakening, and after 30 min and 60 min). However, sampling instructions were not specified in this article. Finally, two studies assessed cortisol at two times of the day: at 09:00 a.m. and at 16:00 p.m. (this is not the circadian rhythm) [37,41], but these studies specified the sampling instructions. Finally, one study investigated the evolution of cortisol levels over time by taking a saliva sample at 16:00 p.m. once a week for 20 weeks [39].
3.3. Main Results
3.3.1. Relationship between Maltreatment and Psycho-Behavioral Disorders
3.3.2. Relationship between Maltreatment and the Hypothalamo–Hypophyseal System
3.3.3. Relationship between Psycho-Behavioral Disorders and Cortisol Levels
3.3.4. Relationship between Psycho-Behavioral Disorders, Cortisol Secretion and Maltreatment
4. Discussion
4.1. The Impact of Maltreatment on the Mental Health of Children and Adolescents
4.2. Cortisol Secretion in Maltreated Subjects
4.3. Associations between Cortisol Secretion and Psycho-Behavioral Disorders
4.4. Associations between Maltreatment, Activity of the Hypothalamo–Hypophyseal Axis, and Psycho-Behavioral Disorders
4.5. Limitations
5. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A
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Authors | Target Population | Subjects (Number, Age) | Control Group (Number, Age) | Maltreatment/Trauma | Cortisol Measurement | Psycho-Behavioral Assessment |
---|---|---|---|---|---|---|
Kuhlman et al. [32] | Subjects in a study of depression among young people | n = 121 Age 9–16 years Mean age: 12.77 (standard deviation 2.26) | None | Questionnaire “The Early Trauma Inventory” | Socially Evaluated Cold Pressor Task: Measurement of the reactivity to stress of the hypothalamic–pituitary axis | Child Behavior Checklist scale (CBCL) |
Timothy et al. [33] | Children of alcohol-dependent fathers | n = 50 (male gender only) Age 8–16 years Mean age: 11.3 years (Standard deviation 2.37) | n = 50 Of comparable age (p = 0.85) and education (p = 0.49) | Questionnaires “Adverse Childhood Experiences Scale” (ACE-IQ) and “Prenatal Psychosocial Profile” | Trier Social Stress Test (TSST) Measurement of reactivity to stress of the hypothalamic–pituitary axis | MINI-Kid, Strengths and Difficulties Questionnaire (SDQ) |
Kaess et al. [34] | General population, diagnosis of borderline personality disorder | n = 69, age 14–16 years, mean Age: 15.5 (Standard deviation 0.4) | None | Questionnaire Childhood Trauma Questionnaire (CTQ) | Measurement of the reactivity of the hypothalamo– pituitary axis on waking (cortisol test, 3 saliva samples/day over 2 days: on waking up, +30 min, +60 min), Instructions for sampling practice not specified | Adolescent Personality Disorder (APD) Scale |
Busso et al. [35] | Children from under-privileged backgrounds | n = 169 Mean Age: 14.9 (Standard deviation 1.4) | None | Questionnaires CTQ and « Screen for Adolescent Violence Exposure » (SAVE) | Trier Social Stress Test (TSST) Measurement of the reactivity to stress of the hypothalamic–pituitary axis, (cortisol/DHEA ratio) | CBCL |
Ouellet- Morin et al. [36] | Subjects in the longitudinal “E-Risk” study | n = 190 Age 12 years Group M: n = 64 | n = 126 | Standardised questionnaires for parents | Psychosocial Stress Test (PST): Measurement of the Reactivity of the hypothalamic–pituitary axis | CBCL Teachers’ Report Form (TRF), Composite scores for social, emotional and behavioral problems |
Cicchetti et al. [37] | Underprivileged backgrounds. M group in connection with social services. | n = 493 Age 7–13 Mean age: 10.08 (Standard deviation 1.87) Group M: n = 238 (which includes n = 51 in Group MP+ for maltreatment after the age of 5 years; and n = 187 in Group MP—for maltreatment after age of 5 years | n = 255 | Exploration of the social services file: scale of maltreatment using the “Maltreatment classification system” (MCS) | Saliva samples for cortisol tests: twice a day for 2 days at 9 am and 4 pm. Practical sampling instructions | Children Depression Inventory (CDI), TRF |
Puetz et al. [27] | Children in social care | n = 25 Age 8–14 years, mean age: 10.6 (Standard deviation 1.75) | n = 26, Mean age: 10.38 (Standard deviation 1.67), comparable in age (p = 0.66), IQ (p = 0.18) and socio-economic level (p = 0.19) | Exploration of social services files and questionnaires for foster families | Assessment of the cortisol circadian rhythm: Saliva samples 3 times/day for 2 days (30 min after getting up, 30 min before lunch and bedtime), Practical instructions for Sampling | CBCL, MINI kid, Impulsiveness venturesomeness Empathy (IVE) Questionnaire |
MacMillan et al. [38] | Children in social care | n = 67 Age: 12–16 years, Mean age: 14.18 (Standard deviation 1.15) Subjects female gender only | n = 25 Mean age 14 (Standard deviation 1.50) comparable in age and gender, but not in socio-economic status (p < 0.001) | Questionnaires CTQ and Childhood Experiences of violence Questionnaire (CEVQ) | Trier Social Stress Test (TSST) Measurement of reactivity to stress of the hypothalamic–pituitary axis | Schedule for affective disorders and schizophrenia for school aged children (K-SADS-E) |
Doom et al. [39] | Children in social care | n = 341 Age 5–13 years Group M: n = 187 Average age: 8.4 (Standard deviation 1.8) 3 sub-groups in group M recent, early maltreatment (RE), non-recent, early maltreatment (RE-) and recent, later maltreatment (RL) | n = 154 | Examination of the social services files: MCS maltreatment system and questionnaires to the families in the control group (maternal-child maltreatment interview) | Measurement of cortisol levels: 1 saliva sample at 4 pm once a week for 20 weeks. Instructions on sampling practices | TRF |
Cook et al. [40] | Subjects of a longitudinal study of underprivileged families | n = 175 Age 14.5–16 years Average age: 15.36 (Standard deviation 1.01) 2 sub-groups “low maltreatment” for CTQ Score < 32 and “high maltreatment” for CTQ >32 (49% vs. 51%) | None | Questionnaire CTQ | Trier Social Stress Test (TSST): Measurement of the reactivity to stress of the hypothalamic–pituitary axis. | Behavior Assessment Scale for Children Self-report on personality (BASC-SRP), Scores for interpersonal competence and anger management |
Cicchetti et al. [41] | Disadvantaged backgrounds. M group in connection with social services | n = 677 Age 6–12 years, Mean age: 9.54 (Standard deviation 2.26) Group M: n = 347 | n = 330 | Exploring the social services files: scale of MCS maltreatment | Saliva samples twice a day for cortisol tests: at 09:00 a.m. and 16:00 p.m. Practical instructions for sampling | CDI, TRF, Resilience Score |
Murray-Close et al. [42] | Disadvantaged backgrounds. M group in connection with social services | n = 418 Age 6–12 years Group M: n = 219 | n = 199 | Exploration of social services files | Assessment of the cortisol circadian rhythm: Saliva samples 3 times a day: at 09:00 a.m. in the morning, 12:30 p.m. before lunch and 16:00 p.m. Practical instructions for sampling | Scores for physical and relational aggression |
Kočovská et al [30] | Early maltreatment and diagnosis of attachment disorder | n = 34 Age 5–12 years Average age: 9.4 (standard deviation 1.8) Average age at adoption: 62.9 months (Standard deviation 25.3) | n = 32 Average age: 8.7 (Standard deviation 2.4) | Questionnaire standardized for the foster family at the beginning of the placement | Assessment of cortisol circadian rhythm: Saliva samples 3 times a day: 30 min after getting up, before lunch and before bedtime. Practical instructions forsampling | Strengths anddifficulties Questionnaire (SDQ), Relationship Problems Questionnaire (RPQ) Total difficulties score |
Cicchetti et al. [43] | Disadvantaged backgrounds. M group in connection with social services | n = 317 Age 6–13 years, Mean age: 9.17 (Standard deviation 2.43) Group M: n = 143, with 2 sub-groups: physical/emotional (PEN) negligence physical/sexual (PSA) abuse | n = 174 | Exploration of Social services files: scale of MCS maltreatment | Morning cortisol levels: 1 sample at 09:00 a.m. Practical Instructions for sampling | TRF False recognition and discrimination scores, dissociation sub-scale |
Negriff et al. [29] | Children in social care | n = 303 Age 9–13 years, Mean age: 10.84 (Standard deviation 1.15) | n = 151 Mean age: 11.11 (Standard deviation 1.15) | Exploration of social services files | Trier Social Stress Test (TSST) Measurement of the Reactivity of the axis, Cortisol testing by saliva samples | Adolescent Delinquency Questionnaire (ADQ), CDI |
Authors | Links between Maltreatment and Psycho-Behavioral Disorders | Links between Maltreatment and Cortisol | Links between Disturbances and Cortisol | Links: Cortisol-Disorders-Maltreatment |
---|---|---|---|---|
Kuhlman et al. [32] | Positive correlation between emotional abuse and IS and unintentional trauma and IS (p < 0.05 for both) | Not stated | Negative correlation of reactivity of the hypothalamic–pituitary axis (slope at peak) with IS and ES (p < 0.01 for both) | Negative correlation of hypothalamic–pituitary axis reactivity/physical abuse interaction with IS (p = 0.007), and ES (p = 0.013), Positive correlation of axis reactivity/emotional abuse interaction with IS (p = 0.001), and ES (p = 0.005) Positive correlation of axis reactivity/unintentional trauma interaction with IS (p = 0.017) and ES (p = 0.027) |
Timothy et al. [33] | Significant difference between the 2 groups in ES only (increase in group M (p = 0.003) | Significant decrease in reactivity in group M (p < 0.01) | not stated | Negative correlation between axis reactivity and total SDQ score in group M only (p < 0.05) |
Kaess et al. [34] | BPD and CTQ score correlation (p < 0.001) | Negative correlation between CTQ score and cortisol reactivity on waking up (p = 0.047) (However, when differentiating by gender: negative correlation for girls and positive correlation for boys). | No correlation between BPD score and Cortisol reactivity (p = 0.537) | Interaction between CTQ score and BPD score correlated with decreased cortisol reactivity on waking in girls only (p = 0.045) |
Busso et al. [35] | Exposure to violence positively correlates with IS and ES scores (p < 0.001 for both). | Exposure to violence negatively correlated with hypothalamo–hypophyseal axis reactivity (p = 0.021) | Negative correlation of reactivity of the hypothalamic–pituitary axis with ES (p = 0.008) (not with IS) | Association between exposure to violence and ES mediated by the reactivity of the hypothalamo–hypophyseal axis (significant indirect effect with bootstrapping) |
Ouellet- Morin et al. [36] | Significant difference between the 2 groups in terms of social (p < 0.001), emotional (p < 0.01), behavioral (p < 0.05) problems (Increase in group M) | Significant decrease in reactivity of the hypothalamo–hypophyseal axis in group M (p < 0.05) | Not stated | Significant association between decreased reactivity of the hypothalamo–hypophyseal axis and social (p < 0.001) and behavioral (p < 0.01) (but not emotional) problem scoresin group M only |
Cicchetti et al. [37] | not stated | not stated | not stated | Children in the MP+ group with high IS/CDI scores have a morning-afternoon cortisol slope which is shallower in comparison to groups C and MP (p = 0.008) |
Puetz et al. [27] | No significant difference in prevalence (MINI kid) between the 2 groups (p = 0.34) CBCL (p < 0.001) and the impulsivity scores part of the IVE (p = 0.005) are increased in group M | Morning–noon slope of the cortisol curve shallower in group M (p = 0.034) Morning cortisol significantly lower in group M (p = 0.04) (no difference in the other 2 times of day) | No correlation | Negative correlation between morning cortisol level and CBCL score in group M only (p = 0.007), No correlation between cortisol slope and CBCL score in either group. |
MacMillan et al. [38] | MDD and PTSD prevalence significantly higher in group M (p < 0.01 for both) | Significant decrease in reactivity of the hypothalamo–hypophyseal axis in group M (p < 0.001) | Not stated | No significant difference in the reactivity of the hypothalamo–hypophyseal axis between subjects with MDE/PTSD and the healthy subjects in the M group. (MDE/PTSD frequency 0% in group C so no comparison possible with this group) |
Doom et al. [39] | Total TRF (p < 0.001), ES (p < 0.001) and IS (p < 0.01) scores higher in group M | Cortisol variability over time is significantly greater in group M (p < 0.05) Significant difference in cortisol variability between the 3 sub-groups RE, RE- and RL (p < 0.05). No difference observed between the sub-groups with different severity of maltreatment | Correlation between TRF score and variability of the level of cortisol (p < 0.05) | No correlation between the TRF score and the interaction between cortisol variability and maltreatment (p = 0.43) |
Cook et al. [40] | Maltreatment positively correlated with anger control score and negatively correlated with interpersonal competence (p < 0.01 for both) | No correlation between the reactivity of the hypothalamo–hypophyseal axis and the maltreatment score | No correlation between axis reactivity and anger control and interpersonal competence scores | Positive correlation between axis reactivity with anger control score in the high maltreatment group (p < 0.01) and negative correlation in the low maltreatment group (p = 0.02) |
Cicchetti et al. [41] | Resilience score significantly lower in group M (p < 0.001) | No significant difference between the 2 groups but correlation between the maltreatment score and the morning cortisol rate (p 0.02) | Negative correlation between resilience score and morning cortisol level only in group C (p = 0.05) | In the physical abuse sub-group, and in the presence of a high level of morning cortisol, resilience score significantly higher than in group C (p = 0.001) or in sexual abuse sub-group (p = 0.021) |
Murray-Close et al. [42] | Not stated | No correlation between maltreatment and cortisol rate/rhythm | Positive correlation between physical aggression score and the rate/decline in morning cortisol Negative correlation between relational aggression score and rate/ decline in morning cortisol | No correlation (association between aggression score and cortisol is stronger in Group C than in Group M) |
Kočovská et al. [30] | Higher Total Difficulty Score and RPQ score in Group M (p < 0.0001 for both) | Similar circadian rhythm between the two groups but lower morning cortisol in group M (p = 0.047) | No correlation | No correlation |
Cicchetti et al. [43] | Higher dissociation score in group M (p < 0.001) | No significant difference in morning cortisol levels between the 2 groups | Correlation between discrimination score and cortisol rate (p = 0.04) | NPE sub-group only: subjects with low cortisol levels had higher false recognition scores (p < 0.001) and a lower discrimination score (p < 0.001) compared with subjects with higher cortisol levels. No correlation shown with subscale dissociation or TRF |
Negriff et al. [29] | Not stated | Significant difference in the reactivity of the hypothalamic–pituitary axis between the 2 groups, for the boys only (p < 0.01) | No correlation | Not stated |
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Leroux, P.-A.; Dissaux, N.; Le Reste, J.Y.; Bronsard, G.; Lavenne-Collot, N. Association between Hpa Axis Functioning and Mental Health in Maltreated Children and Adolescents: A Systematic Literature Review. Children 2023, 10, 1344. https://doi.org/10.3390/children10081344
Leroux P-A, Dissaux N, Le Reste JY, Bronsard G, Lavenne-Collot N. Association between Hpa Axis Functioning and Mental Health in Maltreated Children and Adolescents: A Systematic Literature Review. Children. 2023; 10(8):1344. https://doi.org/10.3390/children10081344
Chicago/Turabian StyleLeroux, Pierre-Antoine, Nolwenn Dissaux, Jean Yves Le Reste, Guillaume Bronsard, and Nathalie Lavenne-Collot. 2023. "Association between Hpa Axis Functioning and Mental Health in Maltreated Children and Adolescents: A Systematic Literature Review" Children 10, no. 8: 1344. https://doi.org/10.3390/children10081344