The authors have declared that no competing interests exist.
Mothers with a history of childhood maltreatment (CM) are likely to transmit their own experiences to the next generation. This is highly influenced by the quality of maternal behavior that enables to buffer infant’s hypothalamic-pituitary-adrenal (HPA) axis response to stress. From a transgenerational perspective the research question is, if infant’s cortisol stress response is influenced by maternal CM experiences or rather by the behavioral pathways during the first year of life.
53 mother-child-dyads were measured at 12 months of infant’s age in a laboratory visit assessing the maternal quality of interactive behavior using the Atypical Maternal Behavior Instrument for Assessment and Classification (AMBIANCE) measured during the strange situation procedure (SSP). Maltreatment experiences were assessed using the childhood trauma questionnaire (CTQ). Salivary cortisol of mother and infant were collected prior to and directly, 15 and 30 minutes after the SSP.
Infants of disruptive mothers showed a significant increase in cortisol (F (3; 147) = 2.897, p= 0.048) after the SSP compared to infants of mothers with sensitive caregiving. Maternal CM did not influence the infant’s cortisol stress response due to the SSP. However maternal cortisol response was altered by trend due to CM (F (1.392; 71.008) = 3.157, p= 0.066).
Our data indicate that infant’s cortisol stress reactivity is influenced by the quality of maternal behavior and not by the transgenerational transmission of maternal CM experiences per se. These findings implicate that helping mothers to improve their caregiving behavior may help to improve stress-reactivity of their infant.
Childhood maltreatment (CM) is considered as a significant risk factor for detrimental development, in particular when it occurs early in life
Dysregulation of the hypothalamic-pituitary-adrenal (HPA) axis has been widely shown in the context of CM. The HPA axis, considered as the body’s major glandotrop stress system, is associated with increased vulnerability to psychological and physical diseases
Specifically, the stress of experiencing CM has been linked to HPA dysregulation during the period of maltreatment as well as until adulthood
Recently, a growing research interest has been focused on the biological correlates of trans-generational transmission of CM showing that maternal child abuse results in disturbances in the HPA axis in their offspring. Brand and colleagues (2010) detected that children of mothers with CM showed lower baseline cortisol compared to children of mothers without CM. Additionally, children of mothers of a combination of both, a history of early maternal abuse and comorbid post-traumatic stress disorder, were associated with greater increases in child’s cortisol levels
The transmission of HPA axis dysregulation due to CM into the next generation was confirmed by Yehuda and colleagues (2005) who reported, that offspring of mothers with traumatic experiences in adulthood and PTSD showed significantly lower cortisol levels in saliva and blood compared to a control group
In childhood sensitive, warm and responsive caregiving plays an equivalent role in successful child’s behavioral and physiological regulation outcomes
TRANS-GEN is an interdisciplinary study consortium investigating in a prospective approach the pathways leading to resilience or vulnerability in the transgenerational transmission of childhood maltreatment (CM) by focusing psychological, biological and social factors.
The study was funded by the Federal Ministry of Education and Research and was approved by the Ethics Committee of Ulm University. After recruiting in the maternity unit of the Ulm University Hospital all mother-infant dyads were followed up twice: 3 months (t1) and 12 months (t2) after birth.
Since October 2013, 533 mother-infant-dyads were being recruited in the women’s hospital of the University Hospital of Ulm 1-6 days after parturition and were willing to complete the screening interview (t0). Inclusion criteria were age >18, over 37 weeks of pregnancy, sufficient knowledge of the German language, no complications during parturition or health problems of mother and/or infant as well as no current drug consumption or a history of severe psychiatric disorders or current infections. 240 mother-infant-dyads could be invited for a follow-up 3 months (t1) after birth in both laboratory as well as in home visit and 158 mother-infant-dyads participated in a further laboratory and home visit around 12 months of infant’s age (t2).
All mother-child-dyads were asked to collect salvia of 4 measurement points. The sample for the following analyses included 53 mother-infant-dyads. Missing data sets were due to the lack of agreement for collecting biological samples of 1 cases of mothers-child-dyads. In addition, 104 of mothers´ and 106 of infant´s collected salvia had no or insufficient amount of saliva for each data point, before (baseline before SSP), directly after (+1 min.) 15 minutes (+15 min.) and 30 minutes (+30 min.) the SSP. For final analysis, we included only mothers and their infants with a complete data set of 4 measurements. Cortisol levels of two infants could not be analyzed due to low amount of saliva. Therefore, we considered complete data sets of 53 mothers and 51 infants for final analyses (complete data sets means no missing of any of each 4 measurement points).
Mothers’ age at time of measurement (t2) was between 21 and 43 years (mean 33.72 years (SD 4.47 years)). Maternal body mass index (BMI) was between 17.26 and 31.83 (mean 24.35 (SD 3.82). 79.2% of the mothers reported to be married or living in a partnership and 88.7% of all mothers had German citizenship. Mother’s level of education at t2 in comparison to the educational background of the German population showed, that 56.6% had a grammar school degree, 11.3% a secondary school degree, 22.6% a basic secondary school degree and 7.5 % no school diploma. Furthermore, 20.8% of the mothers had medical risk factors e.g. chronic disease, high blood pressure or allergies. 30 male and 21 female infants were investigated in laboratory visit. All mother-infant-dyads were invited around 12 months of infant´s age (12.0 ± 0.1 months) (mean 12.43 years (SD 0.80 years)) (
Mothers were screened for CM using the CTQ
All mother infant-dyads were invited for a laboratory visit at 12 months of infant’s age (t2). Due to circadian rhythm of cortisol levels, all mother-child-dyads were assessed from 10.00 am to 1.00 pm. After a short introduction explaining the procedure of the investigation, mothers and infants were asked to have a resting phase of 15-20 minutes before sampling of the first saliva probes (baseline before SSP) prior to the beginning of the SSP. Further saliva samples were collected directly (+1 min. after SSP), 15 minutes (+15 min. after SSP) and 30 minutes (+30 min. after SSP) after the SSP while mothers were asked to play with their infant and relax by using toys. The implementation of the SSP was based on the standardized SSP protocol including 7: (e1) mother and infant were alone in the room with the infant exploring the room and the mother sitting on a chair, (e2) first encounter and interaction with the stranger, (e3) mother went out of the room (first separation), (e4) mother came back after a time period ranging from 30 seconds and 3 minutes dependent on child´s irritation and reaction of being separated from the mother (stranger left the room while reunion),
For measuring the quality of maternal interactive behavior we videotaped mother-infant interactions during the SSP analyzed by the “Atypical Maternal Behavior Instrument for Assessment and Classification (AMBIANCE)” (AMBIANCE;55). The AMBIANCE is based on the theory of Main and Hesse (1990) and has been developed by Lyons-Ruth and colleagues and assesses anomalous parental behavior of mothers´ during interactions with their infant
Additionally to the concepts of frightened and frightening behaviors and dissociated parental states described by Main and Hesse
For saliva sampling, SalivaBio’s Children’s Swabs (SCS) (Salimetrics, State College, USA) were used by following the standard procedures. Therefore, SCS were placed into the infant’s and mothers´ mouths for about 30 seconds. Thereafter, swabs were stored in storage tubes on ice at -20°C. Upon completion of t4, tubes were centrifugalized at 4°C/ rpm and aliquots were stored at -80° C. Cortisol levels (µg/dL) were analyzed by C. Kirschbaum (Technical University of Dresden, Germany). The salivary concentrations were measured using chemiluminescence immunoassay with high sensitivity (IBL International, Hamburg, Germany). The intra and interassay coefficients for cortisol were below 8%.
We conducted statistical analyses using Statistical Package for the Social Sciences version 23.0 (SSP Inc., Chicago, IL). Statistically significant was set at p<.05. Normal distribution of data was tested by non-parametric Kolmogorov-Smirnov test. Since data were normally distributed, data were analyzed as follows: ANCOVA for repeated measures was calculated for each of the cortisol values between subject (group: “CM-” / “CM+”; “not-disrupted” / “disrupted” maternal behavior; mother, infant) and within subjects (for episode “baseline before SSP” to “+30 min.”). Greenhouse-Geisser as well as Sphericity assumed correction for repeated measures were applied. To test differences between the groups within each measurement we used unpaired t-tests. Infant sex, age of the mother at birth as well as the body mass index of the mother were controlled as covariates (
Descriptive statistics are shown in
|
N | Min | Max | Mean | SD |
Mother’s age at birth | 53 | 21 | 43 | 33.72 | 4.47 |
Body mass indexes | 53 | 17.26 | 31.83 | 24.35 | 3.82 |
Infants´ age | 53 | 11 | 14 | 12.43 | 0.80 |
N | Range | Min. | Max. | Mean | Std. Deviation | Variance | ||
Statistic | Statistic | Statistic | Statistic | Statistic | Std. Error | Statistic | Statistic | |
AMBIANCE overall score | 53 | 5 | 1 | 6 | 3,96 | ,166 | 1,208 | 1,460 |
Valid N (listwise) | 53 | |||||||
Frequency | Percent | Valid Percent | Cumulative Percent | |||||
AMBIANCE overall score | ´non-disruptive´ | 32 | 60,4 | 60,4 | 60,4 | |||
´disruptive´ | 31 | 39,6 | 39,6 | 100,0 | ||||
total | 53 | 100,0 | 100,0 |
N | Range | Min. | Mean | Std. Deviation | ||
Statistic | Statistic | Statistic | Statistic | Std. Error | Statistic | |
Maternal CM | 53 | 70 | 1 | 36,53 | 2,043 | 14,871 |
Valid N (listwise) | 53 | |||||
Frequency | Valid Percent | |||||
Maternal CM | CM- | 25 | 47,2 | |||
CM+ | 28 | 52,8 | ||||
total | 53 | 100,0 |
Focusing maternal HPA axis reactivity during SSP by using ANCOVA for repeated measures, neither main time (F (1.392; 71.008) = 0.579, p= 0.503), nor group effects (F (1; 207.539) = 1.052, p= 0.310) were detectable for CM+ compared to CM-. The values showed marginal, but no significant differences for group-by-time effects (F (1.392; 71.008) = 3.157, p= 0.066) (
For infant´s HPA axis time effects (F (2.226; 109.096) = 14.277, p= 0.000) could be shown. For infant’s main group-by-time (F (2.226; 109.096) = 0.595, p= 0.571) or group effects (F (1; 49) = 0.740, p= 0.394), no significant results were detectable (
T-test analyses comparing two independent samples revealed no differences focusing maternal and infant´s cortisol values and CM for each of the measurements (baseline before SSP - +30 min.).
Using ANCOVA for repeated measures the saliva cortisol in mothers relative to maternal interacting behavior showed neither main time (F (1.398; 71.305) = 0.663, p= 0.466), group-by-time (F (1.398; 71.305) = 1.097, p= 0.320) nor group effects (F (1; 51) = 0.053, p= 0.819) (
Saliva cortisol in their infants, however, showed significant time (F (3; 147) = 16.472, p= 0.000) as well as significant main group-by-time effects (F (3; 147) = 2.897, p= 0.048). For main group effects no significant differences could be shown (F (1; 49) = 1.664, p= 0.203) (
T-test analyses comparing two independent samples showed no differences for maternal cortisol levels focusing maternal interacting behavior. For infants cortisol values differences could be shown for the measurement 15 minutes after SSP (+15 min.) (t(49) = -2.108, p = 0.040). Infants of mothers with lower sensitive caregiving showed significant higher cortisol values (M = 6.46, SD = 3.525)than infants of mothers with a higher sensitive interacting behavior (M = 9.613, SD = 7.051).
Pearson correlation analyses between the CTQ sum score of maternal maltreatment and interacting behavior measured by the AMBIANCE global score revealed no significant associations (r(53)=.080, p=0.567) (
AMBIANCE overall score | CTQ overall score | ||
AMBIANCE overall score | Pearson Correlation | 1 | ,131 |
Sig. (2-tailed) | ,348 | ||
N | 53 | 53 | |
CTQ overall score | Pearson Correlation | ,131 | 1 |
Sig. (2-tailed) | ,348 | ||
N | 53 | 53 |
Our findings reveal differences in the cortisol stress responses of mothers and infants in relation to maternal CM and the quality of interacting behavior. Mothers with a history of CM showed no significant, but by trend differences in their cortisol stress response compared to mothers without CM. Transgenerational effects on cortisol stress reactivity in the child were only present when mothers showed disruptive maternal behavior towards the child, but not when mothers have reported maltreatment in their history
Focusing the infant’s cortisol response in association to maternal CM we could not find any differences between both groups of infants with and without maternal CM. This is in line with Martinez-Torteya et al. (2014) who found no direct association between maternal CM and infant’s cortisol reactivity after stressors
Interestingly, our data showed that maternal interacting quality seems to be a main factor that influence the infant´s cortisol stress regulation. Infants of mothers´ with disruptive interacting behavior showed a significant peak of cortisol level after 15 minutes compared to infants of mothers with sensitive interacting behavior. This indicates that enhanced sensitive caregiving resulted in lower infant’s cortisol stress response. The results are in line with previous studies showing that a higher quality of caregiving resulted in a reduced infant’s cortisol stress response
The SSP is conceived as a stressful procedure in which the infant is stressed by two short separations from the caregiver. Several studies confirmed that the quality of maternal interacting behavior may buffer infants´ distress in situation of emotional arousal
Mothers´ with a history of CM showed no significant but marginal differences in course of their cortisol levels compared to mothers without CM. However mothers with a history of CM started with a lower but not significant differences in cortisol baseline than mothers without CM. This was also found by Trickett et al., (2010) who showed in a longitudinal design that adults maltreated in childhood showed lower cortisol baselines than adults without CM
In summary, we did not find any cortisol-related transmission effects of CM to the next generation, however, maternal behavior seemed to play a crucial role in this context. This is a particularly important and encouraging finding with regard to the cycle of maltreatment and the fact that many parents are concerned to transmit their own experiences to their infants. Especially for parents with CM, the former experience of maltreatment was not as crucial like maternal daily interactions and the relationship with their infant. Inadequate or anomalous maternal interacting behavior may aggravate infants´ stress regulatory strategies, which could be a risk for later stress-related mental and physical burden linked to increased stress vulnerability and impaired emotion regulation
Therefore the findings of our analyses indicate both, protection and risk factors. On the one hand, maternal CM experience has been proven to affect cortisol stress response in adulthood. Especially mothers with CM experiences may be particularly vulnerable for dysregulated HPA axis. On the other hand, we were able to show that CM experience did not directly burden the next generation in terms of their stress regulation capacities. However, daily interactions between mother and infant contribute to the development of infants´ resilient stress responsiveness.
Limitations of this study were saliva acquisition problems due to mothers´ and infants´ limited amounts. This resulted in the small sample size of complete data sets. Additionally, in contrast to other studies with high maltreatment load our study showed a rather low severity of CM experiences. This has to be taken into account when comparing our results with other studies with samples showing wider range of CM experiences. Demographic characteristics of our sample can be considered as one limitation since the level of maternal education was high compared to other samples with history of CM.
Mothers with a history of CM are likely to transmit their own experiences to the next generation. Our data show that not CM per se but the current quality of maternal caregiving plays a crucial role for the regulation of infant’s cortisol stress reactivity. We may conclude that CM experiences are transmitted to the next generation via maternal behavior. This can be considered as an encouraging result, focusing the research findings of early life stress since improvement of maternal behavior is part of most preventions and interventions focusing on parent-infant relationships