The dual nature of hypothalamic-pituitary-adrenal axis regulation in dyads of very preterm infants and their mothers

Provenzi, Livio; Giusti, Lorenzo; Fumagalli, Monica; Frigerio, Susanna; Morandi, Francesco; Borgatti, Renato; Mosca, Fabio; Montirosso, Rosario

doi:10.1016/j.psyneuen.2018.10.007

Cited by 26 publications

(20 citation statements)

References 48 publications

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“…3 NICU life-saving procedures still entail invasive and painful stimulations, such as skin-breaking procedures, and NICU-related stress has been associated with emotional and neuroendocrine disruptions later in life. [4][5][6][7] Emotional dysregulation during early childhood is one of the most reported detrimental outcomes of preterm birth and it is sensitive to early exposure to NICU-related stress and pain. 8,9 The serotonin system is a key regulator of emotional development and stress regulation 10 and the SLC6A4 gene encoding for the serotonin transporter is known to be sensitive to epigenetic regulation through changes in DNA methylation in response to environmental exposures.…”

Section: Introductionmentioning

confidence: 99%

“…Preterm infants need long‐lasting specialised care in the neonatal intensive care unit (NICU), which exposes their immature brain to different sources of stress . NICU life‐saving procedures still entail invasive and painful stimulations, such as skin‐breaking procedures, and NICU‐related stress has been associated with emotional and neuroendocrine disruptions later in life . Emotional dysregulation during early childhood is one of the most reported detrimental outcomes of preterm birth, and it is sensitive to early exposure to NICU‐related stress and pain …”

Section: Introductionmentioning

confidence: 99%

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Pain‐related increase in serotonin transporter gene methylation associates with emotional regulation in 4.5‐year‐old preterm‐born children

et al. 2019

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Aim. The main goal of this study was to assess the association between pain-related increase in serotonin transporter gene (SLC6A4) methylation and emotional dysregulation in 4.5-year-old preterm children compared to full-term matched counterparts.Methods. Preterm (n=29) and full-term (n=26) children recruited from two Italian hospitals were followed-up from October 2011 to December 2017. SLC6A4 methylation was assessed from cord blood at birth from both groups and peripheral blood at discharge for preterm ones. At 4.5 years, emotional regulation (i.e., anger, fear, sadness) was assessed through an observational standardized procedure.Results. Preterm children (18 females; mean age = 4.5, range = 4.3 -4.8) showed greater anger display compared to full-term controls (14 females; mean age = 4.5, range = 4.4 -4.9) in response to emotional stress. Controlling for adverse life events occurrence from discharge to 4.5 years and SLC6A4 methylation at birth, CpG-specific SLC6A4 methylation in the neonatal period was predictive of greater anger display in preterm children but not in full-term ones.Conclusion. These findings contribute to highlight how epigenetic regulation of serotonin transporter gene in response to NICU pain exposure contributes to long-lasting programming of anger regulation in preterm children. KEY POINTS• Early exposure to adverse events may contribute to the behavioural phenotype of preterm infants via epigenetic mechanisms.• Pain-related increase in serotonin transporter gene methylation associated with increased anger response to emotional stress at 4.5 years of age in preterm children.• These findings highlight the importance of limiting early pain exposure in preterm infants to reduce the risk of later emotional dysregulation.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Pain‐related increase in serotonin transporter gene methylation associates with emotional regulation in 4.5‐year‐old preterm‐born children

et al. 2019

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“…Other small sample studies ( N = 42 and 63) have found no association with caregiver-related factors (Castral et al, 2015; Thompson & Trevathan, 2009). Infant pre-term status and distress during a three-day sleep training program also predicted increased adrenocortical synchrony (Middlemiss et al, 2012; Provenzi et al, 2019). Cortisol synchrony was found in a sample of low-income Mexican mother–child dyads (Luecken et al, 2019); however, they did not include a higher-income comparison group or examine associations with indices of caregiver or child functioning, impeding the interpretation of these findings.…”

Section: Resultsmentioning

confidence: 99%

A systematic review of caregiver–child physiological synchrony across systems: Associations with behavior and child functioning

DePasquale

2020

Dev Psychopathol

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Extensive research has established a positive association between caregiver-child behavioral synchrony and child developmental functioning. Burgeoning research examining physiological synchrony has yet to elucidate its impact for children’s developing self-regulation. The objectives of this systematic review were to: 1) determine whether there is evidence that caregiver-child physiological synchrony promotes positive child development, 2) examine developmental differences in physiological synchrony and its correlates, and 3) explore whether context, risk, and/or stress influence patterns of synchrony. Sixty-nine studies met the following criteria on PubMed and PsycINFO: 1) peer-reviewed empirical articles in English that 2) examine autonomic, hypothalamic-pituitary-adrenocortical, and/or central nervous system activity 3) for caregivers and children 4) in response to a task and 5) directly examine the association between caregiver and child physiology. Findings varied based on developmental period and current behavioral context. Functional differences may exist across physiological systems and contexts. Synchrony may have different developmental consequences for dyads with and without certain risk factors. Few studies examine physiological synchrony across multiple systems or contexts, nor do they measure child characteristics associated with synchrony. Statistical and methodological challenges impede interpretation. Findings generally support the idea that physiological synchrony may support children’s developing self-regulation. Longitudinal research is needed to examine child developmental outcomes over time.

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“…Second, infants in the current study were also from low-risk family environments, and the current findings may not reflect how parent-infant adrenocortical attunement may be altered for infants from impoverished, high-stress environments, or for infants at significant developmental risk. For instance, Provenzi et al (2019) found that full-term compared to very preterm three-month-old infants displayed significant within-time cortisol correlations with their mothers in the SFP. Lastly, infants and their parents were from white, middle-class, two-parent, mother-father families in the U.S., be noted that Abraham et al (2014), using an Israeli sample, found that primary caregiver mother, secondary caregiver (heterosexual), and primary caregiver same-sex fathers demonstrated a similar "global parental caregiving brain network" contributing to parentinfant biobehavioral synchrony.…”

Section: Limitations and Future Directionsmentioning

confidence: 99%

“…Previous research has used procedures like the Still-Face Procedure (Provenzi et al, 2019; for review see Provenzi et al, 2016), Lab-TAB (e.g., Hibel et al, 2009), and a daily routine activity like a diaper change (Mörelius et al, 2012) to assess mother-infant cortisol attunement at various time points in infancy, but not fatherinfant cortisol attunement. Future research should consider the type of procedure used to elicit cortisol responses in parents and infants, and issues surrounding measurement equivalence for infants and parents, when considering the concept of attunement as it is difficult to argue for attunement between infants and parents when both are responding differently to the same means of measurement.…”

Section: Limitations and Future Directionsmentioning

confidence: 99%

Adrenocortical interdependence in father‐infant and mother‐infant dyads: Attunement or something more?

Bader

Tan

Gonzalez

et al. 2021

Developmental Psychobiology

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Father-infant and mother-infant (one-year-olds) adrenocortical attunement was explored during the Strange Situation Procedure (SSP) among 125 father-infant and 141 mother-infant dyads. Cortisol was assessed at baseline (T1), 20 (T2), and 40 minutes (T3) after the first parent-infant separation. Initial correlations indicated significant associations between father-infant and mother-infant cortisol at each time. Cortisol interdependence was further explored using Actor-Partner Interdependence Models.There was no evidence supporting cortisol interdependence based on within-time residual correlations between parent-infant cortisol, once stability and cross-lagged paths were controlled. Infant cortisol at T2 predicted T3 cortisol for fathers and mothers resulting in a series of follow-up exploratory analyses to examine mediating processes which revealed that infant distress during the SSP predicted infant T2 cortisol, which, in turn, predicted infant negativity during the 15-min mother-infant teaching task that followed the SSP. Among father-infant dyads, infant T2 cortisol predicted infant negativity during father-infant interaction, with infants expressing more negativity having less sensitive fathers. Findings provide little support of parent-infant adrenocortical attunement across either father-infant or mother-infant dyads during the SSP, but preliminary evidence indicates infant distress as a potential mediator.Future research may want to focus on affective and behavioral processes that underlie the concept of parent-infant adrenocortical attunement.

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The dual nature of hypothalamic-pituitary-adrenal axis regulation in dyads of very preterm infants and their mothers

Cited by 26 publications

References 48 publications

Pain‐related increase in serotonin transporter gene methylation associates with emotional regulation in 4.5‐year‐old preterm‐born children

Pain‐related increase in serotonin transporter gene methylation associates with emotional regulation in 4.5‐year‐old preterm‐born children

A systematic review of caregiver–child physiological synchrony across systems: Associations with behavior and child functioning

Adrenocortical interdependence in father‐infant and mother‐infant dyads: Attunement or something more?

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