Elsevier

Psychoneuroendocrinology

Volume 38, Issue 7, July 2013, Pages 1178-1185
Psychoneuroendocrinology

Human milk cortisol is associated with infant temperament

https://doi.org/10.1016/j.psyneuen.2012.11.002Get rights and content

Summary

The implications of the biologically active elements in milk for the mammalian infant are largely unknown. Animal models demonstrate that transmission of glucocorticoids through milk influences behavior and modifies brain development in offspring. The aim of this study was to determine the relation between human milk cortisol levels and temperament of the breastfed infant. Fifty-two mother and infant pairs participated when the infants were three-months old. Milk cortisol levels were assessed and each mother completed the Infant Behavior Questionnaire (IBQ), a widely used parent-report measure of infant temperament. Analyses revealed a positive association between milk cortisol and the negative affectivity dimension of the IBQ (partial r = .37, p < .01). No correlation was found between elevated cortisol levels and the surgency/extraversion or the orienting/regulation dimensions. Further, the positive association between increased maternal milk cortisol and negative affectivity was present among girls (β = .59, p < .01), but not among boys. (Although, the sex by milk cortisol interaction term was not statistically significant, suggesting that these results require replication.) Environmental factors such as maternal demographics and negative maternal affect (depression and perceived stress) at the time of assessment did not account for the positive association. The findings support the proposal that exposure to elevated levels of cortisol in human milk influences infant temperament. The findings further suggest that mothers have the ability to shape offspring phenotype through the transmission of biologically active components in milk.

Section snippets

Study overview

The relation between milk GCs and infant temperament was examined among breastfed infants. At 3-months postpartum cortisol levels were determined in milk collected from breastfeeding mothers. Each mother completed the Revised Infant Behavior Questionnaire, a widely used and well-validated measure of infant temperament (Gartstein and Rothbart, 2003), and measures of maternal perceived stress and depression.

Participants

Fifty-two mother and infant pairs who were enrolled in a larger longitudinal study of

Milk cortisol and infant temperament

Initial analyses of the association between milk cortisol and infant temperament revealed a positive correlation between cortisol and the negative affectivity dimension of the IBQ after adjusting for time of sample collection (partial r = .37, p < .01; see Fig. 1). The association between milk cortisol and the orienting/regulation dimension approached significance (partial r = −.25, p = .07). No association was found between milk cortisol and the surgency/extraversion dimension (partial r = .14, p = .32).

Discussion

These data are among the first to suggest that one avenue through which the human mother may influence offspring phenotype is by the transmission of biologically active hormones in her milk. Specifically, the data demonstrate that infant consumption of maternal milk with higher levels of cortisol is associated with more negative infant temperament. Confidence is increased in these findings because the association persisted even after taking into account maternal demographic characteristics and

Contributors

Laura Glynn designed and funded the study and oversaw the statistical analyses. Katherine Grey assisted with the statistical analyses and wrote the first draft of the manuscript. Elysia Davis consulted on study design and infant data collection. Curt Sandman provided partial funding for the study. All authors contributed to and have approved the final manuscript.

Role of funding sources

This research was supported by grants from the National Institutes of Health (HD-40967 to LMG and NS-41298) and by a grant from the University of California, Irvine (CORCLR to LMG). The breast pumps were donated by Medela.

Conflict of interest

The authors have no conflicts of interest to disclose.

Acknowledgments

The authors thank the families who participated in this project and the staff at the UCI Women and Children's Health and Well-Being project for their excellent work.

References (79)

  • M.K. Davis

    Breastfeeding and chronic disease in childhood and adolescence

    Pediatr. Clin. North Am.

    (2001)
  • C. de Weerth et al.

    Prenatal maternal cortisol levels and infant behavior during the first 5 months

    Early Hum. Dev.

    (2003)
  • N.J. Friedman et al.

    The role of breast-feeding in the development of allergies and asthma

    J. Allergy Clin. Immunol.

    (2005)
  • M.A. Gartstein et al.

    Studying infant temperament via the revised infant behavior questionnaire

    Infant Behav. Dev.

    (2003)
  • L.M. Glynn et al.

    Postnatal maternal cortisol levels predict temperament in healthy breastfed infants

    Early Hum. Dev.

    (2007)
  • K.M. Godfrey et al.

    Fetal nutrition and adult disease

    Am. J. Clin. Nutr.

    (2000)
  • M. Hamosh

    Bioactive factors in human milk

    Pediatr. Clin. North Am.

    (2001)
  • S. Hart et al.

    Breast milk levels of cortisol and secretory immunoglobulin A (SIgA) differ with maternal mood and infant neuro-behavioral functioning

    Infant Behav. Dev.

    (2004)
  • A.J. McDonald

    Cortical pathways to the mammalian amygdala

    Prog. Neurobiol.

    (1998)
  • C.P. McLean et al.

    Brave men and timid women? A review of the gender differences in fear and anxiety

    Clin. Psychol. Rev.

    (2009)
  • E. Mittendorfer-Rutz et al.

    Restricted fetal growth and adverse maternal psychosocial and socioeconomic conditions as risk factors for suicidal behavior of offspring: a cohort study

    Lancet

    (2004)
  • M. Nagano et al.

    Prenatal dexamethasone exposure affects anxiety-like behaviour and neuroendocrine systems in an age-dependent manner

    Neurosci. Res.

    (2008)
  • D. Owen et al.

    Maternal adversity, glucocorticoids and programming of neuroendocrine function and behavior

    Neurosci. Biobehav. Rev.

    (2005)
  • M. Prior et al.

    Does shy-inhibited temperament in childhood lead to anxiety problems in adolescence?

    J. Am. Acad. Child Adolesc. Psychiat.

    (2000)
  • A.K. Salm et al.

    Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress

    Brain Res. Dev. Brain Res.

    (2004)
  • C.E. Schwartz et al.

    Adolescent social anxiety as an outcome of inhibited temperament in childhood

    J. Am. Acad. Child Adolesc. Psychiat.

    (1999)
  • L.A. Sroufe et al.

    Conceptualizing the role of early experience: lessons from the Minnesota longitudinal study

    Dev. Rev.

    (2010)
  • P.D. Trautman et al.

    Effects of early prenatal dexamethasone on the cognitive and behavioral development of young children: results of a pilot study

    Psychoneuroendocrinology

    (1995)
  • L.A. Welberg et al.

    Prenatal glucocorticoid programming of the brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behavior

    Neuroscience

    (2001)
  • D.G. Zuloaga et al.

    Dexamethasone induces apoptosis in the developing rat amygdala in an age-, region-, and sex-specific manner

    Neuroscience

    (2011)
  • L. Angelucci et al.

    Perinatal mother–offspring pituitary adrenal interrelationship in rats: corticosterone in milk may affect adult life

    Endocrinol. Exp.

    (1983)
  • L. Angelucci et al.

    A model for later-life effects of perinatal drug exposure: maternal hormone mediation

    Neurobehav. Toxicol. Teratol.

    (1985)
  • D.J.P. Barker

    Mothers, Babies and Health in Later Life

    (1998)
  • C.E. Bertram et al.

    Prenatal programming of postnatal endocrine responses by glucocorticoids

    Reproduction

    (2002)
  • S. Cohen et al.

    A global measure of perceived stress

    J. Health Soc. Behav.

    (1983)
  • J.L. Cox et al.

    Detection of postnatal depression: development of the 10-item Edinburgh Postnatal Depression Scale

    Br. J. Psychiat.

    (1987)
  • E.P. Davis et al.

    Prenatal maternal stress programs infant stress regulation

    J. Child Psychol. Psychiat.

    (2011)
  • S.S. De Pauw et al.

    Temperament, personality and developmental psychopathology: a review based on the conceptual dimensions underlying childhood traits

    Child Psychiat. Hum. Dev.

    (2010)
  • J.A. DiPietro et al.

    Fetal motor activity and maternal cortisol

    Dev. Psychobiol.

    (2009)
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