Are cortisol concentrations in human breast milk associated with infant crying?

Christine Hechler, Roseriet Beijers, J Marianne Riksen-Walraven, Carolina de Weerth, Christine Hechler, Roseriet Beijers, J Marianne Riksen-Walraven, Carolina de Weerth

Abstract

The present longitudinal study is the first to investigate the association between human breast milk cortisol and infant crying over the first three months of life. Higher concentrations of breast milk cortisol were expected to be differentially associated with fussing and crying in boys and girls. At 2, 6, and 12 weeks of infant age, mothers (N = 70) collected a morning sample of their milk and kept a 3-day diary to measure infant fussing and crying. Cortisol was extracted and quantified from milk samples. Results showed that breast milk cortisol concentrations increased from 2 weeks through 12 weeks of infant age. Milk cortisol was unrelated to the total duration, frequency, and bout length of infant fussing and crying for both boys and girls. Directions for future research aiming to extend our knowledge on the biology of milk cortisol in relation to infant behavior and development are discussed.

Keywords: breast milk cortisol; breastfeeding; humans; infant crying; lactational programming.

© 2018 The Authors. Developmental Psychobiology Published by Wiley Periodicals, Inc.

Figures

Figure 1
Figure 1
Flow chart of the sample

References

    1. Agostoni, C. , Braegger, C. , Decsi, T. , Kolacek, S. , Koletzko, B. , Fleischer Michaelsen, K. , … van Goudoever, J. (2009). Breast‐feeding: A commentary by the ESPGHAN committee on nutrition. Journal of Pediatric Gastroenterology & Nutrition, 49, 112–25. 10.1097/MPG.0b013e31819f1e05
    1. Allen‐Blevis, C. R. , Sela, D. A. , & Hinde, K. (2015). Milk bioactives manipulate microbes to mediate parent‐offspring conflict. Evolution, Medicine, and Public Health, 1, 106–21. 10.1093/emph/eov007
    1. Bäckhed, F. (2011). Programming of host metabolism by the gut microbiota. Annals of Nutrition and Metabolism, 58, S44–S52. 10.1159/000328042
    1. Baker, C. E. (2014). African American fathers’ depression and stress as predictors of father involvement during early childhood. Journal of Black Psychology, 40, 311–33. 10.1177/0095798413486480
    1. Barr, R. G. (2000). Excessive crying In Sameroff A. J., Lewis M., & Miller S. M. (Eds.), Handbook of developmental psychopathology (pp. 327–50). New York, NY: Springer Science+Business Media LLC.
    1. Barr, R. G. , Fairbrother, N. , Pauwels, J. , Green, J. , Chen, M. , & Brant, R. (2014). Maternal frustration, emotional and behavioural responses to prolonged infant crying. Infant Behavior and Development, 37, 652–64. 10.1016/j.infbeh.2014.08.012
    1. Barr, R. G. , Kramer, M. S. , Boisjoly, C. , McVey‐White, L. , & Pless, I. B. (1988). Parental diary of infant cry and fuss behaviour. Archives of Disease in Childhood, 63, 380–7. 10.1136/adc.63.4.380
    1. Barr, R. G. , Paterson, J. A. , MacMartin, L. M. , Lehtonen, L. , & Young, S. N. (2005). Prolonged and unsoothable crying bouts in infants with and without colic. Developmental and Behavioral Pediatrics, 26, 14–23. 0196-206X/00/2601-0014
    1. Barr, R. G. , Trent, R. B. , & Cross, J. (2006). Age‐related incidence curve of hospitalized Shaken Baby Syndrome cases: Convergent evidence for crying as a trigger to shaking. Child Abuse & Neglect, 30, 7–16. 10.1016/j.chiabu.2005.06.009
    1. Beijers, R. , Buitelaar, J. K. , & de Weerth, C. (2014). Mechanisms underlying the effects of prenatal psychosocial stress on child outcomes: Beyond the HPA axis. European Child & Adolescent Psychiatry, 23, 943–56. 10.1007/s00787-014-0566-3
    1. Bilgin, A. , & Wolke, D. (2017). Development of comorbid crying, sleeping, feeding problems across infancy: Neurodevelopmental vulnerability and parenting. Early Human Development, 109, 37–43. 10.1016/j.earlhumdev.2017.04.002
    1. Brand, S. , Furlano, R. , Sidler, M. , Schulz, J. , & Holsboer‐Trachsler, E. (2014). Associations between infants' crying, sleep and cortisol secretion and mother's sleep and well‐being. Neuropsychobiology, 69, 39–51. 10.1159/000356968
    1. Catalani, A. , Casolini, P. , Cigliana, G. , Scaccianoce, S. , Consoli, C. , Cinque, C. , … Angelucci, L. (2002). Maternal corticosterone influences behavior, stress response and corticosteroid receptors in the female rat. Pharmacology, Biochemistry, and Behavior, 73, 105–14. 10.1016/S0091-3057(02)00755-4
    1. Catalani, A. , Casolini, P. , Scaccianoce, S. , Patacchioli, F. R. , Spinozzi, P. , & Angelucci, L. (2000). Maternal corticosterone during lactation permanently affects brain corticosteroid receptors, stress response and behaviour in rat progeny. Neuroscience, 100, 319–25. 10.1016/S0306-4522(00)00277-3
    1. Costigan, C. L. , Cox, M. J. , & Cauce, A. M. (2003). Work‐parenting linkages among dual‐earner couples at the transition to parenthood. Journal of Family Psychology, 17(3), 397–408. 10.1037/0893-3200.17.3.397
    1. de Lauzon‐Guillain, B. , Wijndaele, K. , Clark, M. , Acerini, C. , Hughes, I. A. , Dunger, D. B. , … Wells, J. C. (2012). Breastfeeding and infant temperament at age three months. PLOS One, 10.1371/journal.pone.0029326
    1. de Vries, M. W. (1984). Temperament and infant mortality among the Masai of East Africa. American Journal of Psychiatry, 141, 1189–94.
    1. de Weerth, C. , Fuentes, S. , & de Vos, W. (2013). Crying in infants: On the possible role of intestinal microbiota in the development of colic. Gut Microbes, 4(5), 416–21. 10.4161/gmic.26041
    1. de Weerth, C. , Fuentes, S. , Puylaert, P. , & de Vos, W. M. (2013). Intestinal microbiota of infants with colic: Development and specific signatures. Pediatrics, 131, e550–e8. 10.1542/peds.2012-1449
    1. Del Giudice, M. (2012). Fetal programming by maternal stress: Insight from a conflict perspective. Psychoneuroendocrinology, 37, 1614–29. 10.1016/j.psyneuen.2012.05.014
    1. Dettmer, A. M. , Murphy, A. M. , Guitarra, D. , Slonecker, E. , Suomi, S. J. , Rosenberg, K. L. , … Hinde, K. (2017). Cortisol in neonatal mother's milk predicts later infant social and cognitive functioning in rhesus monkeys. Child Development, 89(2), 525–38. 10.1111/cdev.12783
    1. Dickerson, S. S. , & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130, 355–91. 10.1037/0033-2909.130.3.355
    1. Dimmitt, R. A. , Staley, E. M. , Chuang, G. , Tanner, S. M. , Soltau, T. D. , & Lorenz, R. G. (2010). Role of postnatal acquisition of the intestinal microbiome in the early development of immune function. Journal of Pediatric Gastroenterology and Nutrition, 51, 262–73. 10.1097/MPG.0b013e3181e1a114
    1. Evenhouse, E. , & Reilley, S. (2005). Improved estimates of the benefits of breastfeeding using sibling comparisons to reduce selection bias. Health Service Research, 40, 1781–802. 10.1111/j.1475-6773.2005.00453.x
    1. Finken, M. J. J. , van der Voorn, B. , Hollanders, J. J. , Dijkstra, L. , Toorop, A. A. , & Rotteveel, J. (2017). Cortisol in human milk: The good, the bad, or the ugly? Obesity, 25(7), 1153 10.1002/oby.21882
    1. Frankenhuis, W. E. , & de Weerth, C. (2013). Does early‐life exposure to stress shape or impair cognition? Current Directions in Psychological Science, 22, 407–12. 10.1177/0963721413484324
    1. Fujiwara, T. , Barr, R. G. , Brant, R. , & Barr, M. (2011). Infant distress at five weeks of age and caregiver frustration. The Journal of Pediatrics, 159, 425–30. 10.1016/j.jpeds.2011.02.010
    1. Glynn, L. M. , Davis, E. P. , Schetter, C. D. , Chicz‐Demet, A. , Hobel, C. J. , & Sandman, C. A. (2007). Postnatal maternal cortisol levels predict temperament in healthy breastfed infants. Early Human Development, 83, 675–81. 10.1016/j.earlhumdev.2007.01.003
    1. Grey, K. R. , Davis, E. P. , Sandman, C. A. , & Glynn, L. M. (2013). Human milk cortisol is associated with infant temperament. Psychoneuroendocrinology, 38, 1178–85. 10.1016/j.psyneuen.2012.11.002
    1. Hahn‐Holbrook, J. , Le, T. B. , Chung, A. , Davis, E. P. , & Glynn, L. (2016). Cortisol in human milk predicts child BMI. Obesity, 24, 2471–4. 10.1002/oby.21682
    1. Halpern, L. F. , Brand, K. L. , & Malone, A. F. (2001). Parenting stress in mothers of very‐low‐birth‐weight (VLBW) and full‐term infants: A function of infant behavioral characteristics and child‐rearing attitudes. Journal of Pediatric Psychology, 26, 93–104. 10.1093/jpepsy/26.2.93
    1. Hamosh, M. (2001). Bioactive factors in human milk. Pediatric Clinics of North America, 48, 69–86. 10.1016/S0031-3955(05)70286-8
    1. Hinde, K. (2013). Lactational programming of infant behavioral phenotype In Clancy K. B. H., Hinde K., & Rutherford's J. N. (Eds.), Building Babies: Primate development in proximate and ultimate perspective (pp. 187–207). New York, NY: Springer Science + Business Media.
    1. Hinde, K. , Skibiel, A. L. , Foster, A. B. , Del Rosso, L. , Mendoza, S. P. , & Capitanio, J. P. (2014). Cortisol in mother's milk across lactation reflects maternal life history and predicts infant temperament. Behavioral Ecology, 26(1), 269–81. 10.1093/beheco/aru186
    1. Huang, J. , Peters, K. E. , Vaughn, M. G. , & Witko, C. (2014). Breastfeeding and trajectories of children’s cognitive development. Developmental Science, 17, 452–61. 10.1111/desc.12136
    1. Kolb, B. , & Gibb, R. (2011). Brain plasticity and behaviour in the developing brain. Journal of the Canadian Academy of Child and Adolescent Psychiatry, 20(4), 265–76.
    1. Korja, R. , Huhtala, M. , Maunu, J. , Rautava, P. , Haataja, L. , Lapinleimu, H. , & Lehtonen, L. (2014). Preterm infant's early crying associated with child's behavioral problems and parents' stress. Pediatrics, 133, 1–7. 10.1542/peds.2013-1204
    1. Kusaka, R. , Ohgi, S. , Shigemori, K. , & Fujimoto, T. (2008). Crying and behavioural characteristics in premature infants. Journal of the Japanese Physical Therapy Association, 11, 15–21. 10.1298/jjpta.11.15
    1. Milidou, I. , Søndergaard, C. , Jensen, M. S. , Olsen, J. , & Henriksen, T. B. (2014). Gestational age, small for gestational age, and infantile colic. Paediatric and Perinatal Epidemiology, 2, 138–45. 10.1111/ppe.12095
    1. Miller, E. M. , Aiello, M. O. , Fujita, M. , Hinde, K. , Milligan, L. , & Quinn, E. A. (2013). Field and laboratory methods in human milk research. American Journal of Human Biology, 25, 1–11. 10.1002/ajhb.22334
    1. Nichols, M. R. , & Roux, G. M. (2004). Maternal perspectives on postpartum return to the workplace. Journal of Obstetric, Gynecologic & Neonatal Nursing, 33(4), 463–71. 10.1177/0884217504266909
    1. Nolvi, S. , Uusitupa, H.‐M. , Bridgett, D. J. , Pesonen, H. , Aatsinki, A.‐K., Kataja, E.‐L., … Karlsson, L. (2017). Human milk cortisol concentration predicts experimentally induced fear reactivity: Moderation by infant sex. Developmental Science, e12625 10.1111/desc.12625
    1. Owen, D. , Andrews, M. H. , & Matthews, S. G. (2005). Maternal adversity, glucocorticoids and programming of neuroendocrine function and behavior. Neuroscience and Biobehavioral Reviews, 29, 209–26. 10.1016/j.neubiorev.2004.10.004
    1. Pettigrew, M. M. , Khodaee, M. , Gillespie, B. , Schwartz, K. , Bobo, J. K. , & Foxman, B. (2003). Duration of breastfeeding, daycare, and physician visits among infants 6 months and younger. Annals of Epidemiology, 13, 431–5. 10.1016/S1047-2797(02)00463-5
    1. Pundir, S. , Wall, C. R. , Mitchell, C. J. , Thostensen, E. B. , Lai, C. T. , Geddes, D. T. , & Cameron‐Smith, D. (2017). Variation of human milk glucocorticoids over 24 hour period. Journal of Mammary Gland Biology and Neoplasia, 22, 85–92. 10.1007/s10911-017-9375-x
    1. Radesky, J. S. , Zuckerman, B. , Silverstein, M. , Rivara, F. O. , Barr, M. , Taylor, J. A. , … Barr, R. G. (2013). Inconsolable crying and maternal postpartum depressive symptoms. Pediatrics, 131, 1–8. 10.1542/peds.2012-3316
    1. Reijneveld, S. A. , van der Wal, M. F. , Brugman, E. , Hira Sing, R. A. , & Verloove‐Vanhorick, S. P. (2004). Infant crying and abuse. Lancet, 364, 1340–2. 10.1016/S0140-6736(04)17191-2
    1. Sapolsky, R. M. (2003). Stress and plasticity in the limbic system. Neurochemical Research, 28, 1735–42. 10.1023/A:1026021307833
    1. Sudo, N. , Chida, Y. , Aiba, Y. , Sonoda, J. , Oyama, N. , Yu, X. N. , … Koga, Y. (2004). Postnatal microbial colonization programs the hypothalamic‐pituitary‐adrenal system for stress response in mice. The Journal of Physiology, 558, 263–75. 10.1113/jphysiol.2004.063388
    1. Sullivan, E. C. , Hinde, K. , Mendoza, S. P. , & Capitanio, J. P. (2011). Cortisol concentrations in the milk of rhesus monkey mothers are associated with confident temperament in sons, but not daughters. Developmental Psychobiology, 53, 96–104. 10.1002/dev.20483
    1. Tabachnik, B. G. , & Fidell, L. S. (2007). Multilevel linear modeling In Hartman's S. (Ed.), Using multivariate statistics (pp. 781–857). Boston, MA: Pearson Education Inc.
    1. Thomas, D. G. (2014). Is breast best in the west of England? Use of linked routinely collected data sources to quantify the protective effect of breastfeeding against infectious gastrointestinal and respiratory illness during the first year of life. Lancet, 384, S78 10.1016/S0140-6736(14)62204-2
    1. Van der Voorn, B. , de Waard, M. , van Goudoever, J. B. , Rotteveel, J. , Heijboer, A. C. , & Finken, M. J. J. (2016). Breast‐milk cortisol and cortisone concentrations follow the diurnal rhythm of maternal hypothalamus‐pituitary‐adrenal axis activity. Journal of Nutrition, 146, 2174–9. 10.3945/jn.116.236349
    1. Wells, J. C. K. (2014). Adaptive variability in the duration of critical windows of plasticity: Implications for the programming of obesity. Evolution, Medicine, and Public Health, 2014(1), 109–21. 10.1093/emph/eou019
    1. Wiese, B. S. , & Heidemeier, H. (2012). Successful return to work after maternity leave: Self‐regulatory and contextual influences. Research in Human Development, 9(4), 317–36. 10.1080/15427609.2012.729913
    1. Wolke, D. , Bilgin, A. , & Samara, M. (2017). Systematic review and meta‐analysis: Fussing and crying durations and prevalence of colic in infants. The Journal of Pediatrics, 185, 55–61. 10.1016/j.jpeds.2017.02.020

Source: PubMed

Szponzorok és közreműködők

Egészségi állapot

Kábítószer-beavatkozások

3
Iratkozz fel