Top

Published in:

Open Access 01-06-2020 | Glucocorticoid | Original Article

Diurnal rhythmicity in breast-milk glucocorticoids, and infant behavior and sleep at age 3 months

Authors: Alyssa A. Toorop, Bibian van der Voorn, Jonneke J. Hollanders, Lisette R. Dijkstra, Koert M. Dolman, Annemieke C. Heijboer, Joost Rotteveel, Adriaan Honig, Martijn J. J. Finken

Published in: Endocrine | Issue 3/2020

Abstract

Purpose

In previous studies, associations between breast-milk cortisol levels obtained on one occasion and infant neurodevelopment were demonstrated. However, more recent evidence indicates that breast-milk cortisol and cortisone concentrations follow the diurnal rhythm of maternal hypothalamus-pituitary-adrenal axis, peaking in the early morning and with a nadir at midnight. We studied associations between breast-milk glucocorticoid (GC) rhythmicity, and infant behavior and sleep.

Methods

We included 59 mothers, and their infants, of whom 17 had consulted an expert center during pregnancy for an increased risk of psychological distress. At 1 month postpartum, breast milk was sampled (on average six times) over a 24 h period for assessment of cortisol and cortisone using LC-MS/MS, and experienced maternal distress was assessed using the Hospital Anxiety and Depression Scale questionnaire. Three months after birth, infant behavior was assessed with the Infant Behavior Questionnaire, and infant sleep pattern was quantified by questionnaire. Associations between breast-milk GC rhythm parameters (maximum, delta, and Area Under the Curve increase and ground) and infant behavior and sleep were tested with linear regression analyses.

Results

No consistent associations between breast-milk GC rhythm parameters and infant behavior or sleep were found.

Conclusions

Breast-milk GC rhythmicity at 1 month postpartum was not associated with infant behavior or sleep at the age of 3 months. Findings from previous studies linking breast-milk cortisol to infant neurodevelopment might be biased by the lack of GC measurements across the full diurnal cycle, and should therefore be interpreted with caution.

Available only for authorised users

L. Andersson, I. Sundstrom-Poromaa, M. Bixo, M. Wulff, K. Bondestam, M. aStrom, Point prevalence of psychiatric disorders during the second trimester of pregnancy: a population-based study. Am. J. Obstet. Gynecol. 189(1), 148–154 (2003)CrossRef

M.R. Jarcho, G.M. Slavich, H. Tylova-Stein, O.M. Wolkowitz, H.M. Burke, Dysregulated diurnal cortisol pattern is associated with glucocorticoid resistance in women with major depressive disorder. Biol. Psychol. 93(1), 150–158 (2013). https://doi.org/10.1016/j.biopsycho.2013.01.018 CrossRefPubMedPubMedCentral

S.A. Vreeburg, W.J. Hoogendijk, R.H. DeRijk, R. van Dyck, J.H. Smit, F.G. Zitman, B.W. Penninx, Salivary cortisol levels and the 2-year course of depressive and anxiety disorders. Psychoneuroendocrinology 38(9), 1494–1502 (2013). https://doi.org/10.1016/j.psyneuen.2012.12.017 CrossRefPubMed

J.R. Seckl, Prenatal glucocorticoids and long-term programming. Eur. J. Endocrinol. 151(Suppl 3), U49–62 (2004)CrossRef

E.P. Davis, L.M. Glynn, C.D. Schetter, C. Hobel, A. Chicz-Demet, C.A. Sandman, Prenatal exposure to maternal depression and cortisol influences infant temperament. J. Am. Acad. Child Adolesc. Psychiatry 46(6), 737–746 (2007). https://doi.org/10.1097/chi.0b013e318047b775 CrossRefPubMed

T. Field, M. Diego, M. Hernandez-Reif, B. Figueiredo, S. Schanberg, C. Kuhn, Sleep disturbances in depressed pregnant women and their newborns. Infant Behav. Dev. 30(1), 127–133 (2007). https://doi.org/10.1016/j.infbeh.2006.08.002 CrossRefPubMed

M.P. Luijk, N. Saridjan, A. Tharner, M.H. van Ijzendoorn, M.J. Bakermans-Kranenburg, V.W. Jaddoe, A. Hofman, F.C. Verhulst, H. Tiemeier, Attachment, depression, and cortisol: deviant patterns in insecure-resistant and disorganized infants. Dev. Psychobiol. 52(5), 441–452 (2010). https://doi.org/10.1002/dev.20446 CrossRefPubMed

V. Glover, T.G. O’Connor, K. O’Donnell, Prenatal stress and the programming of the HPA axis. Neurosci. Biobehav Rev. 35(1), 17–22 (2010). https://doi.org/10.1016/j.neubiorev.2009.11.008 CrossRefPubMed

M.A. Zijlmans, J.M. Riksen-Walraven, C. de Weerth, Associations between maternal prenatal cortisol concentrations and child outcomes: a systematic review. Neurosci. Biobehav Rev. 53, 1–24 (2015). https://doi.org/10.1016/j.neubiorev.2015.02.015 CrossRefPubMed

10.

P.J. Brunton, Programming the brain and behaviour by early-life stress: a focus on neuroactive steroids. J. Neuroendocrinol. 27(6), 468–480 (2015). https://doi.org/10.1111/jne.12265 CrossRefPubMed

11.

K. Ivars, N. Nelson, A. Theodorsson, E. Theodorsson, J.O. Strom, E. Morelius, Development of salivary cortisol circadian rhythm and reference intervals in full-term infants. PLoS ONE 10(6), e0129502 (2015). https://doi.org/10.1371/journal.pone.0129502 CrossRefPubMedPubMedCentral

12.

C. de Weerth, R.H. Zijl, J.K. Buitelaar,, Development of cortisol circadian rhythm in infancy. Early Hum. Dev. 73(1–2), 39–52 (2003).CrossRef

13.

H. Oster, E. Challet, V. Ott, E. Arvat, E.R. de Kloet, D.J. Dijk, S. Lightman, A. Vgontzas, E. Van Cauter, The functional and clinical significance of the 24-hour rhythm of circulating glucocorticoids. Endocr. Rev. 38(1), 3–45 (2017). https://doi.org/10.1210/er.2015-1080 CrossRefPubMed

14.

D. Joseph, N.W. Chong, M.E. Shanks, E. Rosato, N.A. Taub, S.A. Petersen, M.E. Symonds, W.P. Whitehouse, M. Wailoo,, Getting rhythm: how do babies do it?. Arch. Dis. Child Fetal Neonatal Ed. 100(1), F50–F54 (2015). https://doi.org/10.1136/archdischild-2014-306104 CrossRefPubMed

15.

K. Nishihara, S. Horiuchi, H. Eto, S. Uchida, The development of infants’ circadian rest-activity rhythm and mothers’ rhythm. Physiol. Behav. 77(1), 91–98 (2002)CrossRef

16.

S. Arslanoglu, E. Bertino, M. Nicocia, G.E. Moro, WAPM Working Group on Nutrition: potential chronobiotic role of human milk in sleep regulation. J. Perinat. Med. 40(1), 1–8 (2012)CrossRef

17.

J. Pacha, Development of intestinal transport function in mammals. Physiol. Rev. 80(4), 1633–1667 (2000). https://doi.org/10.1152/physrev.2000.80.4.1633 CrossRefPubMed

18.

K.Y. Yeh, M. Yeh, P.R. Holt, Induction of intestinal differentiation by systemic and not by luminal corticosterone in adrenalectomized rat pups. Endocrinology 124, 1898–1904 (1989)CrossRef

19.

Dettmer, A. M., Murphy, A. M., Guitarra, D., Slonecker, E., Suomi, S. J., Rosenberg, K. L., Novak, M. A., Meyer, J. S., Hinde, K. Cortisol in neonatal mother’s milk predicts later infant social and cognitive functioning in Rhesus Monkeys. Child Dev. (2017). https://doi.org/10.1111/cdev.12783

20.

K. Hinde, A.L. Skibiel, A.B. Foster, L. Del Rosso, S.P. Mendoza, J.P. Capitanio, Cortisol in mother’s milk across lactation reflects maternal life history and predicts infant temperament. Behav. Ecol. 26(1), 269–281 (2015). https://doi.org/10.1093/beheco/aru186 CrossRefPubMed

21.

E.C. Sullivan, K. Hinde, S.P. Mendoza, J.P. Capitanio, Cortisol concentrations in the milk of rhesus monkey mothers are associated with confident temperament in sons, but not daughters. Dev. Psychobiol. 53(1), 96–104 (2011). https://doi.org/10.1002/dev.20483 CrossRefPubMedPubMedCentral

22.

A. Catalani, P. Casolini, S. Scaccianoce, F.R. Patacchioli, P. Spinozzi, L. Angelucci, Maternal corticosterone during lactation permanently affects brain corticosteroid receptors, stress response and behaviour in rat progeny. Neuroscience 100(2), 319–325 (2000)CrossRef

23.

L.M. Glynn, E.P. Davis, C.D. Schetter, A. Chicz-Demet, C.J. Hobel, C.A. Sandman, Postnatal maternal cortisol levels predict temperament in healthy breastfed infants. Early Hum. Dev. 83(10), 675–681 (2007). https://doi.org/10.1016/j.earlhumdev.2007.01.003 CrossRefPubMed

24.

K.R. Grey, E.P. Davis, C.A. Sandman, L.M. Glynn, Human milk cortisol is associated with infant temperament. Psychoneuroendocrinology 38(7), 1178–1185 (2013). https://doi.org/10.1016/j.psyneuen.2012.11.002 CrossRefPubMed

25.

S. Hart, L.M. Boylan, B. Border, S.R. Carroll, D. McGunegle, R.M. Lampe, Breast milk levels of cortisol and secretory immunoglobulin A (SIgA) differ with maternal mood and infant neuro-behavioral functioning.Infant Behav Development 27(1), 101–106 (2004). https://doi.org/10.1016/j.infbeh.2003.06.002 CrossRef

26.

S. Nolvi, H.M. Uusitupa, D.J. Bridgett, H. Pesonen, A.K. Aatsinki, E.L. Kataja, R. Korja, H. Karlsson, L. Karlsson, Human milk cortisol concentration predicts experimentally induced infant fear reactivity: moderation by infant sex. Dev. Sci. 21(4), e12625 (2018). https://doi.org/10.1111/desc.12625 CrossRefPubMed

27.

B. van der Voorn, M. de Waard, J.B. van Goudoever, J. Rotteveel, A.C. Heijboer, M.J. Finken, Breast-milk cortisol and cortisone concentrations follow the diurnal rhythm of maternal hypothalamus-pituitary-adrenal axis activity. J. Nutr. 146(11), 2174–2179 (2016). https://doi.org/10.3945/jn.116.236349 CrossRefPubMed

28.

C. Hechler, R. Beijers, J.M. Riksen-Walraven, C. de Weerth, Are cortisol concentrations in human breast milk associated with infant crying? Dev. Psychobiol. 60(6), 639–650 (2018). https://doi.org/10.1002/dev.21761 CrossRefPubMedPubMedCentral

29.

T. Stalder, C. Kirschbaum, B.M. Kudielka, E.K. Adam, J.C. Pruessner, S. Wust, S. Dockray, N. Smyth, P. Evans, D.H. Hellhammer, R. Miller, M.A. Wetherell, S.J. Lupien, A. Clow, Assessment of the cortisol awakening response: expert consensus guidelines. Psychoneuroendocrinology 63, 414–432 (2016). https://doi.org/10.1016/j.psyneuen.2015.10.010 CrossRefPubMed

30.

C. Herrmann, International experiences with the hospital anxiety and depression scale–a review of validation data and clinical results. J. Psychosom. Res. 42(1), 17–41 (1997)CrossRef

31.

S.H. Parade, E.M. Leerkes, The reliability and validity of the infant behavior questionnaire-revised. Infant Behav. Dev. 31(4), 637–646 (2008). https://doi.org/10.1016/j.infbeh.2008.07.009 CrossRefPubMedPubMedCentral

32.

J. Worobey, V.M. Blajda, Temperament ratings at 2 weeks, 2 months, and 1 year—differential stability of activity and emotionality. Dev. Psychol. 25(2), 257–263 (1989). https://doi.org/10.1037/0012-1649.25.2.257 CrossRef

33.

M.K. Rothbart, Measurement of temperament in infancy. Child Dev. 52(2), 569–578 (1981). https://doi.org/10.1111/j.1467-8624.1981.tb03082.x CrossRef

34.

B. van der Voorn, F. Martens, N.S. Peppelman, J. Rotteveel, M.A. Blankenstein, M.J. Finken, A.C. Heijboer, Determination of cortisol and cortisone in human mother’s milk. Clin. Chim. Acta 444, 154–155 (2015). https://doi.org/10.1016/j.cca.2015.02.015 CrossRefPubMed

35.

J.C. Pruessner, C. Kirschbaum, G. Meinlschmid, D.H. Hellhammer, Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 28(7), 916–931 (2003)CrossRef

36.

B.E. Murphy, Ontogeny of cortisol-cortisone interconversion in human tissues: a role for cortisone in human fetal development. J. Steroid Biochem. 14(9), 811–817 (1981). https://doi.org/10.1016/0022-4731(81)90226-0 CrossRefPubMed

37.

M.A. Gartstein, G.R. Hancock, S.L. Iverson, Positive affectivity and fear trajectories in infancy: contributions of mother-child interaction factors. Child Dev. 89(5), 1519–1534 (2018). https://doi.org/10.1111/cdev.12843 CrossRefPubMed

38.

B.R. Kim, S.M. Chow, B. Bray, D.M. Teti, Trajectories of mothers’ emotional availability: relations with infant temperament in predicting attachment security. Attach Hum. Dev. 19(1), 38–57 (2017). https://doi.org/10.1080/14616734.2016.1252780 CrossRefPubMed

39.

H.H. Goldsmith, K.S. Lemery, K.A. Buss, J.J. Campos, Genetic analyses of focal aspects of infant temperament. Dev. Psychol. 35(4), 972–985 (1999)CrossRef

40.

A. Catalani, P. Casolini, G. Cigliana, S. Scaccianoce, C. Consoli, C. Cinque, A.R. Zuena, L. Angelucci, Maternal corticosterone influences behavior, stress response and corticosteroid receptors in the female rat. Pharm. Biochem. Behav. 73(1), 105–114 (2002)CrossRef

41.

T.A. Slotkin, F.J. Seidler, C.R. Wood, C. Lau, Development of glucocorticoid receptor regulation in the rat forebrain: implications for adverse effects of glucocorticoids in preterm infants. Brain Res. Bull. 76(5), 531–535 (2008). https://doi.org/10.1016/j.brainresbull.2008.03.002 CrossRefPubMed

42.

R.E. Smith, J.A. Maguire, A.N. Stein-Oakley, H. Sasano, K. Takahashi, K. Fukushima, Z.S. Krozowski, Localization of 11 beta-hydroxysteroid dehydrogenase type II in human epithelial tissues. J. Clin. Endocrinol. Metab. 81(9), 3244–3248 (1996). https://doi.org/10.1210/jcem.81.9.8784076 CrossRefPubMed

43.

J. Blair, J. Adaway, B. Keevil, R. Ross, Salivary cortisol and cortisone in the clinical setting. Curr. Opin. Endocrinol. Diabetes Obes. 24(3), 161–168 (2017). https://doi.org/10.1097/MED.0000000000000328 CrossRefPubMed

44.

Savas, M., Wester, V. L., de Rijke, Y. B., Rubinstein, G., Zopp, S., Dorst, K., van den Berg, S. A. A., Beuschlein, F., Feelders, R. A., Reincke, M., van Rossum, E. F. C. Hair glucocorticoids as biomarker for endogenous Cushing’s syndrome: validation in two independent cohorts. Neuroendocrinology (2019). https://doi.org/10.1159/000498886

45.

K.L. Watterberg, Adrenocortical function and dysfunction in the fetus and neonate. Semin Neonatol. 9(1), 13–21 (2004). https://doi.org/10.1016/j.siny.2003.08.003 CrossRefPubMed

46.

M.T. Ackermans, E. Endert, LC-MS/MS in endocrinology: what is the profit of the last 5 years? Bioanalysis 6(1), 43–57 (2014). https://doi.org/10.4155/bio.13.300 CrossRefPubMed

47.

A.A. Hane, N.A. Fox, C. Polak-Toste, M.M. Ghera, B.M. Guner, Contextual basis of maternal perceptions of infant temperament. Dev. Psychol. 42(6), 1077–1088 (2006). https://doi.org/10.1037/0012-1649.42.6.1077 CrossRefPubMed

48.

C. Reck, M. Muller, A. Tietz, E. Mohler, Infant distress to novelty is associated with maternal anxiety disorder and especially with maternal avoidance behavior. J. Anxiety Disord. 27(4), 404–412 (2013). https://doi.org/10.1016/j.janxdis.2013.03.009 CrossRefPubMed

49.

L. Tikotzky, A.S. Chambers, E. Gaylor, R. Manber, Maternal sleep and depressive symptoms: links with infant negative affectivity. Infant Behav. Dev. 33(4), 605–612 (2010). https://doi.org/10.1016/j.infbeh.2010.07.012 CrossRefPubMed

50.

M.A. Gartstein, M.K. Rothbart,, Studying infant temperament via the revised infant behavior questionnaire. Infant Behav. Dev. 26(1), 64–86 (2003). https://doi.org/10.1016/S0163-6383(02)00169-8 CrossRef

51.

M. Marysko, P. Finke, A. Wiebel, F. Resch, E. Moehler, Can mothers predict childhood behavioural inhibition in early infancy? Child Adol Mental Health 15(2), 91–96 (2010). https://doi.org/10.1111/j.1475-3588.2009.00539.x CrossRef

Title: Diurnal rhythmicity in breast-milk glucocorticoids, and infant behavior and sleep at age 3 months
Authors: Alyssa A. Toorop
Bibian van der Voorn
Jonneke J. Hollanders
Lisette R. Dijkstra
Koert M. Dolman
Annemieke C. Heijboer
Joost Rotteveel
Adriaan Honig
Martijn J. J. Finken
Publication date: 01-06-2020
Publisher: Springer US
Keyword: Glucocorticoid
Published in: Endocrine / Issue 3/2020
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI: https://doi.org/10.1007/s12020-020-02273-w

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

Illustration of figure on mountain summit/© Orapun / Stock.adobe.com, STEP AAG HeroTeaserCollection image/© Tarek / Generated with AI / Stock.adobe.com, ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 3/2020

Glucagon-like peptide-2 analog and inflammatory state in obese mice

The oral microbiome profile and biomarker in Chinese type 2 diabetes mellitus patients

Insulin resistance is related with liver fibrosis in type 2 diabetic patients with non-alcoholic fatty liver disease proven biopsy and Mediterranean diet pattern as a protective factor

Endocrine surgery during COVID-19 pandemic: do we need an update of indications in Italy?

Interaction effect of obesity and thyroid autoimmunity on the prevalence of hyperthyrotropinaemia

The role of AIP variants in pituitary adenomas and concomitant thyroid carcinomas in the Netherlands: a nationwide pathology registry (PALGA) study

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

Highlights from the ACC 2024 Congress

ACC 2024 Congress Coverage