Maternal cortisol during pregnancy is related to infant cardiac vagal control

Psychoneuroendocrinology

Volumn 54, Issue , 2015, Pages 78-89

  Rash, Joshua A ^a   Campbell, Tavis S ^a   Letourneau, Nicole ^b   Giesbrecht, Gerald F ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Cardiac vagal control; Cortisol; Depressed mood; Fetal programming; Respiratory sinus arrhythmia

Indexed keywords

HYDROCORTISONE;

ADULT; ARTICLE; CARDIAC VAGAL CONTROL; CIRCADIAN RHYTHM; FEMALE; GESTATIONAL AGE; HORMONE DETERMINATION; HUMAN; INFANT; NEUROMODULATION; PREGNANCY; PRIORITY JOURNAL; PUERPERAL DEPRESSION; RESPIRATORY SINUS ARRHYTHMIA; SALIVA ANALYSIS; AORTA CHEMORECEPTOR; DEPRESSION; HEART; INNERVATION; MENTAL STRESS; METABOLISM; PHYSIOLOGY; PREGNANCY COMPLICATION; PRENATAL EXPOSURE; PSYCHOLOGY; SALIVA;

ADULT; AORTIC BODIES; DEPRESSION; FEMALE; HEART; HUMANS; HYDROCORTISONE; INFANT; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; RESPIRATORY SINUS ARRHYTHMIA; SALIVA; STRESS, PSYCHOLOGICAL;

EID: 84924443929     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2015.01.024     Document Type: Article

References (73)

1. Allister L., Lester B.M., Carr S., Liu J. The effects of maternal depression on fetal heart rate response to vibroacoustic stimulation. Dev. Neuropsychol. 2001, 20:639-651.
2. Antonow-Schlorke I., Helgert A., Gey C., Coksaygan T., Schubert H., Nathanielsz P.W., Witte O.W., Schwab M. Adverse effects of antenatal glucocorticoids on cerebral myelination in sheep. Obstet. Gynecol. 2009, 113:142-151.
3. Bar-Haim Y., Marshall P.J., Fox N.A. Developmental changes in heart period and high-frequency heart period variability from 4 months to 4 years of age. Dev. Psychobiol. 2000, 37:44-56.
4. Barker D.J. Fetal programming of coronary heart disease. Trends Endocrinol. Metab. 2002, 13:364-368.
5. Beauchaine T. Vagal tone, development, and gray's motivational theory: toward an integrated model of autonomic nervous system functioning in psychopathology. Dev. Psychopathol. 2001, 13:183-214.
6. Benarroch E.E. The central autonomic network: functional organization, dysfunction, and perspective. Mayo Clin. Proc. 1993, 68:988-1001.
7. Bergman K., Sarkar P., O'Connor T.G., Modi N., Glover V. Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. J. Am. Acad. Child Adolesc. Psychiatry 2007, 46:1454-1463.
8. Berntson G.G., Quigley K.S., Jang J.F., Boysen S.T. An approach to artifact identification: application to heart period data. Psychophysiology 1990, 27:586-598.
9. Braun T., Challis J.R., Newnham J.P., Sloboda D.M. Early-life glucocorticoid exposure: the hypothalamic-pituitary-adrenal axis, placental function, and long-term disease risk. Endocr. Rev. 2013, 34:885-916.
10. Brazelton T.B., Nugent J.K. Neonatal Behavioral Assessment Scale 1995, Cambridge University Press, Cambridge.
11. Calkins K., Devaskar S.U. Fetal origins of adult disease. Curr. Probl. Pediatr. Adolesc. Health Care 2011, 41:158-176.
12. Cox J.L., Holden J., Sagovsky R. Detection of postnatal depression. Development of the 10-item Edinburgh Postnatal Depression Scale. Br. J. Psychiatry 1987, 150:782-786.
13. Davis E., Townsend E., Gunnar M., Guiang S., Lussky R., Cifuentes R., Georgieff M. Antenatal betamethasone treatment has a persisting influence on infant HPA axis regulation. J. Perinatol. 2006, 26:147-153.
14. Davis E.P., Glynn L.M., Schetter C.D., Hobel C., Chicz-Demet A., Sandman C.A. Prenatal exposure to maternal depression and cortisol influences infant temperament. J. Am. Acad. Child Adolesc. Psychiatry 2007, 46:737-746.
15. Davis E.P., Sandman C.A. The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Dev. 2010, 81:131-148.
16. Davis E.P., Sandman C.A., Buss C., Wing D.A., Head K. Fetal glucocorticoid exposure is associated with preadolescent brain development. Biol. Psychiatry 2013, 74:647-655.
17. Del Giudice M., Ellis B.J., Shirtcliff E.A. The adaptive calibration model of stress responsivity. Neurosci. Biobehav. Rev. 2011, 35(7):1562-1592.
18. Diego M.A., Field T., Hernandez-Reif M., Schanberg S., Kuhn C., Gonzalez-Quintero V.H. Prenatal depression restricts fetal growth. Early Hum. Dev, 2009, 85:65-70.
19. Dierckx B., Tulen J.H., van den Berg M.P., Tharner A., Jaddoe V.W., Moll H.A., Hofman A., Verhulst F.C., Tiemeier H. Maternal psychopathology influences infant heart rate variability: generation R Study. Psychosom. Med. 2009, 71:313-321.
20. Fekedulegn D.B., Andrew M.E., Burchfiel C.M., Violanti J.M., Hartley T.A., Charles L.E., Miller D.B. Area under the curve and other summary indicators of repeated waking cortisol measurements. Psychosom. Med. 2007, 69:651-659.
21. Feldman R., Eidelman A.I. Skin-to-skin contact (Kangaroo Care) accelerates autonomic and neurobehavioural maturation in preterm infants. Dev. Med. Child Neurol. 2003, 45:274-281.
22. Feldman R., Rosenthal Z., Eidelman A.I. Maternal-preterm skin-to-skin contact enhances child physiologic organization and cognitive control across the first 10 years of life. Biol. Psychiatry 2014, 75:56-64.
23. Fernandes M., Stein A., Srinivasan K., Menezes G., Ramchandani P. Foetal exposure C rural South India. Child Care Health Dev. 2014.
24. Field T. Prenatal depression effects on early development: a review. Infant Behav. Dev. 2011, 34:1-14.
25. Field T., Diego M., Dieter J., Hernandez-Reif M., Schanberg S., Kuhn C., Yando R., Bendell D. Prenatal depression effects on the fetus and the newborn. Infant Behav. Dev. 2004, 27:216-229.
26. Field T., Diego M., Hernandez-Reif M., Vera Y., Gil K., Schanberg S., Kuhn C., Gonzalez-Garcia A. Prenatal maternal biochemistry predicts neonatal biochemistry. Int. J. Neurosci. 2004, 114:933-945.
27. Field T., Diego M., Hernandez-Reif M., Schanberg S., Kuhn C., Yando R., Bendell D. Pregnancy anxiety and comorbid depression and anger: effects on the fetus and neonate. Depress. Anxiety 2003, 17:140-151.
28. Field T., Pickens J., Fox N.A., Nawrocki T., Gonzalez J. Vagal tone in infants of depressed mothers. Dev. Psychopathol. 1995, 7:227-231.
29. Fries E., Dettenborn L., Kirschbaum C. The cortisol awakening response (CAR): facts and future directions. Int. J. Psychophysiol. 2009, 72:67-73.
30. Glover V. Annual research review: prenatal stress and the origins of psychopathology: an evolutionary perspective. J. Child Psychol. Psychiatry 2011, 52:356-367.
31. Goldsmith H., Rothbart M. Prelocomotor and Locomotor Laboratory Temperament Assessment Battery (Lab-TAB; Version 3.1, Technical Manual) 1996, University of Wisconsin, Department of Psychology, Madison.
32. Graziano P., Derefinko K. Cardiac vagal control and children's adaptive functioning: a meta-analysis. Biol. Psychol. 2013, 94:22-37.
33. Grossman P., Taylor E.W. Toward understanding respiratory sinus arrhythmia: relations to cardiac vagal tone, evolution and biobehavioral functions. Biol. Psychol. 2007, 74:263-285.
34. Grote N.K., Bridge J.A., Gavin A.R., Melville J.L., Iyengar S., Katon W.J. A meta-analysis of depression during pregnancy and the risk of preterm birth, low birth weight, and intrauterine growth restriction. Arch. Gen. Psychiatry 2010, 67:1012-1024.
35. Harris A., Seckl J. Glucocorticoids, prenatal stress and the programming of disease. Horm. Behav. 2011, 59:279-289.
36. Hayes L.J., Goodman S.H., Carlson E. Maternal antenatal depression and infant disorganized attachment at 12 months. Attachment Hum. Dev. 2013, 15:133-153.
37. Hinnant J.B., El-Sheikh M. Codevelopment of externalizing and internalizing symptoms in middle to late childhood: Sex, baseline respiratory sinus arrhythmia, and respiratory sinus arrhythmia reactivity as predictors. Dev. Psychopathol. 2013, 25(2):419-436.
38. Holochwost S.J., Gariépy J.L., Propper C.B., Mills-Koonce W.R., Moore G.A. Parenting behaviors and vagal tone at six months predict attachment disorganization at twelve months. Dev. Psychobiol. 2014, 56:1423-1430.
39. Jomeen J., Martin C. Replicability and stability of the multidimensional model of the Edinburgh Postnatal Depression Scale in late pregnancy. J. Psychiatr. Mental Health Nurs. 2007, 14:319-324.
40. Kajantie E. Fetal origins of stress-related adult disease. Ann. N.Y. Acad. Sci. 2006, 1083:11-27.
41. Kapoor A., Matthews S.G. Prenatal stress modifies behavior and hypothalamic-pituitary-adrenal function in female guinea pig offspring: effects of timing of prenatal stress and stage of reproductive cycle. Endocrinology 2008, 149:6406-6415.
42. Kapoor A., Petropoulos S., Matthews S.G. Fetal programming of hypothalamic-pituitary-adrenal (HPA) axis function and behavior by synthetic glucocorticoids. Brain Res. Rev. 2008, 57:586-595.
43. Kemp A.H., Quintana D.S., Gray M.A., Felmingham K.L., Brown K., Gatt J.M. Impact of depression and antidepressant treatment on heart rate variability: a review and meta-analysis. Biol. Psychiatry 2010, 67:1067-1074.
44. Kivlighan K.T., Granger D.A., Schwartz E.B., Nelson V., Curran M., Shirtcliff E.A. Quantifying blood leakage into the oral mucosa and its effects on the measurement of cortisol, dehydroepiandrosterone, and testosterone in saliva. Horm. Behav. 2004, 46:39-46.
45. Liew J., Eisenberg N., Spinrad T.L., Eggum N.D., Haugen R., Kupfer A., Reiser M.R., Smith C.L., Lemery-Chalfant K., Baham M.E. Physiological regulation and fearfulness as predictors of young children's empathy-related reactions. Soc. Dev. 2011, 20:111-134.
46. Little R.J., Rubin D.B. Statistical Analysis with Missing Data. Wiley Series in Probability and Statistics 2002, 1. Wiley, New York, NY. second ed. R.J.A. Little, D.B. Rubin (Eds.).
47. Lundy B.L., Jones N.A., Field T., Nearing G., Davalos M., Pietro P.A., Schanberg S., Kuhn C. Prenatal depression effects on neonates. Infant Behav. Dev. 1999, 22:119-129.
48. Lunshof M.S., Boer K., Wolf H., Koppen S., Velderman J.K., Mulder E.J. Short-term (0-48h) effects of maternal betamethasone administration on fetal heart rate and its variability. Pediatric Res. 2005, 57:545-549.
49. Maccari S., Morley-Fletcher S. Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 2007, 32:S10-S15.
50. Monk C., Sloan R.P., Myers M.M., Ellman L., Werner E., Jeon J., Tager F., Fifer W.P. Fetal heart rate reactivity differs by women's psychiatric status: an early marker for developmental risk?. J. Am. Acad. Child Adolesc. Psychiatry 2004, 43:283-290.
51. Moore K.L., Persaud T.V.N., Torchia M.G., Persaud T. The Developing Human: Clinically Oriented Embryology 2008, Saunders/Elsevier, Philadelphia.
52. Oberlander T.F., Weinberg J., Papsdorf M., Grunau R., Misri S., Devlin A.M. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008, 3:97-106.
53. Okun M.L., Krafty R.T., Buysse D.J., Monk T.H., Reynolds C.F., Begley A., Hall M. What constitutes too long of a delay? Determining the cortisol awakening response (CAR) using self-report and PSG-assessed wake time. Psychoneuroendocrinology 2010, 35:460-468.
54. Ponirakis A., Susman E.J., Stifter C.A. Negative emotionality and cortisol during adolescent pregnancy and its effects on infant health and autonomic nervous system reactivity. Dev. Psychobiol. 1998, 33:163-174.
55. Porges S.W. The polyvagal perspective. Biol. Psychol. 2007, 74:116-143.
56. Porges S.W., Furman S.A. The early development of the autonomic nervous system provides a neural platform for social behaviour: a polyvagal perspective. Infant Child Dev. 2011, 20:106-118.
57. Pruessner J.C., Kirschbaum C., Meinlschmid G., Hellhammer D.H. Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 2003, 28:916-931.
58. Rottenberg J. Cardiac vagal control in depression: a critical analysis. Biol. Psychol. 2007, 74:200-211.
59. Salaria S., Chana G., Caldara F., Feltrin E., Altieri M., Faggioni F., Domenici E., Merlo-Pich E., Everall I. Microarray analysis of cultured human brain aggregates following cortisol exposure: implications for cellular functions relevant to mood disorders. Neurobiol. Dis. 2006, 23:630-636.
60. Sánchez M.M., Young L.J., Plotsky P.M., Insel T.R. Distribution of corticosteroid receptors in the rhesus brain: relative absence of glucocorticoid receptors in the hippocampal formation. J. Neurosci. 2000, 20:4657-4668.
61. Sarkar S., Tsai S.-W., Nguyen T.T., Plevyak M., Padbury J.F., Rubin L.P. Inhibition of placental 11β-hydroxysteroid dehydrogenase type 2 by catecholamines via α-adrenergic signaling. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 281:R1966-R1974.
62. Schneider U., Fiedler A., Schröder B., Jaekel S., Stacke A., Hoyer D., Schleussner E. The effect of antenatal steroid treatment on fetal autonomic heart rate regulation revealed by fetal magnetocardiography (fMCG). Early Hum. Dev. 2010, 86:319-325.
63. Seckl J.R., Holmes M.C. Mechanisms of disease: glucocorticoids, their placental metabolism and fetal'programming'of adult pathophysiology. Nat. Clin. Pract. Endocrinol. Metab. 2007, 3:479-488.
64. Senat M., Minoui S., Multon O., Fernandez H., Frydman R., Ville Y. Effect of dexamethasone and betamethasone on fetal heart rate variability in preterm labour: a randomised study. BJOG: An Int. J. Obstet. Gynaecol. 1998, 105:749-755.
65. Staton L., El-Sheikh M., Buckhalt J.A. Respiratory sinus arrhythmia and cognitive functioning in children. Dev. Psychobiol. 2009, 51:249-258.
66. Tabachnick B., Fidell L. Using Multivariate Statistics 2012, Pearson. International ed.
67. Taylor Z.E., Eisenberg N., Spinrad T.L. Respiratory Sinus Arrhythmia, Effortful Control, and Parenting as Predictors of Children's Sympathy Across Early Childhood. Dev. Psychol. 2015, 51(1):17-25.
68. Thayer J.F., Hansen A.L., Psychol E.S.-R.C., Johnsen B.H. Heart rate variability, prefrontal neural function, and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Ann. Behav. Med. 2009, 37:141-153.
69. Thayer J.F., Lane R.D. A model of neurovisceral integration in emotion regulation and dysregulation. J. Affect. Disord. 2000, 61:201-216.
70. Thayer J.F., Lane R.D. The role of vagal function in the risk for cardiovascular disease and mortality. Biol. Psychol. 2007, 74:224-242.
71. Van den Bergh B.R. Developmental programming of early brain and behaviour development and mental health: a conceptual framework. Dev. Med. Child Neurol. 2011, 53:19-23.
72. van der Wal M.F., van Eijsden M., Bonsel G.J. Stress and emotional problems during pregnancy and excessive infant crying. J. Dev. Behav. Pediatr. 2007, 28:431-437.
73. Yaroslavsky I., Rottenberg J., Kovacs M. Atypical patterns of respiratory sinus arrhythmia index an endophenotype for depression. Dev. Psychopathol. 2014, 26:1337-1352.