Neonatal Pain-Related Stress and NFKBIA Genotype Are Associated with Altered Cortisol Levels in Preterm Boys at School Age

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Grunau, Ruth E ^a,b   Cepeda, Ivan L ^b   Chau, Cecil M Y ^b   Brummelte, Susanne ^a,b   Weinberg, Joanne ^a,b   Lavoie, Pascal M ^a,b   Ladd, Mihoko ^a,b   Hirschfeld, Aaron F ^a,b   Russell, Evan ^c   Koren, Gideon ^c   Van Uum, Stan ^c   Brant, Rollin ^a,b   Turvey, Stuart E ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; CYTOSINE; HYDROCORTISONE; THYMINE;

ALLELE; ARTICLE; CELL ACTIVATION; CHILD; COGNITIVE DEFECT; CONTROLLED STUDY; CYTOKINE RELEASE; DERMATOLOGICAL PROCEDURE; DOWN REGULATION; FEMALE; GENE; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; GESTATIONAL AGE; HAIR LEVEL; HORMONE RESPONSE; HUMAN; HYDROCORTISONE HAIR LEVEL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INFLAMMATION; LIFE STRESS; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MEDICAL PARAMETERS; MOTOR DYSFUNCTION; NEWBORN DISEASE; NFKBIA GENE; PAIN; PREMATURITY; PROMOTER REGION; SCHOOL CHILD; SENSORY DYSFUNCTION;

CHILD; GENOTYPE; HUMANS; HYDROCORTISONE; I-KAPPA B PROTEINS; INFANT, NEWBORN; MALE; PAIN; STRESS, PHYSIOLOGICAL;

EID: 84884184762     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073926     Document Type: Article

References (64)

1. Koenig JI, Walker CD, Romeo RD, Lupien SJ (2011) Stress. 14: 475-80. Effects of stress across the lifespan.
2. Matthews SG, (2002) Early programming of the hypothalamo-pituitary-adrenal axis. Trends Endocrinol Metab 13: 373-380.
3. Welberg LAM, Seckl JR, (2001) Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 13: 113-128.
4. Khulan B, Drake AJ, (2012) Glucocorticoids as mediators of developmental programming effects. Best Pract Res Clin Endocrinol Metab 26: 689-700.
5. Meaney MJ, (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Ann Rev Neuroscience 24: 1161-1192.
6. Tyrka AR, Wier L, Price LH, Ross N, Anderson GM, et al. (2008) Childhood parental loss and adult hypothalamic-pituitary-adrenal function. Biol Psychiatry 63: 1147-1154.
7. Pesonen AK, Raikkonen K, Feldt K, Heinonen K, Osmond C, et al. (2010) Childhood separation experience predicts HPA axis hormonal responses in late adulthood: a natural experiment of World War II. Psychoneuroendocrinology 35: 758-767.
8. Grunau RE, Haley DW, Whitfield MF, Weinberg J, Yu W, et al. (2007) Altered basal cortisol levels at 3, 6, 8 and 18 months in preterm infants born extremely low gestational age. J Pediatr 150: 151-156.
9. Miller GE, Chen E, Parker KJ, (2011) Psychological stress in childhood and susceptibility to the chronic diseases of aging: Moving toward a model of behavioral and biological mechanisms. Psychol Bull 137: 959-997.
10. Grunau RE, Weinberg J, Whitfield MF, (2004) Neonatal procedural pain and preterm infant cortisol response to novelty at 8 months. Pediatrics 114: e77-84.
11. Padett DA, Glaser R, (2003) How stress influences the immune response. Trends Immunol 24: 444-448.
12. Miller AH, Maletic V, Raison CL, (2009) Inflammation and its discontents: The role of cytokines in the pathophysiology of major depression. Biol Psychiatry 65: 732-741.
13. Hingre RV, Gross SJ, Hingre D, Mayes DM, Richman RA, (1994) Adrenal steroidogenesis in very low birth weight preterm infants. J Clin Endocrinol Metab 78: 266-270.
14. Korte C, Styne D, Merritt TA, Mayes D, Wertz A, et al. (1996) Adrenocortical function in the very low birth weight infant: Improved testing sensitivity and association with neonatal outcome. J Pediatr 128: 257-263.
15. Jett PL, Samuels MH, McDaniel PA, Benda GI, LaFranchi SH, et al. (1997) Variability of plasma cortisol levels in extremely low birth weight infants. J Clin Endocrinol Metab 82: 2921-2925.
16. Grunau RE, Holsti L, Haley DW, Oberlander T, Weinberg J, et al. (2005) Neonatal procedural pain exposure predicts lower cortisol and behavioral reactivity in preterm infants in the NICU. Pain 113: 293-300.
17. Lupien SJ, McEwen BS, Gunnar MR, Heim C, (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10: 434-445.
18. Joëls M, (2011) Impact of glucocorticoids on brain function: relevance for mood disorders. Psychoneuroendocrinology 36: 406-414.
19. Fietta P, Fietta P, Delsante G, (2009) Central nervous system effects of natural and synthetic glucocorticoids. Psychiatry Clin Neurosci 63: 613-622.
20. Molina PE (2010) Adrenal gland. In: Molina PE, editor. Endocrine Physiology, 3rd ed. New York: McGraw-Hill.
21. Miller GE, Chen E, (2010) Harsh family climate in early life presages the emergence of a proinflammatory phenotype in adolescence. Psychol Sci 21: 848-56.
22. LaPrairie JL, Murphy AZ, (2010) Long-term impact of neonatal injury in male and female rats: Sex differences, mechanisms and clinical implications. Front Neuroendocrinol. 31(2): 193-202.
23. Dougherty LR, Smith VC, Olino TM, Dyson MW, Bufferd SJ, et al. (2013) Maternal psychopathology and early child temperament predict young children's salivary cortisol 3 years later. J Abnormal Child Psych, 41(4), 531-542.
24. Hayden MS, Ghosh S, (2008) Shared principles in NF-kappaB signaling. Cell 132: 344-362.
25. Lynn DJ, Winsor GL, Chan C, Richard N, Laird MR, et al. (2008) InnateDB: facilitating systems-level analyses of the mammalian innate immune response. Mol Syst Biol 4: 218 doi:10.1038/msb.2008.55.
26. Niederberger E, Geisslinger G, (2008) The IKK-NF-kappaB pathway: a source for novel molecular drug targets in pain therapy? Faseb J 22: 3432-3442.
27. Bonizzi G, Karin M, (2004) The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25: 280-288.
28. Ali S, Hirschfeld AF, Mayer ML, Fortuno ES, Corbett N, et al. (2013) Functional genetic variation in NFKBIA and susceptibility to childhood asthma, bronchiolitis and bronchopulmonary dysplasia. J. Immunol. Published online March 13, 2013, doi:10.4049/jimmunol.1201015.
29. Van Uum SH, Sauvé B, Fraser LA, Morley-Forster P, Paul TL, et al. (2008) Elevated content of cortisol in hair of patients with severe chronic pain: a novel biomarker for stress. Stress 11: 483-488.
30. Vaghri Z, Guhn M, Weinberg J, Grunau RE, Yu W, et al. (2013) Hair cortisol reflects socio-economic factors and hair zinc in preschoolers. Psychoneuroendocrinology 38(3): 331-340.
31. Meyer JS, Novak MA, (2012) Hair cortisol: a novel biomarker of hypothalamic-pituitary-adrenocortical activity. Endocrinology 153: 4120-4127.
32. Holsti L, Grunau RE, Whitfield MF, Oberlander MF, Lindh V, (2006) Behavioral responses to pain are heightened after clustered care in preterm infants born between 30 and 32 weeks gestational age. Clin J Pain 2006: 757-764.
33. Grunau RE, Holsti L, Whitfield MF, Ling E, (2000) Are twitches, startles, and body movements pain indicators in extremely low birth weight infants? Clin J Pain 16: 37-45.
34. Grunau RE, Oberlander TF, Whitfield MF, Fitzgerald C, Lee SK, (2001) Demographic and therapeutic determinants of pain reactivity in very low birth weight neonates at 32 weeks' postconceptional age. Pediatrics 107: 105-112.
35. Fitzgerald M, (2005) The development of nociceptive circuits. Nat Rev Neurosci 6: 507-520.
36. Grunau RE, Whitfield MF, Petrie-Thomas J, Synnes AR, Cepeda IL, et al. (2009) Neonatal pain, parenting stress and interaction, in relation to cognitive and motor development at 8 and 18 months in preterm infants. Pain 143: 138-146.
37. Sauvé B, Koren G, Walsh G, Tokmakejian S, Van Uum SH, (2007) Measurement of cortisol in human hair as a biomarker of systemic exposure. Clin Invest Med 30: E183-E191.
38. Beck AT, Steer RA, Brown GK (1996) Manual for the Beck Depression Inventory, Second Edition (BDI-II). San Antonio, TX: The Psychological Association.
39. Spielberger CD, Gorsuch RL, Lushene RE (1970) Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press.
40. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0.
41. Hoenig JM, Heise DM, (2001) The abuse of power: The pervasive fallacy of power calculations in data analysis. The American Statistician 55: 19-24.
42. Tukey JW (1977): Exploratory Data Analysis. Don Mills, ON: Addison-Wesley.
43. Carpenter LL, Carvalho JP, Tyrka AR, Wier LM, Mello AF, et al. (2007) Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment. Biol psychiatry 62: 1080-1087.
44. Miller GE, Chen E, Zhou ES, (2007) If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychol Bull 133: 25-45.
45. Kajantie E, Phillips DI, Andersson S, Barker DJ, Dunkel L, et al. (2002) Size at birth, gestational age and cortisol secretion in adult life: Foetal programming of both hyper- and hypocortisolism? Clin Endocrinol (Oxf) 57: 635-641.
46. Sharpley CF, McFarlane JR, Slominski A, (2011) Stress-linked cortisol concentrations in hair: What we know and what we need to know. Rev Neurosci 23: 111-121.
47. Pervanidou P, Chrousos GP, (2012) Metabolic consequences of stress during childhood and adolescent. Metabolism 61: 611-619.
48. Buske-Kirschbaum A, Krieger S, Wilkes C, Rauh W, Weiss S, et al. (2007) Hypothalamic-pituitary-adrenal axis function and the cellular immune response in former preterm children. J Clin Endocrinol Metab 92: 3429-3435.
49. Bierhaus A, Wolf J, Andrassy M, Rohleder N, Humpert PM, et al. (2003) A mechanism converting psychosocial stress into mononuclear cell activation. Proc Natl Acad Sci U S A 100: 1920-1925.
50. Miller GE, Chen E, Fok AK, Walker H, Lim A, et al. (2009) Low early-life social class leaves a biological residue manifested by decreased glucocorticoid and increased proinflammatory signaling. Proc Natl Acad Sci USA 106: 14716-14721.
51. Zhang GL, Zou YF, Feng XL, Shi HJ, Du XF, et al. (2011) Association of the NFKBIA gene polymorphisms with susceptibility to autoimmune and inflammatory diseases: a meta-analysis. Inflam Res 60: 11-8.
52. Gene Regulation, BIOBASE Biological Databases. Available: http://www.gene-regulation.com. Accessed 2012 Nov 15 and TFSEARCH Transcriptional Factor Search. Available: http://www.cbrc.jp/research/db/TFSEARCH.html. Accessed 2012 Nov 15. Bioinformatics tools used to analyze the NFKBIA promoter for putative transcription factor binding sites.
53. Brüggemeier U, Kalff M, Franke S, Scheidereit C, Beato M, (1991) Ubiquitous transcription factor OTF-1 mediates induction of the MMTV promoter through synergistic interaction with hormone receptors. Cell 64: 565-572.
54. Darnaudery M, Maccari S, (2008) Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57: 571-585.
55. Viveros MP, Llorente R, Lopez-Gallardo M, Suarez J, Bermudez-Silva F, et al. (2009) Sex-dependent alterations in response to maternal deprivation in rats. Psychoneuroendocrinology 34: S217-S226.
56. Kaiser S, Sachser N, (2005) The effects of prenatal social stress on behaviour: mechanisms and function. Neurosci Biobehav Rev 29: 283-294.
57. Mueller BR, Bale TL, (2008) Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28: 9055-9065.
58. Llorente R, Miguel-Blanco C, Aisa B, Lachize S, Borcel E, et al. (2011) Long term sex-dependent psychoneuroendocrine effects of maternal deprivation and juvenile unpredictable stress in rats. J Neuroendocrinol 23: 329-344.
59. Weinstock M, (2007) Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 32: 1730-1740.
60. McCormick CM, Smythe JW, Sharma S, Meaney MJ, (1995) Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res Dev Brain Res 84: 55-61.
61. Bale TL, (2011) Sex differences in prenatal epigenetic programming of stress pathways. Stress 14: 348-356.
62. Jones A, Godfrey KM, Wood P, Osmond C, Goulden P, et al. (2006) Fetal growth and the adrenocortical response to psychological stress. J Clin Endocrinol Metab 91: 1868-1871.
63. Elzinga BM, Roelofs K, Tollenaar MS, Bakvis P, van Pelt J, et al. (2008) Diminished cortisol responses to psychosocial stress associated with lifetime adverse events a study among healthy young subjects. Psychoneuroendocrinology 33: 227-237.
64. Kajantie E, Raikkonen K, (2010) Early life predictors of the physiological stress response later in life. Neurosci Biobehav Rev 35: 23-32.