A review of rhythm and responsiveness of cortisol in individuals with autism spectrum disorders

Psychoneuroendocrinology

Volumn 49, Issue 1, 2014, Pages 207-228

  Taylor, Julie Lounds ^a,b   Corbett, Blythe A ^a,b  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Autism spectrum disorder; Circadian; Cortisol; Diurnal; Hormones; HPA axis; Responsiveness; Rhythm; Social; Variability

Indexed keywords

HYDROCORTISONE; PSYCHOTROPIC AGENT; BIOLOGICAL MARKER;

ANTICIPATION; ARTICLE; ASPERGER SYNDROME; AUTISM; CIRCADIAN RHYTHM; COHORT ANALYSIS; COMORBIDITY; CORTISOL AWAKENING RESPONSE; DEVELOPMENTAL STAGE; DISEASE SEVERITY; DRUG USE; ENVIRONMENTAL STRESS; HORMONE METABOLISM; HORMONE RESPONSE; HUMAN; HYDROCORTISONE BLOOD LEVEL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INTELLIGENCE QUOTIENT; LIFESPAN; MENTAL STRESS; PSYCHOSOCIAL ENVIRONMENT; SAMPLE SIZE; SEX DIFFERENCE; SOCIAL STRESS; THREAT; AGE; CHILD DEVELOPMENT DISORDERS, PERVASIVE; COMPLICATION; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MENTAL DISEASE; METABOLISM; PHYSIOLOGY; SEXUAL DEVELOPMENT; WAKEFULNESS;

AGE FACTORS; BIOMARKERS; CHILD DEVELOPMENT DISORDERS, PERVASIVE; CIRCADIAN RHYTHM; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MENTAL DISORDERS; PITUITARY-ADRENAL SYSTEM; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL; WAKEFULNESS;

EID: 84909995262     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.07.015     Document Type: Article

References (94)

1. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders: DSM-IV 1994, American Psychiatric Association, Washington, DC. fourth ed.
2. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR 2000, American Psychiatric Association, Washington, DC. fourth ed. (text rev.).
3. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders: DSM-5 2013, American Psychiatric Association, Arlington, VA. fifth ed.
4. Angold A. Adolescent depression, corisol, and DHEA. Psychol. Med. 2003, 33:573-581.
5. Ashwood P., Corbett B.A., Kantor A., Schulman H., Van de Water J., Amaral D.G. In search of cellular immunophenotypes in the blood of children with autism. PLoS One 2011, 6. 10.1371/journal.pone.0019299.
6. Ben-Sasson A., Hen L., Fluss R., Cermak S.A., Engel-Yeger B., Gal E. A meta-analysis of sensory modulation symptoms in individuals with autism spectrum disorders. J. Autism Dev. Disord. 2009, 39:1-11.
7. Bitsika V., Sharpley C.F., Sweeney J.A., McFarlane J.R. HPA and SAM axis responses as correlates of self- vs parental ratings of anxiety in boys with an autistic disorder. Physiol. Behav. 2014, 127:1-7.
8. Bradley E.A., Summers J.A., Wood H.L., Bryson S.E. Comparing rates of psychiatric and behavior disorders in adolescents and young adults with severe intellectual disability with and without autism. J. Autism Dev. Disord. 2004, 34:151-161.
9. Brosnan M., Turner-Cobb J., Munro-Naan Z., Jessop D. Absence of a normal cortisol awakening response (CAR) in adolescent males with Asperger syndrome (AS). Psychoneuroendocrinology 2009, 34:1095-1100.
10. Buske-Kirschbaum A., Jobst S., Wustmans A., Kirschbaum C. Attenuated free cortisol response to psychosocial stress in children with atopic dermatitis. Psychosom. Med. 1997, 59:419-426.
11. Centers for Disease Control and Prevention Prevalence of autism spectrum disorders-Autism and Developmental Disabilities Monitoring Network, United States, 2008. Morb. Mortal. Wkly. Rep. 2012, 61:1-51.
12. Corbett B.A., Mendoza S., Abdullah M., Wegelin J.A., Levine S. Cortisol circadian rhythms and response to stress in children with autism. Psychoneuroendocrinology 2006, 31:59-68.
13. Corbett B.A., Mendoza S., Wegelin J.A., Carmean V., Levine S. Variable cortisol circadian rhythms in children with autism and anticipatory stress. J. Psychiatry Neurosci. 2008, 33:227-234.
14. Corbett B.A., Sharp F.R., Kantor A.B., Schulman H., Walker W., Lit L., Ashwood P., Rocke D. Complement and Apolipoproteins identified in serum of children with autism: a proteomics study. Mol. Psychiatr. 2007, 12:292-306.
15. Corbett B.A., Schupp C.W. The cortisol awakening response (CAR) in male children with autism spectrum disorder. Horm. Behav. 2014, 65(4):345-350.
16. Corbett B.A., Schupp C.W., Lanni K.E. Comparing biobehavioral profiles across two social stress paradigms in children with and without autism spectrum disorders. Mol. Autism 2012, 3:13.
17. Corbett B.A., Schupp C.W., Levine S., Mendoza S. Comparing cortisol, stress, and sensory sensitivity in children with autism. Autism Res. 2009, 2:39-49.
18. Corbett B.A., Schupp C.W., Simon D., Ryan N., Mendoza S. Elevated cortisol during play is associated with age and social engagement in children with autism. Mol. Autism 2010, 1:13.
19. Corbett B.A., Swain D.M., Newsom C., Wang L., Song Y., Edgerton D. Biobehavioral profiles of arousal and social motivation in autism specrtum disorders. J. Child Psychol. Psychiatry 2013, 10.1111/jcpp.12184.
20. Curin J.M., Terzić J., Petković Z.B., Zekan L., Terzić I.M., Šušnjara I.M. Lower cortisol and higher ACTH levels in individuals with autism. J. Autism Dev. Disord. 2003, 33:443-448.
21. Cushing H. Further notes on pituitary basophilism. J. Am. Med. Assoc. 1932, 99:281-284.
22. Dahl R.E., Ryan N.D., Puig-Antich J., Nguyen N.A., al-Shabbout M., Meyer V.A., et al. 24-hour cortisol measures in adolescents with major depression: a controlled study. Biol. Psychiatry 1991, 30:25-36.
23. Derijk R., Sternberg E.M. Corticosteroid action and neuroendocrine-immune interactions. Ann. N.Y. Acad. Sci. 1994, 746:33-41.
24. Dickerson S.S., Kemeny M.E. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol. Bull. 2004, 130:355-391.
25. Doane L.D., Mineka S., Zinbarg R.E., Craske M., Griffith J.W., Adam E.K. Are flatter diurnal cortisol rhythms associated with major depression and anxiety disorders in late adolescence? The role of life stress and daily negative emotion. Dev. Psychopathol. 2013, 25:629-642.
26. Eaves L.C., Ho H.H. Young adult outcome of autism spectrum disorders. J. Autism Dev. Disord. 2008, 38:739-747.
27. Engert V., Efanov S.I., Dedovic K., Dagher A., Pruessner J.C. Increased cortisol awakening response and afternoon/evening cortisol output in healthy young adults with low early life parental care. Psychopharmacology 2011, 214:261-268.
28. Esbensen A.J., Greenberg J.S., Seltzer M.M., Aman M.G. A longitudinal investigation of psychotropic and non-psychotropic medication use among adolescents and adults with autism spectrum disorders. J. Autism Dev. Disord. 2009, 39:1339-1349.
29. Fries E., Dettenborn L., Kirschbaum C. The cortisol awakening response (CAR): facts and future directions. Int. J. Psychophysiol. 2009, 72:67-73.
30. Godavarthi S.K., Dey P., Maheshwari M., Jana N.R. Defective glucocorticoid hormone receptor signaling leads to increased stress and anxiety in a mouse model of Angelman syndrome. Hum. Mol. Genet. 2012, 21:1824-1834.
31. Goodyer I.M., Herbert J., Altham P.M.E., Pearson J., Secher S.M., et al. Adrenal secretion during major depression in 8- to 16-year-olds, I. Altered diurnal rhythms in salivary cortisol and dehydroepiandrosterone (DHEA) at presentation. Psychol. Med. 1996, 26:245-256.
32. Granger D.A., Hibel L.C., Fortunato C.K., Kapelewski C.H. Medication effects on salivary cortisol: tactics and strategy to minimize impact in behavioral and developmental science. Psychoneuroendocrinology 2009, 34:1437-1448.
33. Greaves-Lord K., Huizink A.C., Oldehinkel A.J., Ormel J., Verhulst F.C., Ferdinand R.F. Baseline cortisol measures and developmental pathways of anxiety in early adolescence. Acta Psychiatr. Scand. 2009, 120:178-186.
34. Gunnar M.R., Talge N.M., Herrera A. Stressor paradigms in developmental studies: what does and does not work to produce mean increases in salivary cortisol. Psychoneuroendocrinology 2009, 34:953-967.
35. Gunnar M.R., Vazquez D. Stress Neurobiology and Developmental Psychopathology 2006, John Wiley & Sons Inc., Hoboken, NJ.
36. Gunnar M.R., Wewerka S., Frenn K., Long J.D., Griggs C. Developmental changes in hypothalamus-pituitary-adrenal activity over the transition to adolescence: normative changes and associations with puberty. Dev. Psychopathol. 2009, 21:69-85.
37. Hamza R.T., Hewedi D.H., Ismail M.A. Basal and adrenocorticotropic hormone stimulated plasma cortisol levels among Egyptian Autistic children: relation to disease severity. Ital. J. Pediatr. 2010, 36:7.
38. Hennessey J.W., Levine S. Stress, Arousal, and the Pituitary-adrenal System: A Psychoendocrine Hypothesis 1979, Academic Press, New York, NY.
39. Herman J.P., Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci. 1997, 20:78-84.
40. Heyns D.P., Van Baelen H.V., De Moor P. Study of steroid-protein binding by means of competitive adsorption: application to cortisol binding in plasma. Clin. Chim. Acta 1967, 18:361-370.
41. Hill S.D., Wagner E.A., Shedlarski J.G., Sears S.P. Diurnal cortisol and temperature variation of normal and autistic children. Dev. Psychobiol. 1977, 10:579-583.
42. Hofvander B., Delorme R., Chaste P., Nyden A., Wentz E., Stahlberg O., Herbrecht E., Stopin A., Anckarsater H., Gillberg C., Rastam M., Leboyer M. Psychiatric and psychosocial problems in adults with normal-intelligence autism spectrum disorders. BMC Psychiatry 2009, 9:35.
43. Hoshino Y., Ohno Y., Murata S., Yokoyama F., Kaneko M., Kumashiro H. Dexamethasone suppression text in autistic children. Folia Psychiatr. Neurol. Jpn. 1984, 38:445-450.
44. Hoshino Y., Yokoyama F., Watanabe M., Murata S., Kaneko M., Kumashiro H. The diurnal variation and response to dexamethasone suppression test of saliva cortisol level in autistic children. Jpn. J. Psychiatry Neurol. 1987, 41:227-236.
45. Husebye E.S., Allolio B., Arlt W., Badenhoop K., Bensing S., Betterle C., et al. Consensus statement on the diagnosis, treatment and follow-up of patients with primary adrenal insufficiency. J. Intern. Med. 2013, 275:104-115.
46. Jansen L.M.C., Gispen-de Wied C.C., Jansen M.A., van der Gaag R.-J., Matthys W., van Engeland H. Pituitary-adrenal reactivity in a child psychiatric population: salivary cortisol response to stressors. Eur. Neuropsychopharmacol. 1999, 9:67-75.
47. Jansen L.M.C., Gispen-de Wied C.C., van der Gaag R.-J., van Engeland H. Differentiation between autism and multiple complex developmental disorder in response to psychosocial stress. Neuropsychopharmacology 2003, 28:582-590.
48. Jansen L.M.C., Gispen-de Wied C.C., Van der Gaag R.J., ten Hove F., Willemsen-Swinkels S.W.M., Harteveld E., Van Engeland H. Unresponsiveness to psychosocial stress in a subgroup of autistic-like children, multiple complex developmental disorder. Psychoneuroendocrinology 2000, 25:753-764.
49. Jansen L.M.C., Gispen-de Wied C.C., Wiegant V.M., Westenberg H.G.M., Lahuis B.E., van Engeland H. Autonomic and neuroendocrine responses to a psychosocial stressor in adults with autistic spectrum disorder. J. Autism Dev. Disord. 2006, 36:891-899.
50. Jensen J.B., Realmuto G.M., Garfinkel B.D. The dexamethasone suppression test in infantile autism. J. Am. Acad. Child. Adolesc. Psychiatry 1985, 24:263-265.
51. Kalin N.H., Risch S.C., Janowsky D.S., Murphy D.L. Use of the dexamethasone suppression test in clinical-psychiatry. J. Clin. Psychopharm. 1981, 1:64-69.
52. Kidd S.A., Corbett B.A., Granger D.A., Boyce W.T., Anders T.F., Tager I.B. Daytime secretion of salivary cortisol and alpha-amylase in preschool-aged children with autism and typically developing children. J. Autism Dev. Disord. 2012, 42:2648-2658.
53. Kirschbaum C., Hellhammer D.H. Salivary cortisol. Encyclopedia of Stress 2000, 379-383. Academic Press, San Diego, CA. G. Fink (Ed.).
54. Kirschbaum C., Wust S., Faig H.G., Hellhammer D.H. Heritability of cortisol responses to human corticotropin-releasing hormone, ergometry, and psychological stress in humans. J. Clin. Endocrinol. Metab. 1992, 75:1526-1530.
55. Kudielka B.M., Hellhammer J., Hellhammer D.H., Wolf O.T., Pirke K.M., Varadi E., et al. Sex differences in endocrine and psychological responses to psychosocial stress in healthy elderly subjects and the impact of a 2-week dehydroepiandrosterone treatment. J. Clin. Endocrinol. Metab. 1998, 83:1756-1761.
56. Kudielka B.M., Kirschbaum C. Awakening cortisol responses are influenced by health status and awakening time but not by menstrual cycle phase. Psychoneuroendocrinology 2003, 28:35-47.
57. Lanni K.E., Schupp C.W., Simon D., Corbett B.A. Verbal ability, social stress, and anxiety in children with autistic disorder. Autism 2012, 16:123-138.
58. Levine A., Zagoory-Sharon O., Feldman R., Lewis J.G., Weller A. Measuring cortisol in human psychobiological studies. Physiol. Behav. 2007, 90:43-53.
59. Levine T.P., Sheinkopf S.J., Pescosolido M., Rodino A., Elia G., Lester B. Physiologic arousal to social stress in children with autism spectrum disorders: a pilot study. Res. Autism Spectr. Disord. 2012, 6:177-183.
60. Lopata C., Volker M.A., Putnam S.K., Thomeer M.L., Nida R.E. Effect of social familiarity on salivary cortisol and self-reports of social anxiety and stress in children with high functioning autism spectrum disorders. J. Autism Dev. Disord. 2008, 38:1866-1877.
61. Mendel C.M. The free hormone hypothesis: a physiologically based mathematical model. Endocr. Rev. 1989, 10:232-274.
62. Marceau K., Shirtcliff E.A., Hastings P.D., Klimes-Dougan B., Zahn-Waxler C., Dorn L.D., et al. Within-adolescent coupled changes in cortisol with DHEA and testosterone in response to three stressors during adolescence. Psychoneuroendocrinology 2014, 41:33-45.
63. Marinović-Ćurin J., Marinović-Terzić I., Bujas-Petković Z., Zekan L., Škrabić V., {Eth}ogaš Z., Terzić J. Slower cortisol response during ACTH stimulation test in autistic children. Eur. Child Adolesc. Psychiatry 2008, 17:39-43.
64. Morineau G., Boudi A., Barka A., Gourmelen M., Degeilh F., Hardy N., et al. Radioimmunoassay of cortisone in serum, urine, and saliva to assess the status of the cortisol-cortisone shuttle. Clin. Chem. 1997, 43:1397-1407.
65. Muhtz C., Zyriax B.C., Klahn T., Windler E., Otte C. Depressive symptoms and metabolic risk: effects of cortisol and gender. Psychoneuroendocrinology 2009, 34:1004-1011.
66. Munck A., Guyre P.M. Glucocorticoids and immune function. Psychoneuroimmunology 1991, 447-474. Academic Press, San Diego, CA. R. Ader, D.L. Felten, N. Cohen (Eds.).
67. Naber F.B.A., Swinkels S.H.N., Buitelaar J.K., Bakermans-Kranenburg M.J., van Ijzendoorn M.H., Dietz C., van Daalen E., van Engeland H. Attachment in toddlers with autism and other developmental disorders. J. Autism Dev. Disord. 2007, 37:1123-1138.
68. Newell-Price J., Bertagna X., Grossman A.B., Nieman L.K. Cushing's syndrome. Lancet 2006, 367:1605-1617.
69. Nieman L.K., Biller B.M., Findling J.W., Newell-Price J., Savage M.O., Stewart P.M., et al. The diagnosis of Cushing's syndrome: an endocrine society clinical practice guideline. J. Clin. Endocrinol. Metab. 2008, 93:1526-1540.
70. Nir I., Meir D., Zilber N., Knobler H., Hadjez J., Lerner Y. Circadian melatonin, thyroid-stimulating hormone, prolactin, and cortisol levels in serum of young adults with autism. J. Autism Dev. Disord. 1995, 25:641-654.
71. Pruessner J.C., Wolf O.T., Hellhammer D.H., Buske-Kirschbaum A., von Auer K., Jobst S., Kaspers F., Kirschbaum C. Free cortisol levels after awakening: a reliable biological marker for the assessment of adrenocortical activity. Life Sci. 1997, 61:2539-2549.
72. Richdale A.L., Prior M.R. Urinary cortisol circadian rhythm in a group of high-functioning children with autism. J. Autism Dev. Disord. 1992, 22:433-447.
73. Rose'meyer R. A review of the serotonin transporter and prenatal cortisol in the development of autism spectrum disorders. Mol. Autism 2013, 4:37.
74. Rosmalen J.G., Oldehinkel A.J., Ormel J., de Winter A.F., Buitelaar J.K., Verhulst F.C. Determinants of salivary cortisol levels in 10-12 year old children: a population-based study of individual differences. Psychoneuroendocrinology 2005, 30:483-495.
75. Rotenberg S., McGrath J.J., Roy-Gagnon M.H., Tu M.T. Stability of the diurnal cortisol profile in children and adolescents. Psychoneuroendocrinology 2012, 37:1981-1989.
76. Sandman C.A., Barron J.L., Chicz-DeMet A., DeMet E.M. Brief report: plasma β-endorphin and cortisol levels in autistic patients. J. Autism Dev. Disord. 1991, 21:83-87.
77. Sapolsky R.M., Krey L.C., McEwen B.S. The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr. Rev. 1986, 7:284-301.
78. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21:55-89.
79. Schmidt-Reinwald A., Pruessner J.C., Hellhammer D.H., Federenko I., Rohleder N., Schurmeyer T.H., Kirschbaum C. The cortisol response to awakening in relation to different challenge tests and a 12-hour cortisol rhythm. Life Sci. 1999, 64:1653-1660.
80. Schupp C.W., Simon D., Corbett B.A. Cortisol responsivity differences in children with autism spectrum disorders during free and cooperative play. J. Autism Dev. Disord. 2013, 43:2405-2417.
81. Seltzer M.M., Almeida D.M., Greenberg J.S., Savla J., Stawski R.S., Hong J., Taylor J.L. Psychosocial and biological markers of daily lives of midlife parents of children with disabilities. J. Health Soc. Behav. 2009, 50:1-15.
82. Simon D.M., Corbett B.A. Examining associations between anxiety and cortisol in high functioning male children with autism. J. Neurodev. Disord. 2013, 5:32.
83. Simonoff E., Pickles A., Charman T., Chandler S., Loucas T., Baird G. Psychiatric disorders in children with autism spectrum disorders: prevalence, comorbidity, and associated factors in a population-derived sample. J. Am. Acad. Child Adolesc. Psychiatry 2008, 47:921-929.
84. Smyth J.M., Ockenfels M.C., Gorin A.A., Catley D., Porter L.S., Kirschbaum C., Hellhammer D.H., Stone A.A. Individual differences in the diurnal cycle of cortisol. Psychoneuroendocrinology 1997, 22:89-105.
85. Spratt E.G., Nicholas J.S., Brady K.T., Carpenter L.A., Hatcher C.R., Meekins K.A., Furlanetto R.W., Charles J.M. Enhanced cortisol response to stress in children in autism. J. Autism Dev. Disord. 2012, 42:75-81.
86. Strous R.D., Golubchik P., Maayan R., Mozes T., Tuati-Werner D., Weizman A., Spivak B. Lowered DHEA-S plasma levels in adult individuals with autistic disorder. Eur. Neuropsychopharmacol. 2005, 15:305-309.
87. Tani P., Lindberg N., Matto V., Appelberg B., Nieminen-von Wendt T., von Wendt L., Porkka-Heiskanen T. Higher plasma ACTH levels in adults with Asperger syndrome. J. Psychosom. Res. 2005, 58:533-536.
88. Ten S., New M., Maclaren N. Addison's disease 2001. J. Clin. Endocrinol. Metab. 2001, 86:2909-2922.
89. Tordjman S., Anderson G.M., McBride P.A., Hertzig M.E., Snow M.E., Hall L.M., Thompson S.M., Ferrari P., Cohen D.J. Plasma β-endorphin, adrenocorticotropin hormone, and cortisol in autism. J. Child Psychol. Psychiatry 1997, 38:705-715.
90. Van den Bergh B.R., Van Calster B., Smits T., Van Huffel S., Lagae L. Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology 2008, 33:536-545.
91. Vining R.F., McGinley R.A., Maksvytis J.J., Ho K.Y. Salivary cortisol: a better measure of adrenal cortical function than serum cortisol. Ann. Clin. Biochem. 1983, 20:329-335.
92. Wust S., Wolf J., Hellhammer D.H., Federenko I., Schommer N., Kirschbaum C. The cortisol awakening response-normal values and confounds. Noise Health 2000, 2:79-88.
93. Yamazaki K., Saito Y., Okada F., Fujieda T., Yamashita I. An application of neuroendocrinological studies in autistic children and Heller's syndrome. J. Autism Dev. Disord. 1975, 5:323-332.
94. Zinke K., Fries E., Kliegel M., Kirschbaum C., Dettenborn L. Children with high-functioning autism show a normal cortisol awakening response (CAR). Psychoneuroendocrinology 2010, 35:1578-1582.