A meta-analytic review of the correlation between peripheral oxytocin and cortisol concentrations

Frontiers in Neuroendocrinology

Volumn 43, Issue , 2016, Pages 19-27

  Brown, Christopher A ^a   Cardoso, Christopher ^b,c   Ellenbogen, Mark A ^a  

^a Gina Cody School of Engineering and Computer Science   (Canada)

^b CARLETON UNIVERSITY   (Canada)

^c ROYAL OTTAWA HOSPITAL   (Canada)

Author keywords

Cortisol; Experimental Manipulation; Meta Analysis; Oxytocin; Plasma; Stress

Indexed keywords

HYDROCORTISONE; OXYTOCIN;

DISTRESS SYNDROME; EFFECT SIZE; EXPERIMENTAL MANIPULATION; EXPERIMENTAL TEST; HORMONE RESEARCH; HUMAN; HYDROCORTISONE RELEASE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOASSAY; LACTATION; MEDICAL RESEARCH; MODERATION ANALYSIS; MOLECULAR INTERACTION; NONHUMAN; OXYTOCIN BLOOD LEVEL; OXYTOCIN RELEASE; PRIORITY JOURNAL; PUBLISHING; REVIEW; SALIVA ANALYSIS; SOCIAL ENVIRONMENT; STATISTICAL ANALYSIS; STRESS; URINALYSIS; VALIDITY; ANIMAL; MENTAL STRESS; META ANALYSIS; METABOLISM;

ANIMALS; HUMANS; HYDROCORTISONE; OXYTOCIN; STRESS, PSYCHOLOGICAL;

EID: 84997335706     PISSN: 00913022     EISSN: 10956808     Source Type: Journal    
DOI: 10.1016/j.yfrne.2016.11.001     Document Type: Review

References (76)

1. ∗Alfvén, G., Plasma oxytocin in children with recurrent abdominal pain. J. Pediatr. Gastroenterol. Nutr. 38 (2004), 513–517.
2. ∗Alfven, G., Torre, B., Uvnäs-Moberg, K., Depressed concentrations of oxytocin and cortisol in children with recurrent abdominal pain of non-organic origin. Acta Paediatr., 1994, 1076–1080.
3. Amico, J.A., Ulbrecht, J.S., Robinson, A.G., Clearance studies of oxytocin in humans using radioimmunoassay measurements of the hormone in plasma and urine. J. Clin. Endocrinol. Metab. 64 (1987), 340–345, 10.1210/jcem-64-2-340.
4. Amico, J.A., Mantella, R.C., Vollmer, R.R., Li, X., Anxiety and stress responses in female oxytocin deficient mice. J. Neuroendocrinol. 16 (2004), 319–324, 10.1111/j.0953-8194.2004.01161.x.
5. Balodis, I.M., Wynne-Edwards, K.E., Olmstead, M.C., The other side of the curve: examining the relationship between pre-stressor physiological responses and stress reactivity. Psychoneuroendocrinology 35 (2010), 1363–1373, 10.1016/j.psyneuen.2010.03.011.
6. †Barraza, J.A., Zak, P.J., Empathy toward strangers triggers oxytocin release and subsequent generosity. Ann. NY Acad. Sci. 1167 (2009), 182–189, 10.1111/j.1749-6632.2009.04504.
7. Bartz, J.A., Zaki, J., Bolger, N., Ochsner, K.N., Social effects of oxytocin in humans: context and person matter. Trends Cogn. Sci. 15 (2011), 301–309, 10.1016/j.tics.2011.05.002.
8. ∗Blagrove, M., Fouquet, N.C., Baird, A.L., Pace-Schott, E.F., Davies, A.C., Neuschaffer, J.L., Henley-Einion, J.A., Weidemann, C.T., Thome, J., McNamara, P., Turnbull, O.H., Association of salivary-assessed oxytocin and cortisol levels with time of night and sleep stage. J. Neural Transm. 119 (2012), 1223–1232, 10.1007/s00702-012-0880-1.
9. ∗Bosch, O.G., Eisenegger, C., Gertsch, J., von Rotz, R., Dornbierer, D., Gachet, M.S., Heinrichs, M., Wetter, T.C., Seifritz, E., Quednow, B.B., Gamma-hydroxybutyrate enhances mood and prosocial behavior without affecting plasma oxytocin and testosterone. Psychoneuroendocrinology 62 (2015), 1–10, 10.1016/j.psyneuen.2015.07.167.
10. Carson, D.S., Berquist, S.W., Trujillo, T.H., Garner, J.P., Hannah, S.L., Hyde, S.A., Sumiyoshi, R.D., Jackson, L.P., Moss, J.K., Strehlow, M.C., Cheshier, S.H., Cerebrospinal fluid and plasma oxytocin concentrations are positively correlated and negatively predict anxiety in children. Mol. Psychiatry 20 (2014), 1085–1090.
11. Cardoso, C., Ellenbogen, M.A., Orlando, M.A., Bacon, S.L., Joober, R., Intranasal oxytocin attenuates the cortisol response to physical stress: a dose-response study. Psychoneuroendocrinology 38 (2013), 399–407, 10.1016/j.psyneuen.2012.07.013.
12. Cardoso, C., Kingdon, D., Ellenbogen, M.A., A meta-analytic review of the impact of intranasal oxytocin administration on cortisol concentrations during laboratory tasks: moderation by method and mental health. Psychoneuroendocrinology 49 (2014), 161–170, 10.1016/j.psyneuen.2014.07.014.
13. Christensen, J.C., Shiyanov, P.A., Estepp, J.R., Schlager, J.J., Lack of association between human plasma oxytocin and interpersonal trust in a prisoner's dilemma paradigm. PLoS ONE, 9, 2014, e116172, 10.1371/journal.pone.0116172.
14. Cooper, H., Hedges, L.V., Valentine, J.C., The Handbook of Research Synthesis and Meta-Analysis. second ed., 2009, Russell Sage Foundation, New York, NY.
15. Crespi, B.J., Oxytocin, testosterone, and human social cognition. Biol. Rev., 2015, 10.1111/brv.12175.
16. Ditzen, B., Schaer, M., Gabriel, B., Bodenmann, G., Ehlert, U., Heinrichs, M., Intranasal oxytocin increases positive communication and reduces cortisol levels during couple conflict. Biol. Psychiatry 65 (2009), 728–731, 10.1016/j.biopsych.2008.10.011.
17. Egger, M., Davey Smith, G., Schneider, M., Minder, C., Bias in meta-analysis detected by a simple, graphical test. BMJ 315 (1997), 629–634.
18. Feldman, R., Gordon, I., Schneiderman, I., Weisman, O., Zagoory-Sharon, O., Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 35 (2010), 1133–1141, 10.1016/j.psyneuen.2010.01.013.
19. †Feldman, R., Weller, A., Zagoory-Sharon, O., Levine, A., Evidence for a neuroendocrinological foundation of human affiliation: plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding. Psychol. Sci. 18 (2007), 965–970, 10.1111/j.1467-9280.2007.02010.
20. ∗Ferreira, M.F., Sobrinho, L.G., Santos, M.a., Sousa, M.F., Uvnäs-Moberg, K., Rapid weight gain, at least in some women, is an expression of a neuroendocrine state characterized by reduced hypothalamic dopaminergic tone. Psychoneuroendocrinology 23 (1998), 1005–1013.
21. †Floyd, K., Pauley, P.M., Hesse, C., State and trait affectionate communication buffer adults’ stress reactions. Commun. Monogr. 77 (2010), 618–636, 10.1080/03637751.2010.498792.
22. Gimpl, G., Fahrenholz, F., The oxytocin receptor system: structure, function, and regulation. Physiol. Rev. 81 (2001), 629–683.
23. †Gordon, I., Zagoory-Sharon, O., Schneiderman, I., Leckman, J.F., Weller, A., Feldman, R., Oxytocin and cortisol in romantically unattached young adults: associations with bonding and psychological distress. Psychophysiology 45 (2008), 349–352, 10.1111/j.1469-8986.2008.00649.
24. †Grape, C., Sandgren, M., Hansson, L., Does singing promote well-being? An empirical study of professional and amateur singers during a singing lesson. Behav. Sci. 38 (2002), 65–74.
25. Grewen, K.M., Davenport, R.E., Light, K.C., An investigation of plasma and salivary oxytocin responses in breast- and formula-feeding mothers of infants. Psychophysiology, 2010, 10.1111/j.1469-8986.2009.00968.
26. Heim, C., Young, L.J., Newport, D.J., Mletzko, T., Miller, A.H., Nemeroff, C.B., Lower CSF oxytocin concentrations in women with a history of childhood abuse. Mol. Psychiatry 14 (2009), 954–958, 10.1038/mp.2008.112.
27. Heinrichs, M., Meinlschmidt, G., Neumann, I., Wagner, S., Kirschbaum, C., Ehlert, U., Hellhammer, D.H., Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women. J. Clin. Endocrinol. Metab. 86 (2001), 4798–4804, 10.1210/jcem.86.10.7919.
28. ∗Hew-Butler, T., Noakes, T.D., Soldin, S.J., Verbalis, J.G., Acute changes in endocrine and fluid balance markers during high-intensity, steady-state, and prolonged endurance running: unexpected increases in oxytocin and brain natriuretic peptide during exercise. Eur. J. Endocrinol. 159 (2008), 729–737, 10.1530/EJE-08-0064.
29. Higgins, J.P.T., Thompson, S.G., Quantifying heterogeneity in a meta-analysis. Stat. Med. 21 (2002), 1539–1558, 10.1002/sim.1186.
30. Hoge, E.A., Pollack, M.H., Kaufman, R.E., Zak, P.J., Simon, N.M., Oxytocin levels in social anxiety disorder. CNS Neurosci. Ther. 14 (2008), 165–170, 10.1111/j.1755-5949.2008.00051.x.
31. ∗Hursti, T.J., Börjeson, S., Hellström, P.M., Avall-Lundqvist, E., Stock, S., Steineck, G., Peterson, C., Effect of chemotherapy on circulating gastrointestinal hormone levels in ovarian cancer patients: relationship to nausea and vomiting. Scand. J. Gastroenterol. 40 (2005), 654–661, 10.1080/0036552051001163.
32. ∗Hysek, C.M., Domes, G., Liechti, M.E., MDMA enhances “mind reading” of positive emotions and impairs “mind reading” of negative emotions. Psychopharmacology 222 (2012), 293–302, 10.1007/s00213-012-2645-9.
33. ∗Hysek, C.M., Schmid, Y., Rickli, A., Simmler, L.D., Donzelli, M., Grouzmann, E., Liechti, M.E., Carvedilol inhibits the cardiostimulant and thermogenic effects of MDMA in humans. Br. J. Pharmacol. 166 (2012), 2277–2288, 10.1111/j.1476-5381.2012.01936.x.
34. ∗Hysek, C.M., Schmid, Y., Simmler, L.D., Domes, G., Heinrichs, M., Eisenegger, C., Preller, K.H., Quednow, B.B., Liechti, M.E., MDMA enhances emotional empathy and prosocial behavior. Soc. Cogn. Affect. Neurosci., 2013, 10.1093/scan/nst161.
35. ∗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. 36 (2006), 891–899, 10.1007/s10803-006-0124-z.
36. Jokinen, J., Chatzittofis, A., Hellström, C., Nordström, P., Uvnäs-Moberg, K., Asberg, M., Low CSF oxytocin reflects high intent in suicide attempters. Psychoneuroendocrinology 37 (2012), 482–490.
37. ∗Jong, T.R. de, Menon, R., Bludau, A., Grund, T., Biermeier, V., Klampfl, S.M., Jurek, B., Bosch, O.J., Hellhammer, J., Neumann, I.D., Salivary oxytocin concentrations in response to running, sexual self-stimulation, breastfeeding and the TSST: the Regensburg Oxytocin Challenge (ROC) study. Psychoneuroendocrinology 62 (2015), 381–388, 10.1016/j.psyneuen.2015.08.027.
38. Kagerbauer, S.M., Martin, J., Schuster, T., Blobner, M., Kochs, E.F., Landgraf, R., Plasma oxytocin and vasopressin do not predict neuropeptide concentrations in human cerebrospinal fluid. J. Neuroendocrinol. 25 (2013), 668–673.
39. ∗Keating, C., Dawood, T., Barton, D.A., Lambert, G.W., Tilbrook, A.J., Effects of selective serotonin reuptake inhibitor treatment on plasma oxytocin and cortisol in major depressive disorder. BMC Psychiatry, 13, 2013, 124, 10.1186/1471-244X-13-124.
40. Kirschbaum, C., Hellhammer, D.H., Salivary cortisol. Fink, G., (eds.) Encyclopedia of Stress, 2000, Academic Press, San Diego, 379–383.
41. Kirschbaum, C., Hellhammer, D.H., Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 19 (1994), 313–333.
42. Lang, R.E., Heil, J.W., Ganten, D., Hermann, K., Unger, T., Rascher, W., Oxytocin unlike vasopressin is a stress hormone in the rat. Neuroendocrinology 37 (1983), 314–316.
43. Laurent, H.K., Lucas, T., Pierce, J., Goetz, S., Granger, D.A., Coordination of cortisol response to social evaluative threat with autonomic and inflammatory responses is moderated by stress appraisals and affect. Biol. Psychol. 118 (2016), 17–24, 10.1016/j.biopsycho.2016.04.066.
44. Legros, J.J., Inhibitory effect of oxytocin on corticotrope function in humans: are vasopressin and oxytocin ying-yang neurohormones?. Psychoneuroendocrinology 26 (2001), 649–655.
45. McCullough, M.E., Churchland, P.S., Mendez, A.J., Problems with measuring peripheral oxytocin: can the data on oxytocin and human behavior be trusted?. Neurosci. Biobehav. Rev. 37 (2013), 1485–1492, 10.1016/j.neubiorev.2013.04.018.
46. Meyer-Lindenberg, A., Domes, G., Kirsch, P., Heinrichs, M., Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat. Rev. Neurosci. 12 (2011), 524–538, 10.1038/nrn3044.
47. Neumann, I.D., Johnstone, H.A., Hatzinger, M., Liebsch, G., Shipston, M., Russell, J.A., Landgraf, R., Douglas, A.J., Attenuated neuroendocrine responses to emotional and physical stressors in pregnant rats involve adenohypophysial changes. J. Physiol. 508 (1998), 289–300.
48. Neumann, I.D., Wigger, A., Torner, L., Holsboer, F., Landgraf, R., Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus. J. Neuroendocrinol. 12 (2000), 235–243, 10.1046/j.1365-2826.2000.00442.x.
49. Neumann, I.D., Landgraf, R., Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci. 35 (2012), 649–659, 10.1016/j.tins.2012.08.004.
50. Nishioka, T., Anselmo-Franci, J.A., Li, P., Callahan, M.F., Morris, M., Stress increases oxytocin release within the hypothalamic paraventricular nucleus. Brain Res. 781 (1998), 57–61.
51. ∗Nissen, E., Uvnäs-Moberg, K., Svensson, K., Stock, S., Widström, A.M., Winberg, J., Different patterns of oxytocin, prolactin but not cortisol release during breastfeeding in women delivered by caesarean section or by the vaginal route. Early Hum. Dev. 45 (1996), 103–118.
52. Parker, K.J., Buckmaster, C.L., Schatzberg, A.F., Lyons, D.M., Intranasal oxytocin administration attenuates the ACTH stress response in monkeys. Psychoneuroendocrinology 30 (2005), 924–929, 10.1016/j.psyneuen.2005.04.002.
53. ∗Parker, K.J., Kenna, H.A., Zeitzer, J.M., Keller, J., Blasey, C.M., Amico, J.A., Schatzberg, A.F., Preliminary evidence that plasma oxytocin levels are elevated in major depression. Psychiatry Res. 178 (2010), 359–362, 10.1016/j.psychres.2009.09.017.
54. Pierrehumbert, B., Torrisi, R., Laufer, D., Halfon, O., Ansermet, F., Beck Popovic, M., Oxytocin response to an experimental psychosocial challenge in adults exposed to traumatic experiences during childhood or adolescence. Neuroscience 166 (2010), 168–177, 10.1016/j.neuroscience.2009.12.016.
55. Sapolsky, R.M., Romero, L.M., Munck, A.U., How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21 (2000), 55–89, 10.1210/edrv.21.1.0389.
56. R Core Team, R: A Language and Environment for Statistical Computing. 2013, R Foundation for Statistical Computing, Vienna, Austria 3-900051-07-0 .
57. ∗Schmid, Y., Enzler, F., Gasser, P., Grouzmann, E., Preller, K.H., Vollenweider, F.X., Brenneisen, R., Müller, F., Borgwardt, S., Liechti, M.E., Acute effects of lysergic acid diethylamide in healthy subjects. Biol. Psychiatry 78 (2015), 544–553, 10.1016/j.biopsych.2014.11.015.
58. ∗Schmid, Y., Rickli, A., Schaffner, A., Duthaler, U., Grouzmann, E., Hysek, C.M., Liechti, M.E., Interactions between bupropion and 3,4-methylenedioxymethamphetamine in healthy subjects. J. Pharmacol. Exp. Ther. 353 (2015), 102–111, 10.1124/jpet.114.222356.
59. ∗Schmid, Y., Hysek, C.M., Simmler, L.D., Crockett, M.J., Quednow, B.B., Liechti, M.E., Differential effects of MDMA and methylphenidate on social cognition. J. Psychopharmacol. 28 (2014), 847–856, 10.1177/0269881114542454.
60. Seckl, J.R., Lightman, S.L., Diurnal rhythm of vasopressin but not of oxytocin in the cerebrospinal fluid of the goat: lack of association with plasma cortisol rhythm. J. Endocrinol. 114 (1987), 477–482.
61. Sterne, J.A., Egger, M., Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J. Clin. Epidemiol. 54 (2001), 1046–1055.
62. ∗Strathearn, L., Fonagy, P., Amico, J., Montague, P.R., Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology 34 (2009), 2655–2666, 10.1038/npp.2009.103.
63. Szeto, A., McCabe, P.M., Nation, D.A., Tabak, B.A., Rossetti, M.A., McCullough, M.E., Schneiderman, N., Mendez, A.J., Evaluation of enzyme immunoassay and radioimmunoassay methods for the measurement of plasma oxytocin. Psychosom. Med. 73 (2011), 393–400, 10.1097/PSY.0b013e31821df0c2.
64. ∗Tabak, B.A., McCullough, M.E., Szeto, A., Mendez, A.J., McCabe, P.M., Oxytocin indexes relational distress following interpersonal harms in women. Psychoneuroendocrinology 36 (2011), 115–122, 10.1016/j.psyneuen.2010.07.004.
65. Taylor, S.E., Klein, L.C., Lewis, B.P., Gruenewald, T.L., Gurung, R.A., Updegraff, J.A., Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol. Rev. 107 (2000), 411–429.
66. Taylor, S.E., Saphire-Bernstein, S., Seeman, T.E., Are plasma oxytocin in women and plasma vasopressin in men biomarkers of distressed pair-bond relationships?. Psychol. Sci. 21 (2010), 3–7, 10.1177/0956797609356507.
67. ∗Tops, M., van Peer, J.M., Korf, J., Wijers, A.a., Tucker, D.M., Anxiety, cortisol, and attachment predict plasma oxytocin. Psychophysiology 44 (2007), 444–449, 10.1111/j.1469-8986.2007.00510.
68. ∗Van Londen, L., Goekoop, J.G., Zwinderman, A.H., Lanser, J.B., Wiegant, V.M., De Wied, D., Neuropsychological performance and plasma cortisol, arginine vasopressin and oxytocin in patients with major depression. Psychol. Med. 28 (1998), 275–284.
69. ∗Varga, K., Kekecs, Z., Oxytocin and cortisol in the hypnotic interaction. Int. J. Clin. Exp. Hypn. 62 (2014), 111–128, 10.1080/00207144.2013.841494.
70. Viechtbauer, W., Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36 (2010), 1–48.
71. Weisman, O., Zagoory-Sharon, O., Schneiderman, I., Gordon, I., Feldman, R., Plasma oxytocin distributions in a large cohort of women and men and their gender-specific associations with anxiety. Psychoneuroendocrinology 38 (2013), 694–701, 10.1016/j.psyneuen.2012.08.011.
72. Wotjak, C.T., Ganster, J., Kohl, G., Holsboer, F., Landgraf, R., Engelmann, M., Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: new insights into the secretory capacities of peptidergic neurons. Neuroscience 85 (1998), 1209–1222.
73. Young, E.A., Abelson, J., Lightman, S.L., Cortisol pulsatility and its role in stress regulation and health. Front. Neuroendocrinol. 25 (2004), 69–76, 10.1016/j.yfrne.2004.07.001.
74. ∗Yuen, K.W., Garner, J.P., Carson, D.S., Keller, J., Lembke, A., Hyde, S.A., Kenna, H.A., Tennakoon, L., Schatzberg, A.F., Parker, K.J., Plasma oxytocin concentrations are lower in depressed vs. healthy control women and are independent of cortisol. J. Psychiatr. Res. 51 (2014), 30–36, 10.1016/j.jpsychires.2013.12.012.
75. Zelkowitz, P., Gold, I., Feeley, N., Hayton, B., Carter, C.S., Tulandi, T., Abenhaim, H.A., Levin, P., Psychosocial stress moderates the relationships between oxytocin, perinatal depression, and maternal behavior. Horm. Behav. 66 (2014), 351–360, 10.1016/j.yhbeh.2014.06.014.
76. Zhang, G., Zhang, Y., Fast, D.M., Lin, Z., Steenwyk, R., Ultra sensitive quantitation of endogenous oxytocin in rat and human plasma using a two-dimensional liquid chromatography-tandem mass spectrometry assay. Anal. Biochem. 416 (2011), 45–52, 10.1016/j.ab.2011.04.041.