Abstract
Rationale
There are complex relationships between stress and smoking; smoking may reduce the emotional discomfort of stress, yet nicotine activates stress systems and may alter responses to acute stress. It is important to understand how smoking affects physiological and psychological outcomes after stress and how these may interact to motivate smoking.
Objectives
This study aimed to examine the magnitude and time course of hormonal, cardiovascular, and psychological responses to acute psychosocial stress in smokers and non-smokers to investigate whether responses to acute stress are altered in smokers.
Materials and methods
Healthy male non-smokers (n = 20) and smokers (n = 15) participated in two experimental sessions involving a standardized public speaking stress procedure and a control non-stressful task. The outcome measures included self-reported mood, cardiovascular measures (heart rate and blood pressure), and plasma hormone levels (noradrenaline, cortisol, progesterone, and allopregnanolone).
Results
Smokers exhibited blunted increases in cortisol after the Trier Social Stress Test, and they reported greater and more prolonged subjective agitation than non-smokers. Stress-induced changes in progesterone were similar between smokers and non-smokers, although responses overall were smaller among smokers. Stress did not significantly alter levels of allopregnanolone, but smokers exhibited lower plasma concentrations of this neurosteroid.
Conclusions
These findings suggest that smoking dampens hormonal responses to stress and prolongs subjective discomfort. Dysregulated stress responses may represent a breakdown in the body’s ability to cope efficiently and effectively with stress and may contribute to smokers’ susceptibility to acute stress, especially during abstinence.
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References
al’Absi M, Wittmers LE, Erickson J, Hatsukami D, Crouse B (2003) Attenuated adrenocortical and blood pressure responses to psychological stress in ad libitum and abstinent smokers. Pharmacol Biochem Behav 74:401–410
APA (1994) American psychiatric association diagnostic and statistical manual of psychiatry, 4th edn. APA, Arlington
Astrand P, Rodahl K (1977) Textbook of work physiology. Physiological basis of exercise, 2nd ed. McGraw-Hill Book Co., New York
Back SE, Waldrop AE, Saladin ME, Yeatts SD, Simpson A, McRae AL, Upadhyaya HP, Contini Sisson R, Spratt EG, Allen J, Kreek MJ, Brady KT (2008) Effects of gender and cigarette smoking on reactivity to psychological and pharmacological stress provocation. Psychoneuroendocrinology 33:560–568
Badrick E, Kirschbaum C, Kumari M (2007) The relationship between smoking status and cortisol secretion. J Clin Endocrinol Metab 92(3):819–824
Balfour DJ, Khullar AK, Longden A (1975) Effects of nicotine on plasma corticosterone and brain amines in stressed and unstressed rats. Pharmacol Biochem Behav 3:179–184
Barbaccia ML, Roscetti G, Trabucchi M, Mostallino MC, Concas A, Purdy RH, Biggio G (1996) Time-dependent changes in rat brain neuroactive steroid concentrations and GABAA receptor function after acute stress. Neuroendocrinology 63:166–172
Baron JA, Comi RJ, Cryns V, Brinck-Johnsen T, Mercer NG (1995) The effect of cigarette smoking on adrenal cortical hormones. J Pharmacol Exp Ther 272:151–155
Bitran D, Hilvers RJ, Kellogg CK (1991) Anxiolytic effects of 3 alpha-hydroxy-5 alpha[beta]-pregnan-20-one: endogenous metabolites of progesterone that are active at the GABAA receptor. Brain Res 561:157–161
Bitran D, Purdy RH, Kellogg CK (1993) Anxiolytic effect of progesterone is associated with increases in cortical allopregnanolone and GABAA receptor function. Pharmacol Biochem Behav 45:423–428
Bitran D, Shiekh M, McLeod M (1995) Anxiolytic effect of progesterone is mediated by the neurosteroid allopregnanolone at brain GABAA receptors. J Neuroendocrinol 7:171–177
Cam GR, Bassett JR (1983a) The effect of acute nicotine administration on plasma levels of the thyroid hormones and corticosterone in the rat. Pharmacol Biochem Behav 19:559–561
Cam GR, Bassett JR (1983b) The plasma levels of ACTH following exposure to stress or nicotine. Arch Int Pharmacodyn Ther 264:154–167
Chen H, Fu Y, Sharp BM (2008) Chronic nicotine self-administration augments hypothalamic–pituitary–adrenal responses to mild acute stress. Neuropsychopharmacology 33:721–730
Cheng SY, Glazkova D, Serova L, Sabban EL (2005) Effect of prolonged nicotine infusion on response of rat catecholamine biosynthetic enzymes to restraint and cold stress. Pharmacol Biochem Behav 82:559–568
Cooper KH, Meyer BU, Blide R, Pollock M, Gibbons L (1977) The important role of fitness determination and stress testing in predicting coronary incidence. Ann N Y Acad Sci 301:642–652
de Wit H, Schmitt L, Purdy R, Hauger R (2001) Effects of acute progesterone administration in healthy postmenopausal women and normally-cycling women. Psychoneuroendocrinology 26:697–710
Field AE, Colditz GA, Willett WC, Longcope C, McKinlay JB (1994) The relation of smoking, age, relative weight, and dietary intake to serum adrenal steroids, sex hormones, and sex hormone-binding globulin in middle-aged men. J Clin Endocrinol Metab 79:1310–1316
Folstein MF, Luria R (1973) Reliability, validity, and clinical application of the Visual Analogue Mood Scale. Psychol Med 3:479–486
Fuxe K, Andersson K, Eneroth P, Harfstrand A, Agnati LF (1989) Neuroendocrine actions of nicotine and of exposure to cigarette smoke: medical implications. Psychoneuroendocrinology 14:19–41
Genazzani AR, Petraglia F, Bernardi F, Casarosa E, Salvestroni C, Tonetti A, Nappi RE, Luisi S, Palumbo M, Purdy RH, Luisi M (1998) Circulating levels of allopregnanolone in humans: gender, age, and endocrine influences. J Clin Endocrinol Metab 83:2099–2103
Kiritsy-Roy JA, Mousa SA, Appel NM, Van Loon GR (1990) Tolerance to nicotine-induced sympathoadrenal stimulation and cross-tolerance to stress: differential central and peripheral mechanisms in rats. Neuropharmacology 29:579–589
Kirschbaum C, Wust S, Strasburger CJ (1992) ‘Normal’ cigarette smoking increases free cortisol in habitual smokers. Life Sci 50:435–442
Kirschbaum C, Strasburger CJ, Langkrar J (1993a) Attenuated cortisol response to psychological stress but not to CRH or ergometry in young habitual smokers. Pharmacol Biochem Behav 44:527–531
Kirschbaum C, Pirke KM, Hellhammer DH (1993b) The ‘Trier Social Stress Test’—a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28:76–81
Kirschbaum C, Scherer G, Strasburger CJ (1994) Pituitary and adrenal hormone responses to pharmacological, physical, and psychological stimulation in habitual smokers and nonsmokers. Clin Investig 72:804–810
MacDougall JM, Musante L, Castillo S, Acevedo MC (1988) Smoking, caffeine, and stress: effects on blood pressure and heart rate in male and female college students. Health Psychol 7:461–478
Mantsch JR, Cullinan WE, Tang LC, Baker DA, Katz ES, Hoks MA, Ziegler DR (2007) Daily cocaine self-administration under long-access conditions augments restraint-induced increases in plasma corticosterone and impairs glucocorticoid receptor-mediated negative feedback in rats. Brain Res 1167:101–111
Marx CE, Trost WT, Shampine L, Behm FM, Giordano LA, Massing MW, Rose JE (2006) Neuroactive steroids, negative affect, and nicotine dependence severity in male smokers. Psychopharmacology (Berl) 186:462–472
Matta SG, Fu Y, Valentine JD, Sharp BM (1998) Response of the hypothalamo–pituitary–adrenal axis to nicotine. Psychoneuroendocrinology 23:103–113
McNair D, Lorr M, Droppleman L (1971) Profile of mood states. Educational and Industrial Testing Service, San Diego
Mendelson JH, Sholar MB, Goletiani N, Siegel AJ, Mello NK (2005) Effects of low- and high-nicotine cigarette smoking on mood states and the HPA axis in men. Neuropsychopharmacology 30:1751–1763
Newhouse PA, Sunderland T, Narang PK, Mellow AM, Fertig JB, Lawlor BA, Murphy DL (1990) Neuroendocrine, physiologic, and behavioral responses following intravenous nicotine in nonsmoking healthy volunteers and in patients with Alzheimer’s disease. Psychoneuroendocrinology 15:471–484
Patchev VK, Shoaib M, Holsboer F, Almeida OF (1994) The neurosteroid tetrahydroprogesterone counteracts corticotropin-releasing hormone-induced anxiety and alters the release and gene expression of corticotropin-releasing hormone in the rat hypothalamus. Neuroscience 62:265–271
Patchev VK, Hassan AH, Holsboer DF, Almeida OF (1996) The neurosteroid tetrahydroprogesterone attenuates the endocrine response to stress and exerts glucocorticoid-like effects on vasopressin gene transcription in the rat hypothalamus. Neuropsychopharmacology 15:533–540
Paul SM, Purdy RH (1992) Neuroactive steroids. Faseb J 6:2311–2322
Perkins KA, Grobe JE, Fonte C, Breus M (1992) “Paradoxical” effects of smoking on subjective stress versus cardiovascular arousal in males and females. Pharmacol Biochem Behav 42:301–311
Peters RK, Cady LD Jr., Bischoff DP, Bernstein L, Pike MC (1983) Physical fitness and subsequent myocardial infarction in healthy workers. Jama 249:3052–3056
Pomerleau OF, Pomerleau CS (1990) Cortisol response to a psychological stressor and/or nicotine. Pharmacol Biochem Behav 36:211–213
Porcu P, Sogliano C, Cinus M, Purdy RH, Biggio G, Concas A (2003) Nicotine-induced changes in cerebrocortical neuroactive steroids and plasma corticosterone concentrations in the rat. Pharmacol Biochem Behav 74:683–690
Purdy RH, Moore PH Jr, Rao PN, Hagino N, Yamaguchi T, Schmidt P, Rubinow DR, Morrow AL, Paul SM (1990) Radioimmunoassay of 3 alpha-hydroxy-5 alpha-pregnan-20-one in rat and human plasma. Steroids 55:290–296
Purdy RH, Morrow AL, Moore PH Jr, Paul SM (1991) Stress-induced elevations of gamma-aminobutyric acid type A receptor-active steroids in the rat brain. Proc Natl Acad Sci USA 88:4553–4557
Roy MP, Steptoe A, Kirschbaum C (1994) Association between smoking status and cardiovascular and cortisol stress responsivity in healthy young men. Int J Behav Med 1:264–283
Schultheiss OC, Wirth MM, Stanton SJ (2004) Effects of affiliation and power motivation arousal on salivary progesterone and testosterone. Horm Behav 46:592–599
Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl) 158:343–359
Soderpalm AH, Lindsey S, Purdy RH, Hauger R, Wit de H (2004) Administration of progesterone produces mild sedative-like effects in men and women. Psychoneuroendocrinology 29:339–354
Spielberger C, Gorsuch R, Lushene R (1970) Manual for the State-Trait Anxiety Inventory. Consulting Psychologist Press, Washington, DC
Steptoe A, Ussher M (2006) Smoking, cortisol and nicotine. Int J Psychophysiol 59:228–235
Swan GE, Ward MM, Jack LM (1996) Abstinence effects as predictors of 28-day relapse in smokers. Addict Behav 21:481–490
Tiffany ST, Drobes DJ (1991) The development and initial validation of a questionnaire on smoking urges. Br J Addict 86:1467–1476
Tsuda A, Steptoe A, West R, Fieldman G, Kirschbaum C (1996) Cigarette smoking and psychophysiological stress responsiveness: effects of recent smoking and temporary abstinence. Psychopharmacology (Berl) 126:226–233
Uzunova V, Sheline Y, Davis JM, Rasmusson A, Uzunov DP, Costa E, Guidotti A (1998) Increase in the cerebrospinal fluid content of neurosteroids in patients with unipolar major depression who are receiving fluoxetine or fluvoxamine. Proc Natl Acad Sci USA 95:3239–3244
Wieland S, Lan NC, Mirasedeghi S, Gee KW (1991) Anxiolytic activity of the progesterone metabolite 5 alpha-pregnan-3 alpha-o1-20-one. Brain Res 565:263–268
Wirth MM, Schultheiss OC (2006) Effects of affiliation arousal (hope of closeness) and affiliation stress (fear of rejection) on progesterone and cortisol. Horm Behav 50:786–795
Wirth MM, Meier EA, Fredrickson BL, Schultheiss OC (2007) Relationship between salivary cortisol and progesterone levels in humans. Biol Psychol 74:104–107
Acknowledgments
These experiments complied with current US laws. The authors declare that they have no conflicts of interest. This research was supported by NIDA (DA02812) and the University of Chicago Hospital’s GCRC (USPHS MO1RR000555). We thank Ben Cunningham, Stephen Sittler, Lisa Vicini, Heather Phillips, and Nicholas Van Dam for their technical assistance.
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Childs, E., de Wit, H. Hormonal, cardiovascular, and subjective responses to acute stress in smokers. Psychopharmacology 203, 1–12 (2009). https://doi.org/10.1007/s00213-008-1359-5
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DOI: https://doi.org/10.1007/s00213-008-1359-5