The effects of exogenous progesterone on drug craving and stress arousal in cocaine dependence: Impact of gender and cue type

Psychoneuroendocrinology

Volumn 38, Issue 9, 2013, Pages 1532-1544

  Fox, Helen C ^a   Sofuoglu, Mehmet ^b   Morgan, Peter T ^a   Tuit, Keri L ^a   Sinha, Rajita ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

Cocaine dependence; Drug cue; Gender; Progesterone; Stress; Stroop

Indexed keywords

HYDROCORTISONE; PLACEBO; PROGESTERONE;

ADULT; ANXIETY; AROUSAL; ARTICLE; CLINICAL ARTICLE; COCAINE DEPENDENCE; CONTROLLED STUDY; DIZZINESS; DOUBLE BLIND PROCEDURE; DRUG EFFICACY; DRUG RESPONSE; EMOTIONALITY; FEMALE; GUIDED IMAGERY; HEADACHE; HEART OUTPUT; HORMONE RESPONSE; HUMAN; HYDROCORTISONE BLOOD LEVEL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INHIBITION (PSYCHOLOGY); LOSS OF APPETITE; MALE; MENTAL PERFORMANCE; MENTAL STRESS; MOOD CHANGE; NAUSEA; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SEX DIFFERENCE; SIDE EFFECT; STROOP TEST; WEIGHT GAIN; WITHDRAWAL SYNDROME;

COCAINE DEPENDENCE; DRUG CUE; GENDER; PROGESTERONE; STRESS; STROOP;

ADRENOCORTICOTROPIC HORMONE; ADULT; AFFECT; ALCOHOL DRINKING; ANXIETY; AROUSAL; BLOOD PRESSURE; COCAINE-RELATED DISORDERS; COMORBIDITY; CUES; DEPRESSION; DOUBLE-BLIND METHOD; EMOTIONS; ESTRADIOL; FEMALE; HEART RATE; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMAGERY (PSYCHOTHERAPY); MALE; MIDDLE AGED; PITUITARY-ADRENAL SYSTEM; PROGESTERONE; RELAXATION THERAPY; SEX CHARACTERISTICS; SMOKING; STRESS, PSYCHOLOGICAL; STROOP TEST;

EID: 84883653672     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2012.12.022     Document Type: Article

References (94)

1. Altemus M., Redwine L., Leong Y.M., Yoshikawa T., Yehuda R., Detera-Wadleigh S., Murphy D.L. Reduced sensitivity to glucocorticoid feedback and reduced glucocorticoid receptor mRNA expression in the luteal phase of the menstrual cycle. Neuropsychopharmacology 1997, 17:100-109.
2. Anker J.J., Carroll M.E. Females are more vulnerable to drug abuse than males: evidence from preclinical studies and the role of ovarian hormones. Curr. Top. Behav. Neurosci. 2011, 8:73-96.
3. Anker J.J., Holtz N.A., Carroll M.E. Effects of progesterone on escalation of intravenous cocaine self-administration in rats selectively bred for high or low saccharin intake. Behav. Pharmacol. 2012, 23(2):205-210.
4. Anker J.J., Holtz N.A., Zlebnik N., Carroll M.E. Effects of allopregnanolone on the reinstatement of cocaine-seeking behavior in male and female rats. Psychopharmacology (Berl) 2009, 203(1):63-72.
5. Anker J.J., Larson E.B., Gliddon L.A., Carroll M.E. Effects of progesterone on the reinstatement of cocaine-seeking behavior in female rats. Drug Alcohol Depend. 2007, 107:264-267.
6. Back S.E., Brady K.T., Jackson J.L., Salstrom S., Zinzow H. Gender differences in stress reactivity among cocaine-dependent individuals. Psychopharmacology (Berl) 2005, 180:169-176.
7. Becker J.B. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol. Biochem. Behav. 1999, 64:803-812. Review.
8. Becker J.B., Hu M. Sex differences in drug abuse. Front. Neuroendocrinol. 2008, 29:6-47.
9. Brennan A.R., Arnsten A.F. Neuronal mechanisms underlying attention deficit hyperactivity disorder: the influence of arousal on prefrontal cortical function. Ann. N. Y. Acad. Sci. 2008, 1129:236-245. Review.
10. Chabbert Buffet N., Djakoure C., Maitre S.C., Bouchard P. Regulation of the human menstrual cycle. Front. Neuroendocrinol. 1998, 19:151-186.
11. Chaplin T., Hong K.-I., Bergquist K., Sinha R. Gender differences in response to emotional stress: an assessment across subjective, behavioral, and physiological domains and relations to alcohol craving. Alcohol Clin. Exp. Res. 2008, 32:1242-1250.
12. Chaplin T.M., Hong K., Fox H.C., Siedlarz K.M., Bergquist K., Sinha R. Behavioral arousal in response to stress and drug cue in alcohol and cocaine addicted individuals versus healthy controls. Hum. Psychopharmacol. 2010, 25:368-376.
13. Childs E., Van Dam N.T., de Wit H. Effects of acute progesterone administration upon responses to acute psychosocial stress in men. Exp. Clin. Psychopharmacol. 2010, 18(1):78-86.
14. Collins S.L., Evans S.M., Foltin R.W., Haney M. Intranasal cocaine in humans: effects of sex and menstrual cycle. Pharmacol. Biochem. Behav. 2007, 86:117-124.
15. de Wit H. Sex hormones: a new treatment for cocaine abuse?. Neuropsychopharmacology 2011, 36(11):2155-2156.
16. Earle T.L., Linden W., Weinberg J. Differential effects of harassment on cardiovascular and salivary cortisol stress reactivity and recovery in women and men. J. Psychosom. Res. 1999, 46:125-141.
17. Ekman P., Davidson R.J., Friesen W.V. The Duchenne smile: emotional expression and brain physiology. II. J. Pers. Soc. Psychol. 1990, 58:342-353.
18. Ekman P., Scherer K. Questions about emotion: an introduction. Approaches to Emotion 1984, 1-8. Lawrence Erlbaum, Hillsdale, NJ. K. Scherer, P. Ekman (Eds.).
19. Evans S.M., Foltin R.W. Exogenous progesterone attenuates the subjective effects of smoked cocaine in women, but not in men. Neuropsychopharmacology 2006, 31:659-674.
20. Evans S.M., Foltin R.W. Does the response to cocaine differ as a function of sex or hormonal status in human and non-human primates?. Horm. Behav. 2010, 58:13-21.
21. Evans S.M., HaneyM, Foltin R.W. The effects of smoked cocaine during the follicular and luteal phases of the menstrual cycle in women. Psychopharmacology (Berl) 2002, 159:397-406.
22. Feltenstein M.W., Byrd E.A., Henderson A.R., See R.E. Attenuation of cocaine-seeking by progesterone treatment in female rats. Psychoneuroendocrinology 2009, 34:343-352.
23. First M.B., Spitzer R.L., Gibbon M., Williams J.B.W. Structured Clinical Interview for the DSM-IV Axis I Disorders Patient Edition (SCID-I/P, Version 20, 4/97 Revision) 1997, New York State Psychiatric Institute, New York.
24. Fox H.C., Bergquist K.L., Hong K.I., Sinha R. Stress-induced and alcohol cue-induced craving in recently abstinent alcohol dependent individuals. Alcoholism: Clinical and Experimental Research 2007, 31:395-403.
25. Fox H.C., Hong K.A., Paliwal P., Morgan P.T., Sinha R. Altered levels of sex and stress steroid hormones assessed daily over a 28-day cycle in early abstinent cocaine-dependent females. Psychopharmacology (Berl) 2008, 195:527-536.
26. Fox H.C., Hong K.A., Siedlarz K.M., Sinha R. Enhanced sensitivity to stress and drug/alcohol craving in abstinent cocaine dependent individuals compared to social drinkers. Neuropsychopharmacology 2008, 33:796-805.
27. Fox H.C., Hong K.I., Siedlarz K., Bergquist K.L., Anderson G.M., Kreek M.J., Sinha R. Gender dissociations in autonomic and HPA responses to stress and cues in alcohol dependent patients with cocaine abuse. Alcohol Alcohol. 2009, 44:575-585.
28. Fox H., Seo D., Tuit K., Hansen J., Kimmerling A., Morgan P.T., Sinha R. Guanfacine effects on stress, drug craving and prefrontal activation in cocaine dependent individuals: preliminary findings. J. Psychopharmacol. 2012, Feb 1 [Epub ahead of print].
29. Fox H.C., Sinha R. Sex differences in drug-related stress system changes: implications for treatment in substance-abusing women. Harv. Rev. Psychiatry 2009, 17:103-119.
30. Fox H.C., Talih M., Malison R., Anderson G.M., Kreek M.J., Sinha R. Frequency of recent cocaine and alcohol use affects drug craving and associated responses to stress and to drug-related cues. Psychoneuroendocrinology 2005, 30:880-891.
31. Frankenhaeuser M., von Wright M.R., Collins A., von Wright J., Sedvall G., Swahn C.G. Sex differences in psychoneuroendocrine reactions to examination stress. Psychosom. Med. 1978, 40:334-343.
32. Galliven E.A., Singh A., Michelson D., Bina S., Gold P.W., Deuster P.A. Hormonal and metabolic responses to exercise across time of day and menstrual cycle phase. J. Appl. Physiol. 1997, 83:1822-1831.
33. Golden C.J. Identification of brain disorders by the Stroop Color and Word Test. J. Clin. Psychol. 1976, 32:654-658.
34. Hariri A.R., Tessitore A., Mattay V.S., Fera F., Weinberger D.R. The amygdala response to emotional stimuli: a comparison of faces and scenes. Neuroimage 2002, 17:317-323.
35. Hudson A., Stamp J.A. Ovarian hormones and propensity to drug relapse: a review. Neurosci. Biobehav. Rev. 2011, 35:427-436.
36. Izard C. Patterns of Emotions: A New Analysis of Anxiety and Depression 1972, Academic Press, New York.
37. Justice A.J., de Wit H. Acute doses of d-amphetamine during the follicular and luteal phases of the menstrual cycle in women. Psychopharmacology (Berl) 1999, 145:67-75.
38. Justice A.J., de Wit H. Acute effects of d-amphetamine during the early and late follicular phases of the menstrual cycle in women. Pharmacol. Biochem. Behav. 2000, 66:509-515.
39. Keller-Wood M., Silbiger J., Wood C.E. Progesterone attenuates the inhibition of adrenocorticotropin responses by cortisol in nonpregnant ewes. Endocrinology 1988, 123:647-651.
40. Kirschbaum C., Kudielka B.M., Gaab J., Schommer N.C., Hellhammer D.H. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom. Med. 1999, 6:154-162.
41. Kirschbaum C., Pirke K.M., Hellhammer D.H. Preliminary evidence for reduced cortisol responsivity to psychological stress in women using oral contraceptive medication. Psychoneuroendocrinology 1995, 20:509-514.
42. Kouri E.M., Lundahl L.H., Borden K.N., McNeil J.F., Lukas S.E. Effects of oral contraceptives on acute cocaine response in female volunteers. Pharmacol. Biochem. Behav. 2002, 74:173-180.
43. Laird N.M., Ware J.H. Random-effects models for longitudinal data. Biometrics 1982, 38:963-974.
44. Lang P.J., Kozak M.J., Miller G.A., Levin D.N., McLean A. Emotional imagery: conceptual structure and pattern of somato-visceral response. Psychophysiology 1980, 17:179-192.
45. Lang P.J., Levin D.N., Miller G.A., Kozak M.J. Fear behavior, fear imagery, and the psychophysiology of emotion: the problem of affective response integration. J. Abnorm. Psychol. 1983, 92:276-306.
46. Larson E.B., Anker J.J., Gliddon L.A., Fons K.L., Carroll M.E. Effects of estrogen and progesterone on the escalation of cocaine self-administration in female rats during extended access. Exp. Clin. Psychopharmacol. 2007, 15:461-471.
47. Lee D.Y., Kim J.-Y., Kim J.-H., Choi D.-S., Kim D.-K., Koh K.K., Yoon B-k. Effects of hormone therapy on ambulatory blood pressure in postmenopausal Korean women. Climacteric 2011, 14:92-99.
48. Lindheim S.R., Legro R.S., Morris R.S., Wong I.L., Tran D.Q., Vijod M.A., Stanczyk F.Z., Lobo R.A. The effect of progestins on behavioral stress responses in postmenopausal women. J. Soc. Gynecol. Investig. 1994, 1(1):79-83.
49. Matthews K.A., Owens J.F., Salomon K., Harris K.F., Berga S.L. Influence of hormone therapy on the cardiovascular responses to stress of postmenopausal women. Biol. Psychol. 2005, 69:39-56.
50. McCance-Katz E.F., Carroll K.M., Rounsaville B.J. Gender differences in treatment-seeking cocaine abusers - implications for treatment and prognosis. Am. J. Addict. 1999, 8:300-311.
51. McCance-Katz E.F., Hart C.L., Boyarsky B., Kosten T., Jatlow P. Gender effects following repeated administration of cocaine and alcohol in humans. Subst. Use Misuse 2005, 40(4):511-528.
52. Mendelson J.H., Mello N.K., Sholar M.B., Siegel A.J., KaufmanMJ, Levin J.M. Cocaine pharmacokinetics in men and in women during the follicular and luteal phases of the menstrual cycle. Neuropsychopharmacology 1999, 21:294-303.
53. Mercer D., Carpenter G., Daley D., Patterson C., Volpicelli J. Group Drug Counseling Manual 1994, University of Pennsylvania.
54. Miller G.A., Levi D., Kozak M., Cook E.W., McLean A., Lang P.J. Individual differences in imagery and the psychophysiology of emotion. Cogn. Emot. 1987, 1:367-390.
55. Montoya P., Campos J.J., Schandry R. See red? Turn pale? Unveiling emotions through cardiovascular and hemodynamic changes. Span. J. Psychol. 2005, 8:79-85.
56. Morris J.S., Öhman A., Dolan R. Conscious and unconscious emotional learning in the human amygdala. Nature 1998, 393:467-470.
57. Patkar A.A., Mannelli P., Peindl K., Murray H.W., Meier B., Leone F.T. Changes in tobacco smoking following treatment for cocaine dependence. Am. J. Drug Alcohol Abuse 2006, 32:135-148.
58. Phan K.L., Wager T., Taylor S.F., Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 2002, 16:331-348.
59. Quinones-Jenab V. Why are women from venus and men from mars when they abuse cocaine?. Brain Res. 2006, 1126:200-203.
60. Quinones-Jenab V., Jenab S. Progesterone attenuates cocaine-induced responses. Horm. Behav. 2010, 58(1):22-32.
61. Reed S.C., Evans S.E., Bedi G., Rubin E., Foltin R. The effects of oral micorinized progesterone on smoked cocaine self-administration in women. Horm. Behav. 2011, 59:227-235.
62. Rupprecht R. Neuroactive steroids: mechanisms of action and neuropsychopharmacological properties. Psychoneuroendocrinology 2003, 28(2):139-168.
63. Russo S.J., Sun W.L., Minerley A.C., Weierstall K., Nazarian A., Festa E.D., Niyomchai T., Akhavan A., Jenab S., Quiñones-Jenab V. Progesterone does not affect cocaine-induced conditioned place preference or locomotor activity in male rats. Ethn. Dis. 2010, 20(Suppl. 1). S1-73-77.
64. Russo S.J., Sun W.L., Minerly A.C., Weierstall K., Nazarian A., Festa E.D., Niyomchai T., Akhavan A., Luine V., Jenab S., Quiñones-Jenab V. Progesterone attenuates cocaine-induced conditioned place preference in female rats. Brain Res. 2008, 1189:229-235.
65. Substance Abuse and Mental Health Services Administration. Overview of findings from the 2006 National Survey on Drug Use and Health [Office of Applied Studies, NHSAA Series H-21; DHHS pub. no. SMA 03-3774]. Rockville, MD: SAMHSA, 2007.
66. Substance Abuse and Mental Health Services Administration. (2010). Results from the 2009 National Survey on Drug Use and Health: Volume I. Summary of National Findings (Office of Applied Studies, NSDUH Series H-38A, HHS Publication No. SMA 10-4586 Findings). Rockville, MD.
67. Sarnyai Z., Shaham Y., Heinrichs S.C. The role of cortocotropin-releasing factor in drug addiction. Pharmocol. Rev. 2001, 53:209-243.
68. Schwartz G.E., Weinberger D.A., Singer J.A. Cardiovascular differentiation of happiness, sadness, anger, and fear following imagery and exercise. Psychosom. Med. 1981, 43:343-364.
69. Sinha R. Modeling stress and drug craving in the laboratory: implications for addiction treatment development. Addict. Biol. 2009, 14:84-98.
70. Sinha R., Fox H.C., Hong K.I., Hansen J., Tuit K., Kreek M.J. Effects of adrenal sensitivity, stress- and cue-induced craving, and anxiety on subsequent alcohol relapse and treatment outcomes. Arch. Gen. Psychiatry 2011, 68:942-952.
71. Sinha R., Fox H.C., Paliwal P., Hong K.A., Morgan P.T., Bergquist K.L. Sex steroid hormones, stress response and drug craving in cocaine dependent women: implications for relapse susceptibility. Exp. Clin. Psychopharmacol. 2007, 15:445-452.
72. Sinha R., Fuse T., Aubin L.R., O'Malley S.S. Psychological stress, drug-related cues and cocaine craving. Psychopharmacology (Berl) 2000, 152:140-148.
73. Sinha R., Fox H.C., Hong K.A., Bergquist K.L., Bhagwagar Z., Siedlarz K. Enhanced negative emotion and alcohol craving, and altered physiological responses following stress and cue exposure in alcohol dependent individuals. Neuropsychopharmacology 2009, 34:1198-1208.
74. Sinha R., Garcia M., Paliwal P., Kreek M.J., Rounsaville B.J. Stress-induced cocaine craving and hypothalamic-pituitary-adrenal responses are predictive of cocaine relapse outcomes. Arch. Gen. Psychiatry 2006, 63:324-331.
75. Sinha R., Lovallo W.R., Parsons O.A. Cardiovascular differentiation of emotions. Psychosom. Med. 1992, 54:422-435.
76. Sinha R., Talih M., Malison R., Cooney N., Anderson G.M., Kreek M.J. Hypothalamic-pituitary-ACDrenal axis and sympatho-ACDreno-medullary responses during stress-induced and drug cue-induced cocaine craving states. Psychopharmacology (Berl) 2003, 170:62-72.
77. Sita A., Miller S.B. Estradiol, progesterone and cardiovascular response to stress. Psychoneuroendocrinology 1996, 21:339-346.
78. Sofuoglu M., Babb D.A., Hatsukami D.K. Effects of progesterone treatment on smoked cocaine response in women. Pharmacol. Biochem. Behav. 2002, 72:431-435.
79. Sofuoglu M., Dudish-Poulsen S., Nelson D., Pentel P.R., Hatsukami D.K. Sex and menstrual cycle differences in the subjective effects from smoked cocaine in humans. Exp. Clin. Psychopharmacol. 1999, 7:274-283.
80. Sofuoglu M., Mitchell E., Kosten T.R. Effects of progesterone treatment on cocaine responses in male and female cocaine users. Pharmacol. Biochem. Behav. 2004, 78:699-705.
81. Sofuoglu M., Poling J., Gonzalez G., Gonsai K., Oliveto A., Kosten T.R. Progesterone effects on cocaine use in male cocaine users maintained on methadone: a randomized, double-blind, pilot study. Exp. Clin. Psychopharmacol. 2007, 15(5):453-460.
82. Stout R.L., Wirtz P.W., Carbonari J.P., Del Boca F.K. Ensuring balanced distribution of prognostic factors in treatment outcome research. J. Stud. Alcohol. Suppl. 1994, 12:70-75.
83. Svec F. The biopotency of dexamethasone at causing hepatic glucocorticoid receptor down-regulation in the intact mouse. Biochim. Biophys. Acta 1988, 970(1):90-95.
84. Tersman Z., Collins A., Eneroth P. Cardiovascular responses to psychological and physiological stressors during the menstrual cycle. Psychosom. Med. 1991, 53:185-197.
85. Tiffany S.T., Singleton E., Haertzen C.A., Henningfield J.E. The development of the cocaine craving questionnaire. Drug Alcohol Depend. 1993, 34:19-28.
86. van Wingen G.A., van Broekhoven F., Verkes R.J., Petersson K.M., Bäckström T., Buitelaar J.K., Fernández G. Progesterone selectively increases amygdala reactivity in women. Mol. Psychiatry 2008, 13(3):325-333.
87. Waldrop A.E., Back S.E., Brady K.T., Upadhyaya H.P., McRae A.L., Saladin M.E. Daily stressor sensitivity, abuse effects, and cocaine use in cocaine dependence. Addict. Behav. 2007, 32:3015-3025.
88. Waldrop A.E., Price K.L., Desantis S.M., Simpson A.N., Back S.E., McRae A.L., Spratt E.G., Kreek M.J., Brady K.T. Community-dwelling cocaine-dependent men and women respond differently to social stressors versus cocaine cues. Psychoneuroendocrinology 2010, 35:798-806.
89. Wei L.J. The adaptive biased-coin design for sequential experiments. Ann. Stat. 1978, 6:92-100.
90. Wei L.J., Lachin J.M. Properties of the urn randomization in clinical trials. Control. Clin. Trials 1988, 9(4):345-364. 1988 Dec, Erratum in: Controlled Clin Trials 10(1):following 126.
91. Witkiewitz K., Marlatt G.A. Emphasis on interpersonal factors in a dynamic model of relapse. Am. Psychol. 2005, 60(4):341-342.
92. Whalen P.J., Rauch S.L., Etcoff N.L., McInerney S.C., Lee M.B., Jenike M.A. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J. Neurosci. 1998, 18:411-418.
93. Young E.A., Altemus M., Parkison V., Shastry S. Effects of estrogen antagonists and agonists on the ACTH response to restraint stress in female rats. Neuropsychopharmacology 2001, 25:881-891.
94. Zumoff B., Miller L., Levin J., Levit C.D., Miller E.H., Heinz U., Kalin M., Denman H., Jandorek R., Rosenfeld R.S. Follicular-phase serum progesterone levels of nonsmoking women do not differ from the levels of nonsmoking men. Steroids 1990, 55:557-559.