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Allopregnanolone During Short-Term Smoking Abstinence: Associations with Depressive Symptoms, Smoking-Related Symptomatology and Nicotine Response

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Allopregnanolone During Short-Term Smoking Abstinence: Associations with Depressive Symptoms, Smoking-Related Symptomatology and Nicotine Response Allopregnanolone during Short-Term Smoking Abstinence: Associations with depressive symptoms, smoking-related symptomatology and nicotine response A Dissertation SUBMITTED TO THE FACULTY OF UNIVERSITY OF MINNESOTA BY Alicia Marie Allen IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Adviser: Harry Lando, PhD November, 2012 © Alicia Marie Allen, 2012 Acknowledgements This project was funded by National Institute on Drug Abuse (NIDA) Grants R01-DA08075 and R36-DA032539, and the J.B. Hawley Award (School of Public Health, University of Minnesota). Additional support comes from Grant Number 1UL1RR033183 from the National Center for Research Resources (NCRR) and by Grant Number 8UL1TR000114-02 from the National Center for Advancing Translational Sciences (NCATS) of the National Institutes of Health (NIH) to the University of Minnesota Clinical and Translational Science Institute (CTSI). The University of Minnesota CTSI is part of a national Clinical and Translational Science Award (CTSA) consortium created to accelerate laboratory discoveries into treatments for patients. Its contents are solely the responsibility of the authors, and do not necessarily represent the official views of CTSI, NIDA, NCRR, NCATS or NIH. Additional thanks go to the research staff – Lindsay Farnsworth, Kathryn Resner, Sara Paradise, Nicole Tosun, Jennifer Widenmier, and Danielle Young – for their dedication to participant recruitment and follow-up, as well as data collection, entry and management. Finally, I would also like to acknowledge Dr. Richard Hauger and Alan Turken at the University of California, San Diego for analyzing the allopregnanolone samples. i Abstract Background: Allopregnanolone (ALLO) is a neuroactive steroid metabolized from progesterone and, therefore, varies by menstrual phase in premenopausal women. Previously published literature has shown that risk for relapse to smoking varies by menstrual phase. Further, recent preclinical research indicates that ALLO may protect against drug abuse behaviors. Therefore, this dissertation project aims to characterize ALLO by menstrual phase in women with and without depressive symptoms (Paper #1) and explore the effect of ALLO on smoking-related symptomatology (SRS; Paper #2) and nicotine response (NR; Paper #3) during short-term smoking abstinence. Methods: At screening, participants (n=87) were stratified by depressive symptoms status and, using a controlled cross-over study design, were randomized to testing order (i.e., follicular (F) menstrual phase followed by the luteal (L) phase or vice versa (L-F)). The six-day testing week consisted of two days of ad libitum smoking followed by four days of biochemically verified smoking abstinence. ALLO was measured twice during each testing week: during ad libitum smoking and on the fourth day of smoking abstinence. Participants completed daily forms to assess SRS during the testing week. On the fourth day of smoking abstinence, participants participated in a NR lab session. Growth curve and covariance pattern models, adjusted for menstrual phase and testing order, were used to assess the effect of ALLO on SRS and NR, respectively. Results: In the first paper (n=84), a significant menstrual phase difference was observed in the change in ALLO level during smoking cessation. Specifically, ALLO decreased by 10% in the F phase and increased by 31% in the L phase (p<0.01). There were no significant differences in ALLO levels between the depressive symptoms groups. In the second paper (n=64), the absolute level of ii ALLO on the day before quit was significantly associated with the following: (1) perceived stress on the day before quit ( β=-2.25, p<0.01), (2) the change in perceived stress during smoking abstinence (β=0.79, p<0.01), and (3) premenstrual symptoms of pain and water retention on the day before quit (β=1.09, p<0.01; β=1.08, p<0.01; respectively). The change in ALLO during smoking abstinence was significantly associated with the following: (1) positive and negative affect on the day before quit ( β=1.15, p<0.01; β=1.04, p=0.04; respectively), (2) perceived stress on the day before quit ( β=-1.77, p=0.01), (3) the change in perceived stress during smoking cessation (β=0.17, p<0.01), and (4) the change in depressive symptoms on the day of quit ( β=-1.52, p=0.02). Finally, in the third paper (n=77), ALLO had a significant, positive association with the following variables prior to initiation of nicotine nasal spray: systolic blood pressure ( β=0.85, p=0.04), diastolic blood pressure ( β=1.19, p<0.01), and subjective levels of physical symptoms ( β=0.58, p<0.01), dizziness ( β =0.88, p<0.01), jitteriness ( β=0.90, p=0.04) and pleasantness ( β=2.05, p=0.041). ALLO also had significant associations with changes in cognition from baseline to post nicotine nasal spray use: specifically, discriminability (a measure of attention; β=1.15, p=0.05), and bias (a measure of impulsivity; β=0.12, p=0.02). Conclusion: ALLO varied significantly by menstrual phase and smoking status, and had a significant effect on several measures of SRS and NR. While several of these associations were favorable (i.e., perceived stress on the day before quit and pleasantness on the fourth day of smoking abstinence), some were not (i.e., premenstrual symptoms on the day before quit and increased subjective report of physical symptoms on the fourth day of smoking abstinence). Therefore, it remains unknown whether or not ALLO is a protective factor against drug abuse behaviors. Additional research is needed to explore the role of ALLO directly on smoking cessation outcomes. iii Table of Contents Page Number List of Tables vi List of Figures vii A. Introduction 1 B. Significance, Background & Innovation 4 C. Parent Study Overview 12 D. Pape r #1: The Role of Menstrual Phase and Depressive Symptoms Status on 17 Allopregnanolone Levels during Short-Term Smoking Abstinence D.1. Overview 17 D.2. Background & Significance 18 D.3. Methods 20 D.4. Results 23 D.5. Summary of Results 24 E. Paper #2: Allopregnanolone and Smoking - Related Symptomatology during Short-Term 25 Smoking Abstinence E.1. Overview 25 E.2. Background & Significance 27 E.3. Methods 29 E.4. Results 31 E.3. Summary of Results 33 F. Paper #3: Allopregnanolon e and Nicotine Response during Short-Term Smoking 37 Abstinence F.1. Overview 37 F.2. Background & Significance 39 F.1. Methods 41 F.2. Results 44 F.3. Summary of Results 46 iv G. Discussion 47 G.1. Overview 47 G.2. Menstrual Phase 47 G.3. Depressive Symptoms 49 G.4. Perceived Stress 52 G.5. Premenstrual Symptoms 53 G.6. Smoking-Specific Symptomatology 54 G.7. Other Nicotine Response Measures 55 G.8. Strengths & Limitations 57 G.9. Future Directions 58 G.10. Conclusions 59 H. References 60 v List of Tables Page Number Table 1. Study Measures 13 Table 2. Frequency of Depressive Symptoms Status by Classification Tool 21 Table 3. Demographics & Smoking Behavior by 23 Depressive Symptoms Status (n=84) Table 4. Allopregnanolone (ng/mL) by Menstrual Phase, Smoking Status and Depressive Symptoms 24 Status (n=84) Table 5. Demographics, Smoking Behavior & Allopregnanolone Levels (n=64) 31 Table 6. Associations between Smoking-Related Symptomatology and Allopregnanolone (n=64) 34 Table 7. Demographics, Smoking Behavior & Allopregnanolone Levels (n=77) 44 Table 8. Associations between Nicotine Response 45 Variables and Allopregnanolone (n=77) vi List of Figures Page Number Figure 1. Estimated Estrogen and Progesterone Values during the Human Menstrual Cycle 5 Figure 2. Estimated Allopregnanolone Levels during the Human Menstrual Cycle 7 Figure 3. Central Hypothesis 11 Figure 4. Parent Study Flow Diagram 12 Figure 5. Nicotine Exposure Session Protocol 14 Figure 6. Smoking-Related Symptomatology during Short-Term Smoking Cessation by Allopregnanolone 35 Level on Day 2 (n=64) Figure 7. Smoking-Related Symptomatology during Short-Term Smoking Cessation by Change in 36 Allopregnanolone Level from Day 2 to Day 6 (n=64) vii A. INTRODUCTION Cigarette smoking persists as the leading cause of preventable morbidity and mortality in the United States (CDC, 2010). Despite the many advancements in smoking cessation interventions, the majority of smokers, especially women, relapse soon after a quit attempt (Benowitz, 2009; CDC, 2010; Perkins et al 2001; Perkins & Scott, 2008; USDHHS, 2001). Evidence continues to accumulate suggesting that sex hormones may influence risk for smoking relapse (e.g. Lynch & Sofuoglu, 2011). Recently, new efforts have begun to focus on the role of allopregnanolone (ALLO), which is a stress-reducing neuroactive steroid. ALLO is primarily, though not exclusively, metabolized from the sex hormone progesterone (Backstrom et al 1986; Ottander et al, 2005). Therefore, the level in ALLO in women varies by menstrual phase such that it is lower in the follicular phase (i.e., low progesterone) and higher in the luteal phase (i.e., high progesterone; Genazzani et al 1998; Nyberg et al 2007). Within the animal literature, ALLO has been found to have protective effects against the drug abuse behaviors of escalation, reinstatement, and withdrawal; some of these associations varied by sex (Anker et al, 2008; Carroll & Anker, 2010). Although ALLO has been shown to be associated with a variety of smoking relapse risk factors (including depressive symptoms, smoking-related symptomatology and variables associated with nicotine response), there is currently a lack of clinical research on the role of ALLO in addictive behaviors. Therefore, the goal of this doctoral dissertation is to conduct a series of 1 secondary-data analyses to investigate the role of menstrual-timed endogenous levels of ALLO on these smoking relapse risk factors. The “Menstrual Phase and Depressive Symptoms in Acute Smoking Abstinence” (MPADS; 2006-2012) incorporated a controlled cross-over study design to collect data from women smokers with and without depressive symptoms during both the follicular (F; low ALLO) and luteal (L; high ALLO) menstrual phases.
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