Advertisement

Therapeutic challenges for concurrent ethanol and nicotine consumption: naltrexone and varenicline fail to alter simultaneous ethanol and nicotine intake by female alcohol-preferring (P) rats

  • Robert A. Waeiss
  • Christopher P. Knight
  • Sheketha R. Hauser
  • Lauren A. Pratt
  • William J. McBride
  • Zachary A. RoddEmail author
Original Investigation

Abstract

Rationale and objectives

Simultaneous alcohol and nicotine consumption occurs in the majority of individuals with alcohol use disorder (AUD) and nicotine dependence. Varenicline (Var) is used to assist in the cessation of nicotine use, while naltrexone (Nal) is the standard treatment for AUD. Despite evidence that ethanol (EtOH) and nicotine (NIC) co-use produces unique neuroadaptations, preclinical research has focused on the effects of pharmacotherapeutics on a single reinforcer. The current experiments examined the effects of Var and Nal on EtOH, NIC, or EtOH+NIC intake.

Methods

Animals were randomly assigned to one of four drinking conditions of 24-h access to a three-bottle choice paradigm, one of which always contained water. Drinking conditions were water only, 0.07 and 0.14 mg/mL NIC (NIC only), 15% and 30% EtOH (EtOH only), or 15% and 30% EtOH with 0.14 mg/mL NIC (EtOH+NIC). The effects of Var (0, 1, or 2 mg/kg) or Nal (0, 1, or 10 mg/kg) injections on maintenance and relapse consumption were determined during four consecutive days.

Results

Var reduced maintenance and relapse NIC intake but had no effect on EtOH or EtOH+NIC drinking. Conversely, Nal reduced EtOH maintenance and relapse drinking, but had no effect on NIC or EtOH+NIC drinking.

Discussion

The results indicate the standard pharmacological treatments for nicotine dependence and AUD were effective at reducing consumption of the targeted reinforcer but neither reduced EtOH+NIC co-use/abuse. These findings suggest that co-abuse may promote unique neuroadaptations that require models of polysubstance abuse to develop pharmacotherapeutics to treat AUD and nicotine dependence.

Keywords

Alcohol-preferring (P) rats Alcohol Ethanol Nicotine Co-abuse Varenicline Naltrexone Maintenance Relapse Addiction 

Notes

Funding information

This study was supported by NIAAA grants AA07611, AA07462, AA10721, AA20908, and AA019366.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

213_2019_5174_MOESM1_ESM.pdf (236 kb)
ESM 1 (PDF 236 kb)

References

  1. Agboola SA, Coleman T, McNeill A, Leonardi-Bee J (2015) Abstinence and relapse among smokers who use varenicline in a quit attempt-a pooled analysis of randomized controlled trials. Addiction 110(7):1182–1193PubMedCrossRefGoogle Scholar
  2. Baker TB, Piper ME, Stein JH, Smith SS, Bolt DM, Fraser DL, Fiore MC (2016) Effects of nicotine patch vs varenicline vs combination nicotine replacement therapy on smoking cessation at 26 weeks: A randomized clinical trial. JAMA 315(4):371–379Google Scholar
  3. Benowitz NL (1988) Pharmacologic aspects of cigarette smoking and nicotine addiction. N Engl J Med 319:1318–1330PubMedCrossRefGoogle Scholar
  4. Biala G, Budzynska B, Kruk M (2005) Naloxone precipitates nicotine abstinence syndrome and attenuates nicotine-induced antinociception in mice. Pharmacol Rep 57(6):755–760PubMedGoogle Scholar
  5. Blomqvist O, Engel JA, Nissbrandt H, Soderpalm B (1993) The mesolimbic dopamine-activating properties of ethanol are antagonized by mecamylamine. Eur J Pharmacol 249:207–213PubMedCrossRefGoogle Scholar
  6. Breese GR, Chu K, Dayas CV, Funk D, Knapp DJ, Koob GF, Lê DA, O’Dell LE, Overstreet DH, Roberts AJ, Sinha R, Valdez GR, Weiss F (2005) Stress enhancement of craving during sobriety: a risk for relapse. Alcohol Clin Exp Res 29(2):185–195PubMedPubMedCentralCrossRefGoogle Scholar
  7. Ceylan-Isik AF, McBride SM, Ren J (2010) Sex difference in alcoholism: who is at a greater risk for development of alcoholic complication? Life Sci 87:133–138PubMedPubMedCentralCrossRefGoogle Scholar
  8. Chi H, de Wit H (2003) Mecamylamine attenuates the subjective stimulant-like effects of alcohol in social drinkers. Alcohol Clin Exp Res 27:780–786PubMedCrossRefGoogle Scholar
  9. Clark A, Little HJ (2004) Interactions between low concentrations of ethanol and nicotine on firing rate of ventral tegmental dopamine neurones. Drug Alcohol Depend 75(2):199–206PubMedCrossRefGoogle Scholar
  10. Corrigall WA, Coen KM, Adamson KL (1994) Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res 653(1–2):278–284PubMedCrossRefPubMedCentralGoogle Scholar
  11. Covey LS, Glassman AH, Stetner F (1999) Naltrexone effects on short-term and long-term smoking cessation. J Addict Dis 18(1):31–40PubMedCrossRefGoogle Scholar
  12. Czachowski CL, Froehlich JC, DeLory M (2018) The effects of long-term varenicline administration on ethanol and sucrose seeking and self-administration in male P rats. Alcohol Clin Exp Res 42(2):453–460PubMedCrossRefGoogle Scholar
  13. Daeppen JB, Smith TL, Danko GP, Gordon L, Landi NA, Nurnberger JI, Bucholz KK, Raimo E, Schuckit MA (2000) Clinical correlates of cigarette smoking and nicotine dependence in alcohol-dependent men and women. Alcohol Alcohol 35(2):171–175PubMedCrossRefGoogle Scholar
  14. David SP, Chu IM, Lancaster T, Stead LF, Evins AE, Prochaska JJ (2014) Systematic review and meta-analysis of opioid antagonists for smoking cessation. BMJ Open 4(3):e004393PubMedPubMedCentralCrossRefGoogle Scholar
  15. de Bejczy A, Löf E, Walther L, Guterstam J, Hammarberg A, Asanovska G, Franck J, Isaksson A, Söderpalm B (2015) Varenicline for treatment of alcohol dependence: a randomized, placebo-controlled trial. Alcohol Clin Exp Res 39(11):2189–2199PubMedCrossRefGoogle Scholar
  16. Deehan GJ, Hauser SR, Waeiss RA, Knight CP, Toalston JE, Truitt WA, McBride WJ, Rodd ZA (2015) Co-administration of ethanol and nicotine: the enduring alterations in the rewarding properties of nicotine and glutamate activity within the mesocorticolimbic system of female alcohol-preferring (P) rats. Psychopharmacology 232(23):4293–4302PubMedPubMedCentralCrossRefGoogle Scholar
  17. Delnevo CD, Wackowski OA, Giovenco DP, Manderski MT, Hrywna M, Ling PM (2012) Examining market trends in the United States smokeless tobacco use: 2005–2011. Tob ControlGoogle Scholar
  18. Dhaher R, Toalston JE, Hauser SR, Bell RL, McKinzie DL, McBride WJ, Rodd ZA (2012) Effects of naltrexone and LY255582 on ethanol maintenance, seeking, and relapse responding by alcohol-preferring (P) rats. Alcohol 46(1):17–27PubMedCrossRefGoogle Scholar
  19. DiFranza JR, Guerrera MP (1990) Alcoholism and smoking. J Stud Alcohol 51(2):130–135PubMedCrossRefGoogle Scholar
  20. Digard H, Errington G, Richter A, McAdams K (2009) Patterns and behaviors of snus consumption in Sweden. Nicotine Tob Res 11:1175–1181PubMedPubMedCentralCrossRefGoogle Scholar
  21. Digard H, Proctor C, Kulasekaran A, Malmqvist U, Richter A (2013) Determination of nicotine absorption from multiple tobacco products and nicotine gum. Nicotine Tob Res 15(1):255–261PubMedCrossRefPubMedCentralGoogle Scholar
  22. Donoghue K, Elzerbi C, Saunders R, Whittington C, Pilling S, Drummond C (2015) The efficacy of acamprosate and naltrexone in the treatment of alcohol dependence, Europe versus the rest of the world: a meta-analysis. Addiction 110(6):920–930PubMedCrossRefPubMedCentralGoogle Scholar
  23. Erwin BL, Slaton RM (2014) Varenicline in the treatment of alcohol use disorders. Ann Pharmacother 48(11):1445–1455PubMedCrossRefPubMedCentralGoogle Scholar
  24. Exley R, Maubourguet N, David V, Eddine R, Evrard A, Pons S, Marti F, Threlfell S, Cazala P, McIntosh JM, Changeux JP, Maskos U, Cragg SJ, Faure P (2011) Distinct contributions of nicotinic acetylcholine receptor subunit alpha4 and subunit alpha6 to the reinforcing effects of nicotine. Proc Natl Acad Sci U S A 108(18):7577–7582PubMedPubMedCentralCrossRefGoogle Scholar
  25. Froehlich JC, Fischer SM, Dilley JE, Nicholson ER, Smith TN, Filosa NJ, Rademacher LC (2016) Combining varenicline (Chantix) with naltrexone decreases alcohol drinking more effectively than does either drug alone in a rodent model of alcoholism. Alcohol Clin Exp Res 40(9):1961–1970PubMedPubMedCentralCrossRefGoogle Scholar
  26. Froehlich JC, Nicholson ER, Dilley JE, Filosa NJ, Rademacher LC, Smith TN (2017) Varenicline reduces alcohol intake during repeated cycles of alcohol reaccess following deprivation in alcohol-preferring (P) rats. Alcohol Clin Exp Res 41(8):1510–1517PubMedPubMedCentralCrossRefGoogle Scholar
  27. Funk D, Lo S, Coen K, Lê AD (2016) Effects of varenicline on operant self-administration of alcohol and/or nicotine in a rat model of co-abuse. Behav Brain Res 296:157–162PubMedCrossRefPubMedCentralGoogle Scholar
  28. George O, Lloyd A, Carroll FI, Damaj MI, Koob GF (2011) Varenicline blocks nicotine intake in rats with extended access to nicotine self-administration. Psychopharmacology 213(4):715–722PubMedCrossRefPubMedCentralGoogle Scholar
  29. Gonzales D, Rennard SI, Nides M, Oncken C, Azoulay S, Billing CB, Watsky EJ, Gong J, Williams KE, Reeves KR (2006) Varenicline, an alpha4beta2 nicotinic acetylcholine receptor partial agonist, vs sustained-release bupropion and placebo for smoking cessation: a randomized controlled trial. JAMA. 296(1):47–55Google Scholar
  30. Grady SR, Drenan RM, Breining SR, Yohannes D, Wageman CR, Fedorov NB, McKinney S, Whiteaker P, Bencherif M, Lester HA, Marks MJ (2010) Structural differences determine the relative selectivity of nicotinic compounds for native α4β2*-, α6β2*-, α3β4*- and α7-nicotinic acetylcholine receptors. Neuropharmacology 58(7):1054–1066PubMedPubMedCentralCrossRefGoogle Scholar
  31. Grant B, Hasin D, Chou S, Stinson F, Dawson D (2004) Nicotine dependence and psychiatric disorders in the United States: results from the national epidemiologic survey on alcohol and related conditions. Arch Gen Psychiatry 61(11):1107–1115PubMedCrossRefGoogle Scholar
  32. Grucza R, Bierut L (2006) Co-occurring risk factors for alcohol dependence and habitual smoking: update on findings from the Collaborative Study on the Genetics of Alcoholism. Alcohol Res Health 29(3):172–178PubMedGoogle Scholar
  33. Gueorguieva R, Wu R, Donovan D, Rounsaville BJ, Couper D, Krystal JH, O’Malley SS (2010) Naltrexone and combined behavioral intervention effects on trajectories of drinking in the COMBINE study. Drug Alcohol Depend 107(2–3):221–229PubMedCrossRefGoogle Scholar
  34. Gulliver S, Rohsenow DJ, Colby SM, Dey AN, Abrams DB, Niaura RS, Monti PM (1995) Interrelationship of smoking and alcohol dependence, use and urges to use. J Stud Alcohol 56(2):202–206PubMedCrossRefGoogle Scholar
  35. Gurley DA, Lanthorn TH (1998) Nicotinic agonists competitively antagonize serotonin at mouse 5-HT3 receptors expressed in Xenopus oocytes. Neurosci Lett 247(2–3):107–110Google Scholar
  36. Hauser SR, Getachew B, Oster SM, Dhaher R, Ding ZM, Bell RL, McBride WJ, Rodd ZA (2012a) Nicotine modulates alcohol-seeking and relapse by alcohol-preferring (P) rats in a time-dependent manner. Alcohol Clin Exp Res 36(1):43–54PubMedCrossRefGoogle Scholar
  37. Hauser SR, Katner SN, Deehan GA Jr, Ding ZM, Toalston JE, Scott BJ, Bell RL, McBride WJ, Rodd ZA (2012b) Development of an oral operant nicotine/ethanol co-use model in alcohol-preferring (P) rats. Alcohol Clin Exp Res 36:1963–1972PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hauser SR, Bracken AL, Deehan GA, Toalston JE, Ding ZM, Truitt WA, Bell RL, McBride WJ, Rodd ZA (2014) Selective breeding for high alcohol preference increases the sensitivity of the posterior VTA to the reinforcing effects of nicotine. Addict Biol 19(5):800–811PubMedCrossRefGoogle Scholar
  39. Hodge CW, Haraguchi M, Erickson H, Samson HH (1993) Ventral tegmental microinjections of quinpirole decrease ethanol and sucrose-reinforced responding. Alcohol Clin Exp Res 17(2):370–375PubMedCrossRefGoogle Scholar
  40. Holgate JY, Shariff M, Mu EH, Bartlett S (2017) A rat drinking in the dark model for studying ethanol and sucrose consumption. Front Behav Neurosci 11:29PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hurt RT, Ebbert JO, Croghan IT, Schroeder DR, Hurt RD, Hays JT (2018) Varenicline for tobacco-dependence treatment in alcohol-dependent smokers: a randomized controlled trial. Drug Alcohol Depend 184:12–17PubMedCrossRefGoogle Scholar
  42. John U, Hill A, Rumpf H, Hapke U, Meyer C (2003a) Alcohol high risk drinking, abuse and dependence among tobacco smoking medical care patients and the general population. Drug Alcohol Depend 69(2):189–195PubMedCrossRefGoogle Scholar
  43. John U, Rumpf H, Hanke M, Gerke P, Hapke U (2003b) Estimation of tobacco- or alcohol-attributable disease rates in national hospital care: an approach based on routine in-patient disease register data and systematic diagnosis of alcohol use disorders. Alcohol Alcohol 38(4):339–346PubMedCrossRefGoogle Scholar
  44. Jonas DE, Amick HR, Feltner C, Bobashev G, Thomas K, Wines R, Kim MM, Shanahan E, Gass CE, Rowe CJ, Garbutt JC (2014) Pharmacotherapy for adults with alcohol use disorders in outpatient settings: a systematic review and meta-analysis. Jama 311(18):1889–1900PubMedCrossRefGoogle Scholar
  45. Jorenby DE, Hays JT, Rigotti NA, Azoulay S, Watsky EJ, Williams KE, Billing CB, Gong J, Reeves KR (2006) Efficacy of varenicline, an alpha4beta2 nicotinic acetylcholine receptor partial agonist, vs placebo or sustained-release bupropion for smoking cessation: a randomized controlled trial. JAMA 296(1):56–63PubMedCrossRefGoogle Scholar
  46. Kasten CR, Frazee AM, Boehm SL 2nd (2016) Developing a model of limited-access nicotine consumption in C57Bl/6J mice. Pharmacol Biochem Behav 148L:28–37CrossRefGoogle Scholar
  47. King A, Cao D, O’Malley S, Kranzler H, Cai X, deWit H, Matthews A, Stachoviak R (2012) Effects of naltrexone on smoking cessation outcomes and weight gain in nicotine-dependent men and women. J Clin Psychopharmacol 32(5):630–636PubMedPubMedCentralCrossRefGoogle Scholar
  48. Lajtha A, Sershen H (2010) Nicotine: alcohol reward interactions. Neurochem Res 35:1248–1258PubMedCrossRefGoogle Scholar
  49. Lê AD, Funk D, Lo S, Coen K (2014) Operant self-administration of alcohol and nicotine in a preclinical model of co-abuse. Psychopharmacology 231(20):4019–4029PubMedPubMedCentralCrossRefGoogle Scholar
  50. Lummis SC, Thompson AJ, Bencherif M, Lester HA (2011) Varenicline is a potent agonist of the human 5-hydroxytryptamine3 receptor. J Phamacol Exp Ther 339:125–131CrossRefGoogle Scholar
  51. Maggio SE, Saunders MA, Baxter TA, Nixon K, Prendergast MA, Zheng G, Crooks P, Dwoskin LP, Slack RD, Newman AH, Bell RL, Bardo MT (2018a) Effects of the nicotinic agonist varenicline, nicotinic antagonist r-bPiDI, and DAT inhibitor (R)-modafinil on co-use of ethanol and nicotine in female P rats. Psychopharmacology 235(5):1439–1453PubMedCrossRefPubMedCentralGoogle Scholar
  52. Maggio SE, Saunders MA, Nixon K, Prendergast MA, Zheng G, Crooks P, Dwoskin LP, Bell RL, Bardo MT (2018b) An improved model of ethanol and nicotine co-use in female P rats: effects of naltrexone, varenicline, and the selective nicotinic α6β2* antagonist r-bPiDI. Drug Alcohol Depend 193:154–161PubMedCrossRefPubMedCentralGoogle Scholar
  53. Maisel NC, Blodgett JC, Wilbourne PL, Humphreys K, Finney JW (2013) Meta-analysis of naltrexone and acamprosate for treating alcohol use disorders: when are these medications most helpful? Addiction 108(2):275–293PubMedCrossRefPubMedCentralGoogle Scholar
  54. Malin DH, Lake JR, Carter VA, Cunningham JS, Wilson OB (1993) Naloxone precipitates nicotine abstinence syndrome in the rat. Psychopharmacology 112(2–3):339–342PubMedCrossRefPubMedCentralGoogle Scholar
  55. Malin DH, Lake JR, Payne MC, Short PE, Carter VA, Cunningham JS, Wilson OB (1996) Nicotine alleviation of nicotine abstinence syndrome is naloxone-reversible. Pharmacol Biochem Behav 53(1):81–85PubMedCrossRefPubMedCentralGoogle Scholar
  56. Martell N (2014) Tobacco returns to the bar, this time inside cocktails. National Public Radio. Retrieved from https://www.npr.org/
  57. McKinzie DL, Nowak KL, Yorger L, McBride WJ, Murphy JM, Lumeng L, Li T-K (1998) The alcohol deprivation effect in the alcohol-preferring P rat under free drinking and operant access conditions. Alcohol Clin Exp Res 22:1170–1176PubMedCrossRefGoogle Scholar
  58. Melendez RI, Rodd-Henricks ZA, Engleman EA, Li TK, McBride WJ, Murphy JM (2002) Microdialysis of dopamine in the nucleus accumbens of alcohol-preferring (P) rats during anticipation and operant self-administration of ethanol. Alcohol Clin Exp Res 26:318–325PubMedCrossRefGoogle Scholar
  59. Melendez RI, Rodd ZA, McBride WJ, Murphy JM (2004) Involvement of the mesopallidal dopamine system in ethanol reinforcement. Alcohol 32:137–144PubMedCrossRefGoogle Scholar
  60. Motschman CA, Gass JC, Wray JM, Germeroth LJ, Schlienz NJ, Munoz DA, Moore FE, Rhodes JD, Hawk LW, Tiffany ST (2016) Selection criteria limit generalizability of smoking pharmacotherapy studies differentially across clinical trials and laboratory studies: a systematic review on varenicline. Drug Alcohol Depend 169:180–189PubMedCrossRefPubMedCentralGoogle Scholar
  61. National Research Council (2011) Guide for the care and use of laboratory animals, 8th edn. The National Academies Press, Washington, DCGoogle Scholar
  62. New York Times Magazine (Marshall Selladec) (2003) The 3rd Annual Year in Ideas; Nicotini, The. Published Dec 14, 2003Google Scholar
  63. O’Connor EC, Parker D, Rollema H, Mead AN (2010) The α4β2 nicotinic acetylcholine-receptor partial agonist varenicline inhibits both nicotine self-administration following repeated dosing and reinstatement of nicotine seeking in rats. Psychopharmacology 208(3):365–376PubMedCrossRefPubMedCentralGoogle Scholar
  64. O’Malley SS, Jaffe AJ, Rode S, Rounsaville BJ (1996) Experience of a “slip” among alcoholics treated with naltrexone or placebo. Am J Psychiatry 153(2):281–283PubMedCrossRefPubMedCentralGoogle Scholar
  65. O’Malley SS, Cooney JL, Krishnan-Sarin S, Dubin JA, McKee SA, Cooney NL, Blakeslee A, Meandzija B, Romano-Dahlgard D, Wu R, Makuch R, Jatlow P (2006) A controlled trial of naltrexone augmentation of nicotine replacement therapy for smoking cessation. Arch Intern Med 166(6):667–674PubMedCrossRefPubMedCentralGoogle Scholar
  66. Ortiz NC, O’Neill HC, Marks MJ, Grady SR (2012) Varenicline blocks β2*-nAChR-mediated response and activates β4*-nAChR-mediated responses in mice in vivo. Nicotine Tob Res 14(6):711–719PubMedPubMedCentralCrossRefGoogle Scholar
  67. Petrakis I, Ralevski E, Desai N, Trevisan L, Gueorguieva R, Rounsaville B, Krystal J (2012) Noradrenergic vs serotonergic antidepressant with or without naltrexone for veterans with PTSD and comorbid alcohol dependence. Neuropsychopharmacology 37(4):996–1004PubMedCrossRefPubMedCentralGoogle Scholar
  68. Randall PA, Jaramillo AA, Frisbee S, Besheer J (2015) The role of varenicline on alcohol-primed self-administration and seeking behavior in rats. Psychopharmacology 232(14):2443–2454PubMedPubMedCentralCrossRefGoogle Scholar
  69. Rodd ZA, Bell RL, Kuc KA, Murphy JM, Lumeng L, Li TK, McBride WJ (2003) Effects of repeated alcohol deprivations on operant ethanol self-administration by alcohol-preferring (P) rats. Neuropsychopharmacology 28:1614–1621PubMedCrossRefPubMedCentralGoogle Scholar
  70. Rodd ZA, Bell RL, McQueen VK, Davids MR, Hsu CC, Murphy JM, Li TK, Lumeng L, McBride WJ (2005) Prolonged increase in the sensitivity of the posterior ventral tegmental area to the reinforcing effects of ethanol following repeated exposure to cycles of ethanol access and deprivation. J Pharmacol Exp Ther 315(2):648–657PubMedPubMedCentralCrossRefGoogle Scholar
  71. Rodd ZA, Bell RL, Kuc KA, Murphy JM, Lumeng L, McBride WJ (2009) Effects of concurrent access to multiple ethanol concentrations and repeated deprivations on alcohol intake of high-alcohol-drinking (HAD) rats. Addict Biol 14:152–164PubMedCrossRefGoogle Scholar
  72. Rodd ZA, Bell RL, Oster SM, Toalston JE, Pommer TJ, McBride WJ, Murphy JM (2010) Serotonin-3 receptors in the posterior ventral tegmental area regulate ethanol self-administration of alcohol-preferring (P) rats. Alcohol 44(3):245–255PubMedPubMedCentralCrossRefGoogle Scholar
  73. Rodd-Henricks ZA, McKinzie DL, Crile RS, Murphy JM, McBride WJ (2000) Regional heterogeneity for the intracranial self-administration of ethanol within the ventral tegmental area of female Wistar rats. Psychopharmacology 149:217–224PubMedCrossRefGoogle Scholar
  74. Rodd-Henricks ZA, Bell RL, Kuc KA, Murphy JM, McBride WJ, Lumeng L, Li TK (2001) Effects of concurrent access to multiple ethanol concentrations and repeated deprivations on alcohol intake of alcohol-preferring rats. Alcohol Clin Exp Res 25:1140–1150PubMedCrossRefGoogle Scholar
  75. Rodd-Henricks ZA, Bell RL, Kuc KA, Murphy JM, McBride WJ, Lumeng L, Li TK (2002a) Effects of ethanol exposure on subsequent acquisition and extinction of ethanol self-administration and expression of alcohol-seeking behavior in adult alcohol-preferring (P) rats: I. Periadolescent exposure. Alcohol Clin Exp Res 26:1632–1641PubMedCrossRefGoogle Scholar
  76. Rodd-Henricks ZA, Bell RL, Kuc KA, Murphy JM, McBride WJ, Lumeng L, Li TK (2002b) Effects of ethanol exposure on subsequent acquisition and extinction of ethanol self-administration and expression of alcohol-seeking behavior in adult alcohol-preferring (P) rats: II. Adult exposure. Alcohol Clin Exp Res 26:1642–1652PubMedCrossRefGoogle Scholar
  77. Rollema H, Chambers LK, Coe JW, Glowa J, Hurst RS, Lebel LA, Lu Y, Mansbach RS, Mather RJ, Rovetti CC, Sands SB, Schaeffer E, Schulz DW, Tingley FI, Williams KE (2007) Pharmacological profile of the α4β2 nicotinic acetylcholine receptor partial agonist varenicline, an effective smoking cessation aid. Neuropharmacology 52(3):985–994PubMedCrossRefGoogle Scholar
  78. Sable HJ, Bell RL, Rodd ZA, McBride WJ (2006) Effects of naltrexone on the acquisition of alcohol intake in male and female periadolescent and adult alcohol-preferring (P) rats. Int J Adolesc Med Health 18:139–149PubMedCrossRefGoogle Scholar
  79. Scuppa G, Cippitelli A, Toll L, Ciccocioppo R, Ubaldi M (2015) Varenicline decreases nicotine but not alcohol self-administration in genetically selected Marchigian Sardinian alcohol-preferring (msP) rats. Drug Alcohol Depend 156:126–132PubMedPubMedCentralCrossRefGoogle Scholar
  80. Smith PH, Weinberger AH, Zhang J, Emme E, Mazure CM, McKee SA (2017) Sex differences in smoking cessation pharmacotherapy comparative efficacy: a network meta-analysis. Nicotine Tob Res 19(3):273–281PubMedPubMedCentralGoogle Scholar
  81. Soderpalm B, Ericson M, Olausson P, Blomqvist O, Engel JA (2000) Nicotinic mechanisms involved in the dopamine activating and reinforcing properties of ethanol. Behav Brain Res 113:85–96PubMedCrossRefGoogle Scholar
  82. Soyka M, Müller CA (2017) Pharmacotherapy of alcoholism - an update on approved and off-label medications. Expert Opin Pharmacother 18(12):1187–1199PubMedCrossRefGoogle Scholar
  83. Spanagel R, Zieglgansberger W (1997) Anti-craving compounds for ethanol: new pharmacological tools to study addictive processes. Trends Pharmacol Sci 18:54–59PubMedCrossRefGoogle Scholar
  84. Spanagel R, Hölter SM, Allingham K, Landgraf R, Zieglgänsberger W (1996) Acamprosate and alcohol: I. Effects on alcohol intake following alcohol deprivation in the rat. Eur J Pharmacol 305(1–3):39–44PubMedCrossRefGoogle Scholar
  85. Steensland P, Simms JA, Holgate J, Richards JK, Bartlett SE (2007) Varenicline, an alpha4beta2 nicotinic acetylcholine receptor partial agonist, selectively decreases ethanol consumption and seeking. Proc Natl Acad Sci U S A 104(30):12518–12523PubMedPubMedCentralCrossRefGoogle Scholar
  86. Thompson A, Ashcroft DM, Owens L, van Staa TP, Pirmohamed M (2017) Drug therapy for alcohol dependence in primary care in the UK: a Clinical Practice Research Datalink study. PLoS One 12(3):1–14Google Scholar
  87. Tizabi Y, Copeland RJ, Louis VA, Taylor RE (2002) Effects of combined systemic alcohol and central nicotine administration into ventral tegmental area on dopamine release in the nucleus accumbens. Alcohol Clin Exp Res 26(3):394–399PubMedCrossRefGoogle Scholar
  88. Tizabi Y, Bai L, Copeland RJ, Taylor RE (2007) Combined effects of systemic alcohol and nicotine on dopamine release in the nucleus accumbens shell. Alcohol Alcohol 42(5):413–416PubMedCrossRefGoogle Scholar
  89. Toalston JE, Oster SM, Kuc KA, Pommer TJ, Murphy JM, Lumeng L, Bell RL, McBride WJ, Rodd ZA (2008) Effects of alcohol and saccharin deprivations on concurrent ethanol and saccharin operant self-administration by alcohol-preferring (P) rats. Alcohol 42:277–284PubMedPubMedCentralCrossRefGoogle Scholar
  90. Toll B, White M, Wu R, Meandzija B, Jatlow P, Makuch R, O’Malley S (2010) Low-dose naltrexone augmentation of nicotine replacement for smoking cessation with reduced weight gain: a randomized trial. Drug Alcohol Depend 2010(3):200–206CrossRefGoogle Scholar
  91. Truitt WA, Hauser SR, Deehan GJ, Toalston JE, Wilden JA, Bell RL, McBride WJ, Rodd ZA (2015) Ethanol and nicotine interaction within the posterior ventral tegmental area in male and female alcohol-preferring rats: evidence of synergy and differential gene activation in the nucleus accumbens shell. Psychopharmacology 232(3):639–649PubMedCrossRefPubMedCentralGoogle Scholar
  92. Volpicelli JR, Alterman AI, Hayashida M, O’Brien CP (1992) Naltrexone in the treatment of alcohol dependence. Arch Gen Psychiatry 49(11):876–880PubMedCrossRefPubMedCentralGoogle Scholar
  93. Volpicelli JR, Rhines KC, Rhines JS, Volpicelli LA, Alterman AI, O’Brien CP (1997) Naltrexone and alcohol dependence. Role of subject compliance. Arch Gen Psychiatry 54:737–742PubMedCrossRefPubMedCentralGoogle Scholar
  94. Wetter DW, Kenford SL, Smith SS, Fiore MC, Jorenby DE, Baker TB (1999) Gender differences in smoking cessation. J Consult Clin Psychol 67(4):555–562PubMedCrossRefPubMedCentralGoogle Scholar
  95. Wong G, Wolter T, Croghan G, Croghan I, Offord K, Hurt R (1999) A randomized trial of naltrexone for smoking cessation. Addiction 94(8):1227–1237PubMedCrossRefPubMedCentralGoogle Scholar
  96. Zhu S, Lee M, Zhuang Y, Gamst A, Wolfson T (2012) Interventions to increase smoking cessation at the population level: how much progress has been made in the last two decades? Tob Control 21(2):110–118PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Program in Medical Neuroscience, Paul and Carole Stark Neurosciences Research InstituteIndiana University School of MedicineIndianapolisUSA
  2. 2.Department of Psychiatry, Institute of Psychiatric ResearchIndiana University School of MedicineIndianapolisUSA

Personalised recommendations