Sex-dependent effects of cannabis-induced analgesia

Drug and Alcohol Dependence

Volumn 167, Issue , 2016, Pages 112-120

  Cooper, Ziva D ^a   Haney, Margaret ^a  

^a NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

Abuse liability; Analgesia; Cannabinoids; Sex differences; Subjective effects

Indexed keywords

CANNABINOID; CANNABIS; DRONABINOL; ILLICIT DRUG;

ADULT; ANALGESIA; ANTINOCICEPTION; ARTICLE; BODY MASS; BODY WEIGHT; CANNABIS ADDICTION; CANNABIS INDUCED ANALGESIA; CANNABIS SMOKING; CARDIOVASCULAR EFFECT; COLD PRESSOR TEST; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; FEMALE; HUMAN; HUMAN EXPERIMENT; HYPERALGESIA; MALE; MCGILL PAIN QUESTIONNAIRE; NOCICEPTION; NORMAL HUMAN; PAIN INTENSITY; PAIN THRESHOLD; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; RETROSPECTIVE STUDY; RISK FACTOR; SEX DIFFERENCE; UNITED STATES; WATER IMMERSION; DRUG EFFECTS; PAIN; PROCEDURES; PSYCHOLOGY; YOUNG ADULT;

ADULT; ANALGESIA; CANNABIS; DOUBLE-BLIND METHOD; FEMALE; HUMANS; MALE; MARIJUANA SMOKING; PAIN; PAIN THRESHOLD; RETROSPECTIVE STUDIES; SEX FACTORS; YOUNG ADULT;

EID: 84994228757     PISSN: 03768716     EISSN: 18790046     Source Type: Journal    
DOI: 10.1016/j.drugalcdep.2016.08.001     Document Type: Article

References (70)

1. Abrams, D.I., Jay, C.A., Shade, S.B., Vizoso, H., Reda, H., Press, S., Kelly, M.E., Rowbotham, M.C., Petersen, K.L., Cannabis in painful HIV-associated sensory neuropathy: a randomized placebo-controlled trial. Neurology 68 (2007), 515–521.
2. Black, M.L., Hill, J.L., Zacny, J.P., Behavioral and physiological effects of remifentanil and alfentanil in healthy volunteers. Anesthesiology 90 (1999), 718–726.
3. Bonn-Miller, M.O., Boden, M.T., Bucossi, M.M., Babson, K.A., Self-reported cannabis use characteristics, patterns and helpfulness among medical cannabis users. Am. J. Drug Alcohol Abuse 40 (2014), 23–30.
4. Buggy, D.J., Toogood, L., Maric, S., Sharpe, P., Lambert, D.G., Rowbotham, D.J., Lack of analgesic efficacy of oral delta-9-tetrahydrocannabinol in postoperative pain. Pain 106 (2003), 169–172.
5. Campesi, I., Fois, M., Franconi, F., Sex and gender aspects in anesthetics and pain medication. Handb. Exp. Pharmacol. 214 (2012), 265–278.
6. Castelli, M.P., Fadda, P., Casu, A., Spano, M.S., Casti, A., Fratta, W., Fattore, L., Male and female rats differ in brain cannabinoid CB1 receptor density and function and in behavioural traits predisposing to drug addiction: effect of ovarian hormones. Curr. Pharm. Des. 20 (2014), 2100–2113.
7. Colpaert, F.C., Tarayre, J.P., Alliaga, M., Bruins Slot, L.A., Attal, N., Koek, W., Opiate self-administration as a measure of chronic nociceptive pain in arthritic rats. Pain 1 (2001), 33–45.
8. Comer, S.D., Sullivan, M.A., Vosburg, S.K., Kowalczyk, W.J., Houser, J., Abuse liability of oxycodone as a function of pain and drug use history. Drug Alcohol Depend. 109 (2010), 130–138.
9. Conley, K.M., Toledano, A.Y., Apfelbaum, J.L., Zacny, J.P., Modulating effects of a cold water stimulus on opioid effects in volunteers. Psychopharmacology (Berl.) 131 (1997), 313–320.
10. Cooper, Z.D., Haney, M., Investigation of sex-dependent effects of marijuana in daily marijuana smokers. Drug Alcohol Depend. 136 (2014), 85–91.
11. Cooper, Z.D., Comer, S.D., Haney, M., Analgesic effects of smoked and oral THC in healthy marijuana smokers. Neuropsychopharmacology, 2013, 10.1038/npp.2013.97 Eub ahead of print.
12. Craft, R.M., Leitl, M.D., Gonadal hormone modulation of the behavioral effects of delta9-tetrahydrocannabinol in male and female rats. Eur. J. Pharmacol. 578 (2008), 37–42.
13. Craft, R.M., Wakley, A.A., Tsutsui, K.T., Laggart, J.D., Sex differences in cannabinoid 1 vs. cannabinoid 2 receptor-selective antagonism of antinociception produced by delta 9-tetrahydrocannabinol and CP55,940 in the rat. J. Pharmacol. Exp. Ther. 340 (2012), 787–800.
14. Craft, R.M., Marusich, J.A., Wiley, J.L., Sex differences in cannabinoid pharmacology: a reflection of differences in the endocannabinoid system?. Life Sci. 92 (2013), 476–481.
15. Craft, R.M., Sex differences in opioid analgesia: from mouse to man. Clin. J. Pain 19 (2003), 175–186.
16. Ehlers, C.L., Gizer, I.R., Vieten, C., Gilder, D.A., Stouffer, G.M., Lau, P., Wilhelmsen, K.C., Cannabis dependence in the San Francisco D = family study: age of onset of use, DSM-IV symptoms, withdrawal, and heritability. Addict. Behav. 35 (2010), 102–110.
17. Ellis, R.J., Toperoff, W., Vaida, F., van den Brande, G., Gonzales, J., Gouaux, B., Bentley, H., Atkinson, J.H., Smoked medicinal cannabis for neuropathic pain in HIV: a randomized, crossover clinical trial. Neuropsychopharmacology 34 (2009), 672–680.
18. Evans, S.M., Foltin, R.W., Exogenous progesterone attenuates the subjective effects of smoked cocaine in women, but not in men. Neuropsychopharmacology 31 (2006), 659–674.
19. Evans, S.M., Haney, M., Foltin, R.W., The effects of smoked cocaine during the follicular and luteal phases of the menstrual cycle in women. Psychopharmacology (Berl.) 159 (2002), 397–406.
20. Fattore, L., Spano, M.S., Altea, S., Angius, F., Fadda, P., Fratta, W., Cannabinoid self-administration in rats: sex differences and the influence of ovarian function. Br. J. Pharmacol. 152 (2007), 795–804.
21. Fattore, L., Spano, M.S., Altea, S., Fadda, P., Fratta, W., Drug- and cue-induced reinstatement of cannabinoids-seeking behavior in male and female rats: influence of ovarian hormones. Br. J. Pharmacol. 160 (2010), 724–735.
22. Finseth, T.A., Hedeman, J.L., Brown, R.P. 2nd, Johnson, K.I., Binder, M.S., Kluger, B.M., Self-reported efficacy of cannabis and other complementary medicine modalities by Parkinson's disease patients in Colorado. Evid. Based Complement. Altern. Nat. Med., 2015 Article ID 874849.
23. Foltin, R.W., Brady, J.V., Fischman, M.W., Emurian, C.S., Dominitz, J., Effects of smoked marijuana on social interaction in small groups. Drug Alcohol Depend. 20 (1987), 87–93.
24. Gil, K.M., Ginsberg, B., Muir, M., Sykes, D., Williams, D.A., Patient-controlled analgesia in postoperative pain: the relation of psychological factors to pain and analgesic use. Clin. J. Pain 6 (1990), 137–142.
25. Greenwald, M.K., Stitzer, M.L., Antinociceptive, subjective and behavioral effects of smoked marijuana in humans. Drug Alcohol Depend. 59 (2000), 261–275.
26. Haney, M., Comer, S.D., Ward, A.S., Foltin, R.W., Fischman, M.W., Factors influencing marijuana self-administration by humans. Behav. Pharmacol. 8 (1997), 101–112.
27. Haney, M., Ward, A.S., Comer, S.D., Foltin, R.W., Fischman, M.W., Abstinence symptoms following smoked marijuana in humans. Psychopharmacology (Berl.) 141 (1999), 395–404.
28. Haney, M., Rabkin, J., Gunderson, E., Foltin, R.W., Dronabinol and marijuana in HIV(+) marijuana smokers: acute effects on caloric intake and mood. Psychopharmacology (Berl.) 181 (2005), 170–178.
29. Hart, C.L., Haney, M., Ward, A.S., Fischman, M.W., Foltin, R.W., Effects of oral THC maintenance on smoked marijuana self-administration. Drug Alcohol Depend. 67 (2002), 301–309.
30. Hernandez-Avila, C.A., Rounsaville, B.J., Kranzler, H.R., Opioid-, cannabis- and alcohol-dependent women show more rapid progression to substance abuse treatment. Drug Alcohol Depend. 74 (2004), 265–272.
31. Hill, S.Y., Schwin, R., Goodwin, D.W., Powell, B.J., Marijuana and pain. J. Pharmacol. Exp. Ther. 188 (1974), 415–418.
32. Ilgen, M.A., Bohnert, K., Kleinberg, F., Jannausch, M., Bohnert, A.S., Walton, M., Blow, F.C., Characteristics of adults seeking medical marijuana certification. Drug Alcohol Depend. 132 (2013), 654–659.
33. Issa, M.A., Narang, S., Jamison, R.N., Michna, E., Edwards, R.R., Penetar, D.M., Wasan, A.D., The subjective psychoactive effects of oral dronabinol studied in a randomized, controlled crossover clinical trial for pain. Clin. J. Pain 30 (2014), 472–478.
34. Karst, M., Salim, K., Burstein, S., Conrad, I., Hoy, L., Schneider, U., Analgesic effect of the synthetic cannabinoid CT-3 on chronic neuropathic pain. JAMA 290 (2003), 1757–1762.
35. Khan, S.S., Secades-Villa, R., Okuda, M., Wang, S., Pérez-Fuentes, G., Kerridge, B.T., Blanco, C., Gender differences in cannabis use disorders: results from the national epidemiological survey of alcohol and related conditions. Drug Alcohol Depend. 130 (2013), 101–108.
36. Kraft, B., Frickey, N.A., Kaufmann, R.M., Reif, M., Frey, R., Gustorff, B., Kress, H.G., Lack of analgesia by oral standardized cannabis extract on acute inflammatory pain and hyperalgesia in volunteers. Anesthesiology 109 (2008), 101–110.
37. Lee, M.C., Ploner, M., Wiech, K., Bingel, U., Wanigasekera, V., et al. Amygdala activity contributes to the dissociative effect of cannabis on pain perception. Pain 154 (2013), 124–134.
38. Lenz, H., Raeder, J., Draegni, T., Heyerdahl, F., Schmelz, M., et al. Effects of COX inhibition on experimental pain and hyperalgesia during and after remifentanil infusions in humans. Pain 152 (2011), 1289–1297.
39. Lynch, W.J., Kalayasiri, R., Sughondhabirom, A., Pittman, B., Coric, V., Morgan, P.T., Malison, R.T., Subjective responses and cardiovascular effects of self-administered cocaine in cocaine-abusing men and women. Addict. Biol. 13 (2008), 403–410.
40. Marusich, J.A., Craft, R.M., Lefever, T.W., Wiley, J.L., The impact of gonadal hormones on cannabinoid dependence. Exp. Clin. Psychopharmacol. 23 (2015), 206–216.
41. McConnell, B.V., Applegate, M., Keniston, A., Kluger, B., Maa, E.H., Use of complementary and alternative medicine in an urban county hospital epilepsy clinic. Epilepsy Behav. 34 (2014), 73–76.
42. Mello, N.K., Knudson, I.M., Mendelson, J.H., Sex and menstrual cycle effects on progressive ratio measures of cocaine self-administration in cynomolgus monkeys. Neuropsychopharmacology 32 (2007), 1956–1966.
43. Melzack, R., The short-form McGill pain questionnaire. Pain 30 (1987), 191–197.
44. Miller, L.K., Devi, L.A., The highs and lows of cannabinoid receptor expression in disease: mechanisms and their therapeutic implications. Pharmacol. Rev. 63 (2011), 461–470.
45. Naef, M., Curatolo, M., Petersen-Felix, S., Arendt-Nielsen, L., Zbinden, A., Brenneisen, R., The analgesic effect of oral delta-9-tetrahydrocannabinol (THC), morphine, and a THC-morphine combination in healthy subjects under experimental pain conditions. Pain 105 (2003), 79–88.
46. Niikura, K., Narita, M., Butelman, E.R., Kreek, M.J., Suzuki, T., Neuropathic and chronic pain stimuli downregulate central mu-opioid and dopaminergic transmission. Trends Pharmacol. Sci. 31 (2010), 299–305.
47. Noyes, R.J., Brunk, S.F., Baram, D.A., Canter, A., Analgesic effect of delta-9-tetrahydrocannabinol. J Clin. Pharmacol. 15 (1975), 139–143.
48. Nurmikko, T.J., Serpell, M.G., Hoggart, B., Toomey, P.J., Morlion, B.J., Haines, D., Sativex successfully treats neuropathic pain characterised by allodynia: a randomised, double-blind, placebo-controlled clinical trial. Pain 133 (2007), 210–220.
49. Raehal, K.M., Bohn, L.M., β-Arrestins: regulatory role and therapeutic potential in opioid and cannabinoid receptor-mediated analgesia. Handb. Exp. Pharmacol., 219, 2014 427–413.
50. Redmond, W.J., Goffaux, P., Potvin, S., Marchand, S., Analgesic and antihyperalgesic effects of nabilone on experimental heat pain. Curr. Med. Res. Opin. 24 (2008), 1017–1024.
51. Rog, D.J., Nurmikko, T.J., Young, C.A., Oromucosal delta9-tetrahydrocannabinol/cannabidiol for neuropathic pain associated with multiple sclerosis: an uncontrolled, open-label, 2-year extension trial. Clin. Ther. 29 (2007), 2068–2079.
52. Ryan-Ibarra, S., Induni, M., Ewing, D., Prevalence of medical marijuana use in California, 2012. Drug Alcohol Rev. 34 (2015), 141–146.
53. Sandén, C., Broselid, S., Cornmark, L., Andersson, K., Daszkiewicz-Nilsson, J., Martensson, U.E., Olde, B., Leeb-Lundberg, L.M., G protein-coupled estrogen receptor 1/G protein-coupled receptor 30 localizes in the plasma membrane and traffics intracellularly on cytokeratin intermediate filaments. Mol. Pharmacol. 79 (2011), 400–410.
54. 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. 7 (1999), 274–283.
55. Sofuoglu, M., Babb, D.A., Hatsukami, D.K., Effects of progesterone treatment on smoked cocaine response in women. Pharmacol. Biochem. Behav. 72 (2002), 431–435.
56. Stinson, F.S., Ruan, W.J., Pickering, R., Grant, B.F., Cannabis use disorders in the USA: prevalence, correlates and co-morbidity. Psychol. Med. 36 (2006), 1447–1460.
57. Substance Abuse and Mental Health Services Administration, Center for Behavioral Health Statistics and Quality, Treatment Episode Data Set (TEDS): 2000–2010. State Admissions to Substance Abuse Treatment Services, DASIS Series: S-63, HHS Publication No. SMA-12-4729. 2012, Substance Abuse and Mental Health Services Administration, Rockville, MD.
58. Svendsen, K.B., Jensen, T.S., Bach, F.W., Does the cannabinoid dronabinol reduce central pain in multiple sclerosis? Randomised double blind placebo controlled crossover trial. BMJ, 329, 2004, 253.
59. Tseng, A.H., Craft, R.M., Sex differences in antinociceptive and motoric effects of cannabinoids. Eur. J. Pharmacol. 430 (2001), 41–447.
60. United Nations Office on Drugs and Crime, World Drug Report., 2013, Division for Policy Analysis and Public Affairs United Nations Office, Vienna, Austria.
61. Wakley, A.A., Craft, R.M., Antinociception and sedation following intracerebroventricular administration of (Δ⁹-tetrahydrocannabinol in female vs male rats. Behav. Brain Res. 216 (2011), 200–206.
62. Wakley, A.A., Wiley, J.L., Craft, R.M., Sex differences in antinociceptive tolerance to delta-9-tetrahydrocannabinol in the rat. Drug Alcohol Depend. 143 (2014), 22–28.
63. Wakley, A.A., Wiley, J.L., Craft, R.M., Gonadal hormones do not alter the development of antinociceptive tolerance to delta-9-tetrahydrocannabinol in adult rats. Pharmacol. Biochem. Behav. 133 (2015), 111–121.
64. Wallace, M., Schulteis, G., Atkinoson, J.H., Wolfson, T., Lazzaretto, D., Bentley, H., Gouaux, B., Abramson, I., Dose-dependent effects of smoked cannabis on capsaicin-induced pain and hyperalgesia in healthy volunteers. Anesthesiology 107 (2007), 785–796.
65. Ware, M.A., Wang, T., Shapiro, S., Robinson, A., Ducruet, T., Huynh, T., Gamsa, A., Bennett, G.J., Collet, J.P., Smoked cannabis for chronic neuropathic pain: a randomized controlled trial. CMAJ 182 (2010), E694–701.
66. Wilsey, B., Marcotte, T., Tsodikov, A., Millman, J., Bentley, H., Gouaux, B., et al. A randomized, placebo-controlled, crossover trial of cannabis cigarettes in neuropathic pain. J. Pain 9 (2008), 506–521.
67. Wilsey, B., Marcotte, T., Deutsch, R., Gouaux, B., Sakai, S., Donaghe, H., Low-dose vaporized cannabis significantly improves neuropathic pain. J. Pain 14 (2013), 136–148.
68. Zacny, J.P., Beckman, N.J., The effects of a cold-water stimulus on butorphanol effects in males and females. Pharmacol. Biochem. Behav. 78 (2004), 653–659.
69. Zacny, J.P., McKay, M.A., Toledano, A.Y., Marks, S., Young, C.J., Klock, P.A., Apfelbaum, J.L., The effects of cold-water immersion stressor on the reinforcing and subjective effects of fentanyl in healthy colunteers. Drug Alcohol Depend. 42 (1996), 133–142.
70. Zacny, J.P., Coalson, D.W., Young, C.J., Klafta, J.M., Lichtor, J.L., Rupani, G., Thapar, P., Apfelbaum, J.L., Propofol at conscious sedation doses produces mild analgesia to cold pressor-induced pain in healthy volunteers. J. Clin. Anesth. 8 (1996), 469–474.