Effects of mood inductions by meal ambiance and moderate alcohol consumption on endocannabinoids and N-acylethanolamines in humans: a randomized crossover trial

Ilse C Schrieks, Dina Ripken, Annette Stafleu, Renger F Witkamp, Henk F J Hendriks, Ilse C Schrieks, Dina Ripken, Annette Stafleu, Renger F Witkamp, Henk F J Hendriks

Abstract

Background: The endocannabinoid system is suggested to play a regulatory role in mood. However, the response of circulating endocannabinoids (ECs) to mood changes has never been tested in humans. In the present study, we examined the effects of mood changes induced by ambiance and moderate alcohol consumption on plasma ECs 2-arachidonoylglycerol (2-AG), anandamide (AEA), and some N-acylethanolamine (NAE) congeners in humans.

Methods: Healthy women (n = 28) participated in a randomized cross-over study. They consumed sparkling white wine (340 mL; 30 g alcohol) or alcohol-free sparkling white wine (340 mL; <2 g alcohol) as part of a standard evening meal in a room with either a pleasant or an unpleasant ambiance.

Results: Plasma concentrations of palmitoylethanolamide (PEA) and stearoylethanolamide (SEA) increased after 30 min in the unpleasant ambiance, while they decreased in the pleasant ambiance. Changes in ECs and their NAE congeners correlated with mood states, such as happiness and fatigue, but in the pleasant ambiance without alcohol only. ECs and their NAE congeners were correlated with serum free fatty acids and cortisol.

Conclusion: This is the first human study to demonstrate that plasma NAEs are responsive to an unpleasant meal ambiance. Furthermore, associations between mood states and ECs and their NAE congeners were observed.

Trial registration: Clinicaltrials.gov NCT01426022.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Flow chart (CONSORT).
Fig 1. Flow chart (CONSORT).
Adapted from Schrieks et al. (2014) [26] under a CC BY license, with permission from PLOS ONE, original copyright 2014.
Fig 2. Overview of the experimental procedures…
Fig 2. Overview of the experimental procedures during a study day.
Time points are indicated within parentheses. BAC, Blood alcohol concentration; POMS, Profile of Mood States questionnaire.
Fig 3. Changes in endocannabinoids and N…
Fig 3. Changes in endocannabinoids and N-acylethanolamines after mood inductions by ambiance and moderate alcohol consumption.
(A) 2-arachidonoylglycerol (2-AG), (B) anandamide (AEA) and related compounds (C) palmitoylethanolamide (PEA) and (D) stearoylethanolamide (SEA). Black bars represent pleasant ambiance with alcohol; white bars represent pleasant ambiance without alcohol; grey bars represent unpleasant ambiance with alcohol; striped bars represent unpleasant ambiance without alcohol. PEA and SEA concentrations are increased 30 min after a meal in the unpleasant ambiance, but decreased after a meal in the unpleasant ambiance (*P = 0.073; ** P = 0.036). n = 16.
Fig 4. Correlations between changes in mood…
Fig 4. Correlations between changes in mood and endocannabinoids and N-acylethanolamines in a pleasant ambiance without alcohol.
A) 2-arachidonoylglycerol (2-AG), B) anandamide (AEA), C) palmitoylethanolamide (PEA), D) docosahexaenoylethanolamide (DHEA), E) oleoylethanolamide (OEA), and F) stearoylethanolamide (SEA). The figure shows spearman rank correlations with ranked values on both axes of the panels. n = 16.
Fig 5. Postprandial changes in (A) serum…
Fig 5. Postprandial changes in (A) serum free fatty acid and (B) cortisol after mood inductions.
White bars represent pleasant ambiance with alcohol; grey bars represent unpleasant ambaince with alcohol; black bars represent pleasant ambiance without alcohol; striped bars represent unpleasant ambiance without alcohol. Cortisol concentration is more decreased 120 min after a meal with alcohol than without alcohol (*P = 0.001). n = 28.

References

    1. Finn DP, Viveros MP, Marco EM. The endocannabinoid system and emotional processing: Pathophysiology and therapeutic potential. J Psychopharmacol. 2012;26: 3–6. 10.1177/0269881111405364
    1. Ruehle S, Rey AA, Remmers F, Lutz B. The endocannabinoid system in anxiety, fear memory and habituation. J Psychopharmacol. 2012;26: 23–39. 10.1177/0269881111408958
    1. Matias I, Bisogno T, Di Marzo V. Endogenous cannabinoids in the brain and peripheral tissues: Regulation of their levels and control of food intake. Int J Obes (Lond). 2006;30: S7–S12.
    1. De Petrocellis L, Di Marzo V. An introduction to the endocannabinoid system: From the early to the latest concepts. Best Pract Res Clin Endocrinol Metab. 2009;23: 1–15. 10.1016/j.beem.2008.10.013
    1. Di Marzo V. Endocannabinoids: synthesis and degradation In: Reviews of Physiology Biochemistry and Pharmacology. Springer; 2008. pp. 1–24.
    1. Busquets-Garcia A, Puighermanal E, Pastor A, de la Torre R, Maldonado R, Ozaita A. Differential role of anandamide and 2-arachidonoylglycerol in memory and anxiety-like responses. Biol Psychiatry. 2011;70: 479–486. 10.1016/j.biopsych.2011.04.022
    1. Sciolino NR, Zhou W, Hohmann AG. Enhancement of endocannabinoid signaling with JZL184, an inhibitor of the 2-arachidonoylglycerol hydrolyzing enzyme monoacylglycerol lipase, produces anxiolytic effects under conditions of high environmental aversiveness in rats. Pharmacol Res. 2011;64: 226–234. 10.1016/j.phrs.2011.04.010
    1. Gobbi G, Bambico FR, Mangieri R, Bortolato M, Campolongo P, Solinas M, et al. Antidepressant-like activity and modulation of brain monoaminergic transmission by blockade of anandamide hydrolysis. Proc Natl Acad Sci U S A. 2005;102: 18620–18625.
    1. Rubino T, Realini N, Castiglioni C, Guidali C, Viganó D, Marras E, et al. Role in anxiety behavior of the endocannabinoid system in the prefrontal cortex. Cereb Cortex. 2008;18: 1292–1301.
    1. Moreira FA, Grieb M, Lutz B. Central side-effects of therapies based on CB1 cannabinoid receptor agonists and antagonists: Focus on anxiety and depression. Best Pract Res Clin Endocrinol Metab. 2009;23: 133–144. 10.1016/j.beem.2008.09.003
    1. Hill MN, Patel S. Translational evidence for the involvement of the endocannabinoid system in stress-related psychiatric illnesses. Biol Mood Anxiety Disord. 2013;3: 19-5380-3-19.
    1. Phan KL, Angstadt M, Golden J, Onyewuenyi I, Popovska A, de Wit H. Cannabinoid modulation of amygdala reactivity to social signals of threat in humans. J Neurosci. 2008;28: 2313–2319. 10.1523/JNEUROSCI.5603-07.2008
    1. Gruber SA, Rogowska J, Yurgelun-Todd DA. Altered affective response in marijuana smokers: An FMRI study. Drug Alcohol Depend. 2009;105: 139–153. 10.1016/j.drugalcdep.2009.06.019
    1. Crosby KM, Bains JS. The intricate link between glucocorticoids and endocannabinoids at stress-relevant synapses in the hypothalamus. Neuroscience. 2012;204: 31–37. 10.1016/j.neuroscience.2011.11.049
    1. Hill MN, Tasker JG. Endocannabinoid signaling, glucocorticoid-mediated negative feedback, and regulation of the hypothalamic-pituitary-adrenal axis. Neuroscience. 2012;204: 5–16. 10.1016/j.neuroscience.2011.12.030
    1. Hill MN, McEwen BS. Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorticoids. Prog Neuropsychopharmacol Biol Psychiatry. 2010;34: 791–797. 10.1016/j.pnpbp.2009.11.001
    1. Hill MN. Introduction to the special issue on stress, emotional behavior, and the endocannabinoid system: A decade of research. Neuroscience. 2012;204: 1–4. 10.1016/j.neuroscience.2012.01.038
    1. Hill MN, Miller GE, Carrier EJ, Gorzalka BB, Hillard CJ. Circulating endocannabinoids and N-acyl ethanolamines are differentially regulated in major depression and following exposure to social stress. Psychoneuroendocrinology. 2009;34: 1257–1262. 10.1016/j.psyneuen.2009.03.013
    1. Dlugos A, Childs E, Stuhr KL, Hillard CJ, de Wit H. Acute stress increases circulating anandamide and other N-acylethanolamines in healthy humans. Neuropsychopharmacology. 2012;37: 2416–2427. 10.1038/npp.2012.100
    1. Di Marzo V, Verrijken A, Hakkarainen A, Petrosino S, Mertens I, Lundbom N, et al. Role of insulin as a negative regulator of plasma endocannabinoid levels in obese and nonobese subjects. Eur J Endocrinol. 2009;161: 715–722. 10.1530/EJE-09-0643
    1. Joosten M, Balvers M, Verhoeckx K, Hendriks H, Witkamp R. Plasma anandamide and other N-acylethanolamines are correlated with their corresponding free fatty acid levels under both fasting and non-fasting conditions in women. Nutrition & Metabolism. 2010;7: 49.
    1. Wansink B. Environmental factors that increase the food intake and consumption volume of unknowing consumers. Annu Rev Nutr. 2004;24: 455–479.
    1. Persson LO, Sjöberg L, Svensson E. Mood effects of alcohol. Psychopharmacology (Berl). 1980;68: 295–299.
    1. King A, de Wit H. Rewarding, stimulant, and sedative alcohol responses and relationship to future binge drinking. Arch Gen Psychiat. 2011;68: 389–399. 10.1001/archgenpsychiatry.2011.26
    1. Hendler RA, Ramchandani VA, Gilman J, Hommer DW. Stimulant and sedative effects of alcohol. Curr Top Behav Neurosci. 2013;13: 489–509. 10.1007/7854_2011_135
    1. Schrieks IC, Stafleu A, Kallen VL, Grootjen M, Witkamp RF, Hendriks HF. The biphasic effects of moderate alcohol consumption with a meal on ambiance-induced mood and autonomic nervous system balance: A randomized crossover trial. PloS one. 2014;9: e86199 10.1371/journal.pone.0086199
    1. Nyenhuis DL, Yamamoto C, Luchetta T, Terrien A, Parmentier A. Adult and geriatric normative data and validation of the profile of mood states. J Clin Psychol. 1999;55: 79–86.
    1. Balvers MGJ, Verhoeckx KCM, Witkamp RF. Development and validation of a quantitative method for the determination of 12 endocannabinoids and related compounds in human plasma using liquid chromatography-tandem mass spectrometry. J Chromatogr B Biomed Sci Appl. 2009;877: 1583–1590.
    1. Pasman WJ, Blokdijk VM, Bertina FM, Hopman WPM, Hendriks HFJ. Effect of two breakfasts, different in carbohydrate composition, on hunger and satiety and mood in healthy men. Int J Obes Relat Metab Disord. 2003;27: 663–668.
    1. Gross JJ, Levenson RW. Emotion elicitation using films. Cogn Emot. 1995;9: 87–108.
    1. Rottenberg J, Ray RD, Gross JJ. Emotion elicitation using films In: Coan JA, Allen JJB, editors. The handbook of emotion elicitation and assessment. New York: Oxford University Press, Inc; 2007. pp. 9–28. 10.1016/j.encep.2006.08.003
    1. Lane AM, Soos I, Leibinger E, Karsai I, Hamar P. Validity of the Brunel Mood Scale for use with UK, Italian and Hungarian athletes In: Lane AM, editor. Mood and human performance: Conceptual, measurement and applied issues. New York: Nova Science Publishers, Inc; 2007. pp. 119–130.
    1. Lutz B. Endocannabinoid signals in the control of emotion. Curr Opin Pharmacol. 2009;9: 46–52. 10.1016/j.coph.2008.12.001
    1. Hauer D, Schelling G, Gola H, Campolongo P, Morath J, Roozendaal B, et al. Plasma concentrations of endocannabinoids and related primary fatty acid amides in patients with post-traumatic stress disorder. Plos one. 2013;8: e62741 10.1371/journal.pone.0062741
    1. Lo Verme J, Fu J, Astarita G, La Rana G, Russo R, Calignano A, et al. The nuclear receptor peroxisome proliferator-activated receptor-alpha mediates the anti-inflammatory actions of palmitoylethanolamide. Mol Pharmacol. 2005;67: 15–19.
    1. Keppel Hesselink JM, Kopsky DJ, Witkamp RF. Palmitoylethanolamide (PEA)—‘Promiscuous’ anti-inflammatory and analgesic molecule at the interface between nutrition and pharma. PharmaNutrition. 2013
    1. Ghafouri N, Ghafouri B, Larsson B, Stensson N, Fowler CJ, Gerdle B. Palmitoylethanolamide and stearoylethanolamide levels in the interstitium of the trapezius muscle of women with chronic widespread pain and chronic neck-shoulder pain correlate with pain intensity and sensitivity. Pain. 2013;154: 1649–1658. 10.1016/j.pain.2013.05.002
    1. Choukèr A, Kaufmann I, Kreth S, Hauer D, Feuerecker M, Thieme D, et al. Motion sickness, stress and the endocannabinoid system. PLoS One. 2010;5: e10752 10.1371/journal.pone.0010752
    1. Wells AS, Read NW, Uvnas-Moberg K, Alster P. Influences of fat and carbohydrate on postprandial sleepiness, mood, and hormones. Physiol Behav. 1997;61: 679–686.

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj