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Official websites use. Share sensitive information only on official, secure websites. Corresponding author: Hollis C. Karoly hollis. In recent years, human and animal studies have converged to support altered inflammatory signaling as one molecular mechanism underlying the pathophysiology of alcohol use disorders AUDs. Alcohol binds to receptors on immune cells, triggering signaling pathways that produce pro-inflammatory cytokines. Chronic inflammation is associated with tissue damage, which may contribute to negative effects of AUD. Conversely, cannabis is associated with decreased inflammatory signaling, and animal studies suggest that cannabinoids may impact alcohol-induced inflammation. Thus, the impact of cannabis on inflammation in AUDs in humans warrants examination. We examined whether alcohol consumption, cannabis use and gender were associated with changes in circulating cytokines, and whether there was a significant interaction between alcohol and cannabis use predicting blood levels of circulating cytokines. A positive association between alcohol and IL-6 emerged. Follow-up moderation analyses indicated a cannabis by alcohol interaction predicting circulating IL-6, such that cannabis non-users showed a stronger relationship between alcohol and IL-6 compared to cannabis users. These preliminary findings suggest that cannabinoid compounds may serve to mitigate inflammation associated with alcohol use. In addition, the present results provide data to inform future investigations, with the goal of ultimately leveraging knowledge of the role of inflammation in AUDs to develop more effective treatments focused on novel immune targets. Recent evidence from human and animal research has converged to support the role of alcohol in promoting deleterious adaptations in inflammatory signaling cascades. It is likely that perturbation of the immune system is a critical mechanism in the etiology of AUD Alfonso-Loeches and Guerri, ; Coller and Hutchinson, ; Leclercq et al. Briefly, inflammation is a component of the innate immune system, which relies on germline-encoded, pattern-recognition receptors, such as Toll-like receptors TLRs , to identify invading pathogens and activate various immune cells. Of particular importance to the discussion of alcohol and immune signaling is TLR4, a cell-surface receptor found in numerous peripheral immune cells as well as microglial cells in the brain. Activation of the TLR4-mediated pathway by alcohol is associated with the aberrant production of inflammatory mediators, such as pro-inflammatory cytokines, Fernandez-Lizarbe et al. Alcohol-related damage to the brain and other organs e. Chronic alcohol use in humans impairs the function of the intestinal barrier Parlesak et al. In general, higher circulating LPS in the blood indicates greater gut permeability, and is associated with inflammation e. Another study collected whole blood following an acute binge-alcohol administration in humans, and found an increase in circulating endotoxin in the blood, as well as increased inflammatory cytokines e. In addition, blood levels of pro-inflammatory cytokines e. The mechanism through which this peripheral-to-central nervous system cytokine signaling occurs is not completely understood, but may involve the ability of certain cytokines to penetrate the blood brain barrier BBB via circumventricular organs or active transport across the blood-brain barrier Quan and Banks, Thus, although neuroinflammation cannot be measured in vivo in human subjects, assays of peripheral inflammation may still provide useful information regarding the impact of alcohol on inflammatory signaling. Specifically, endocannabinoids have been shown to ameliorate inflammation associated with traumatic brain injury TBI in rodent models Mayeux et al. Cannabinoid agonists have also demonstrated anti-inflammatory effects that confer protective benefits in individuals with co-occurring HIV and alcohol abuse Perdisky et al. Thus, given the opposing effects of alcohol and cannabinoids on inflammatory signaling, and the role of cannabinoid receptors in alcohol-induced inflammatory signaling, cannabinoid receptors may serve as an important treatment target for alcohol use disorders Nair et al. We hypothesized that alcohol use would be positively associated with blood levels of these three cytokines. We further expected that the positive relationship between alcohol consumption and cytokine levels would be stronger among individuals with lower levels of cannabis use compared to individuals who reported regular cannabis consumption. The study was approved by the local ethics committee and written informed consent was obtained from all participants. A total of 66 male and female participants between the ages of 25—40 were recruited from the greater Boulder-Denver area using flyers and online advertisements e. The age range was selected to minimize the impact of development and aging on inflammatory markers Jaspan et al. Interested individuals were asked screening questions via phone. In order to assess the continuum of alcohol use behaviors, we recruited individuals broadly who endorsed any level of drinking over the past 3 months. However, given that prior work in this area has primarily been done in subjects with AUD e. To ensure that participants were not currently under the influence of any substances while completing the study, they were asked ahead of time to refrain from drinking alcohol within 48 hours, smoking cannabis within 6 hours or smoking cigarettes within 2 hours of the session. At the start of this session, all participants were breathalyzed. Only participants with a breath alcohol level BrAC of zero were allowed to participate in the study. A demographics questionnaire was used to collect information on age, sex, marital status, SES, occupation, income, education, and race. All participants also completed the Timeline Follow-back TLFB Sobell and Sobell, , which is an assessment method that obtains estimates of daily alcohol, cigarette, and other drug use. This instrument requires subjects to recall from memory the number of drinks consumed for each day over the prior 90 days as well as their use of tobacco products and recreational drugs, including cannabis. The total score on the ADS ranges from 0 to 47, with scores of 9 or more suggesting that alcohol dependence is likely. Blood samples were collected by a certified phlebotomist. Plasma samples were undiluted, ran in duplicate, and measured using a microplate reader Elx Biotek Inc, Winooski, VT set to the wavelength suggested by the manufacturer. Regarding cannabis consumption, the TLFB only assesses for frequency e. Given the difficulty of quantifying the amount of cannabis used by an individual per day due to different THC strain potencies, varying methods of consumption, and because individual users do not always know the exact amount consumed in a particular sitting Gray et al. Regarding the TLFB alcohol consumption variable, given that binge drinking has been associated with increased inflammation in both animals and humans Bala et al. This is not a good measure of drinking in this sample, as the maximum number of drinks consumed on a heavy drinking day in these subjects is, on average, 8. A standard curve was created using Microsoft Excel Version In all models reported below, residuals were approximately normally distributed 1 and homoscedasticity was established, as assessed by a visual inspection of a plot standardized residuals versus standardized predicted values for each model. In all models, slope values are reported as standardized coefficients. Critical alpha was set at. Given the exploratory nature of this work, we did not correct for multiple tests. We also limited the number of covariates included in each model to increase our power to detect effects. Gender was included as a covariate in all models, given that the relationship between alcohol consumption and circulating cytokines may differ for males and females e. Because individuals were excluded from the study if they smoked cigarettes more than 3 days per week, and because they were instructed not to smoke cigarettes within 2 hours of the study session, smoking data was not included as a covariate in primary regression analyses. However, given the link between smoking and increased inflammatory signaling Van der Vaart et al. In addition, given that individuals were screened out for recent illicit drug use, we did not include a drug-use covariate in primary regression models. However, because, as we have now clarified, there were 6 individuals who did report use of an illicit substance 1—2 times in the past days, we conducted follow-up analyses using a binary covariate for the presence of an illicit drug-use episode in the past 90 days, to ensure that illicit drug use was not significantly impacting these results. Note that both drinks per drinking day and days of cannabis use were mean centered for all moderation models. Because moderation analyses were planned a priori Shadish et al. Table 1 presents the means and standard deviations for various demographic and substance use variables. Although subjects were screened out for illicit drug use on the phone screen, 6 subjects reported illicit drug use once or twice during the past 90 days on the TLFB. Given that none of these individuals reported use in the past 90 days i. Specifically, for IL-6, 2 outliers were dropped; for IL-8, 1 outlier was removed and 1 individual was dropped for having a concentration that was too low to detect; for IL-1B, 7 individuals were removed due to having concentrations that were too low to detect. In the model in which IL-6 was the criterion, the predictors accounted for In the model in which IL-8 was the criterion, the predictors explained 5. In the model in which IL-6 was the criterion, predictors explained Figure 3 illustrates these group differences. All significant results remained even when TLFB total number of cigarettes and TLFB cigarettes per smoking day were each separately included as covariates. Inspection of individual regression slopes indicates no significant cannabis by drinks per drinking day interaction. Results of main effects and interaction models are presented in Table 2. Multivariate association of gender, cannabis use and alcohol consumption with circulating cytokines: main effects and interactions. Interaction models were not run for IL-8 given that significant main effects were not found. Most notably, we observed an alcohol by cannabis interaction predicting circulating IL-6, such that individuals who did not report cannabis use demonstrated a significant positive association between alcohol consumption and IL-6, whereas those who did use cannabis showed no association. We did not observe any significant relationships between alcohol or cannabis use and IL Our finding that drinks per drinking day was positively associated with circulating IL-6 is consistent with prior work demonstrating that circulating interleukins are correlated with AUD severity Leclercq et al. This suggests that, at least in the present sample of less clinically severe i. Counter to our hypotheses, circulating IL-8 was not associated with alcohol consumption or cannabis use in the present study. Increased plasma IL-8 has been previously shown in alcohol dependent patients Hill et al. Similarly, another study demonstrated increased IL-8 among alcohol dependent inpatients compared to healthy controls Leclercq et al. The subjects in the present study did not have significant chronicity of alcohol use, and none reported alcohol-related liver problems or prior inpatient hospitalization, which may explain our lack of findings for IL Further, although there is some evidence for an indirect link between cannabinoid signaling and IL-8 Mormina et al. These results suggest that compared to other cytokines, IL-8 may not play a primary role in inflammatory signaling in substance use disorders. In the moderation model, a significant interaction between cannabis use and drinks per drinking day emerged. The direction of this interaction is such that lower cannabis use was associated with a stronger relationship between alcohol consumption and circulating IL Specifically, among individuals who did not consume cannabis during the days immediately prior to the study, there was a strong positive relationship between alcohol consumption and IL-6, but in those who did consume cannabis, there was no relationship. This finding suggests that the pro-inflammatory effects of alcohol use were attenuated in those who use both alcohol and cannabis. These results are consistent with findings from human studies demonstrating that cannabis use is associated with reductions in IL-6 Keen et al. This cannabis by alcohol interaction suggests that more in-depth exploration of the mechanism s by which cannabinoids may exert anti-inflammatory properties, particularly in the context of heavy alcohol use, are warranted. To date, the influence of cannabis and alcohol together on inflammatory signaling in humans is unknown. Although it has been previously suggested that cannabis may exacerbate the risks of using alcohol, this study suggests that cannabinoids may also have the potential to reduce alcohol-related harm. The identification of cannabinoids or combinations of cannabinoids that have anti-inflammatory properties without psychoactive effects e. In light of the present findings, and given the role of cannabinoid receptors in alcohol-induced inflammation Agudelo et al. A primary limitation of the present study is that we did not directly measure neuroinflammation, and it is unclear to what extent peripheral measures of inflammation such as peripheral cytokines are associated with neuroinflammation. However, to date, it is unclear whether peripheral cytokines are significantly associated with neuroinflammation in human subjects with AUDs. Further, although alcohol is likely to contribute to peripheral inflammation, given that alcohol dependence is associated with elevated plasma cytokine levels in humans e. Future animal research directly measuring neuroinflammatory markers is necessary to better understand this relationship. However, although it is not currently possible to collect direct measures of neuroinflammation from human subjects, there may be additional peripheral markers that could help to explicate the relationship between alcohol use and inflammation. In particular, recent work has suggested that peripheral inflammation may play a role in the development and maintenance of AUDs through alcohol-induced gut-permeability and intenstinal dysbiosis, which refers to the development pathogenic bacteria in the gut. Intestinal dysbiosis has been shown to not only exacerbate depression, anxiety and craving, but possibly contribute to the symptoms of alcohol addiction through interacting with the stress system, disrupting normal sleep processes and interfering with social interaction de Timary et al. Not surprisingly, given that the gut is a major source of immune factors, considerable human research has already demonstrated the critical role of gut microbiota in influencing psychiatric disorders and promoting aberrant behavior Dinan et al. Further, alcohol dependent subjects with dysbiosis have demonstrated greater severity of AUD symptoms compared to those without dysbiosis Leclercq et al. Thus, an important next step is to further examine the possible role of gut permeability and intestinal dysbiosis in alcohol-induced inflammation through incorporating gut microbiome sample collection into studies observing the relationship between alcohol use and inflammation. Another limitation of the present study is that no diagnostic information was collected about current or past alcohol or other substance use disorders. The inclusion of such clinical information in future work would be useful, given that inflammatory changes are likely related to clinical severity and chronicity of substance use e. Similarly, we did not collect diagnostic information about other psychiatric disorders such as depression, anxiety and bipolar disorders. This information should also be included in future research, given the emerging link between psychiatric illness and altered inflammatory signaling Reus et al. Another limitation of the present study is that subjects were scheduled throughout the day, and blood collection times were not standardized across participants. Future studies should consider controlling for the time of day when blood collections were performed, given that cytokines and other immune mediators are influenced by circadian rhythms Lange et al. Further, the present study did not administer urine-drug screens to verify self-reported cannabis use. Future studies should incorporate an objective biological measure of cannabis and other illicit drug use in order to corroborate self-report data. Also, the present study included some light cigarette smokers e. Although this pattern of substance use serves to make the present results more generalizable across the heavy-drinking population, future studies would ideally recruit subjects with no cigarette or illicit drug use, in order to more specifically examine the relationship between alcohol use and inflammation. In addition, the present study did not directly measure circulating LPS in the blood. The addition of such a measure, as done in previous human studies Bala et al. Finally, the present study includes only cross-sectional data, which means that causal conclusions about the relationship between alcohol use and inflammation cannot be drawn. To test causal hypotheses, future longitudinal work should examine how changes in drinking patterns over time may impact inflammatory markers. In light of previously demonstrated associations between alcohol, cannabis and inflammation, the present results can serve to inform the selection of inflammatory markers to test in future analyses e. Ultimately, convergence between human and animal studies of alcohol consumption and inflammatory signaling across brain and peripheral tissues would provide the most compelling evidence for better understanding the relationship between inflammation and alcohol use, including explicating the possible role of peripheral immune signaling. These results also highlight the need for future work exploring the potential role for cannabinoids such as THC and CBD as anti-inflammatory treatments in the context of alcohol use disorders. Overall, despite the preliminary nature of these results and the need for replication and corroboration across human and animal work, our findings provide promising initial data to inform future investigations, with the goal of ultimately leveraging knowledge of the role of inflammatory signaling in alcohol use disorders to develop more effective treatments focused on novel targets within the immune system. One slight outlier remains in plot of standardized residuals for IL-6 models. Removal of this value does not change the overall pattern of significant results. To maintain the 3 SD cutoff for removing outliers, we have allowed this point to remain in the analysis. As a library, NLM provides access to scientific literature. Alcohol Clin Exp Res. Published in final edited form as: Alcohol Clin Exp Res. Find articles by Hollis C Karoly. Find articles by L Cinnamon Bidwell. Find articles by Raeghan Mueller. Find articles by Kent Hutchison. Issue date Mar. PMC Copyright notice. The publisher's version of this article is available at Alcohol Clin Exp Res. Open in a new tab. The authors have no conflicts of interest or financial disclosures to report. Similar articles. Add to Collections. Create a new collection. Add to an existing collection. Choose a collection Unable to load your collection due to an error Please try again. Add Cancel. Heavy Drinking Days a. Total Drinks a. Total Drinking Days a. Maximum Drinks a. Cannabis Days a. Total Cigarettes a. Interaction Models.

United States v. Maturin-Barraza, No. 09-2211 (10th Cir. 2010)

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