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Alcohol Research:

Current Reviews RESEARCH Current Reviews

VOLUME 39 • NUMBER 1 • 2018 THE JOURNAL OF THE NATIONAL INSTITUTE ON ALCOHOL AND

Binge Drinking: Predictors, Patterns, and Consequences Volume 39 • Number 1 National Institute on Editorial Advisory Board Readers should note that disclosure of a competing and Alcoholism financial interest does not imply that the information in the article is questionable or that conclusions are Robert M. Anthenelli, M.D., Department of , biased. Note, too, that Alcohol Research: Current Reviews George F. Koob, Ph.D. University of California San Diego, San Diego, California is not in the position to verify the accuracy of disclosure Director statements made by authors. We rely instead on authors Raul Caetano, M.D., Ph.D., School of , to provide complete and accurate information. This Bridget Williams-Simmons, Ph.D. University of Texas, Dallas, Texas information is provided at the end of each article. Director, Office of Science Policy and Communications Tammy Chung, Ph.D., Departments of Psychiatry Alcohol Research: Current Reviews (ISSN: 2168-3492) is Jennifer A. Hobin, Ph.D. and , University of Pittsburgh, Pittsburgh, a peer-reviewed journal produced twice per year under Editor in Chief, Alcohol Research: Current Reviews Pennsylvania contract to ICF by the National Institute on Alcohol Abuse Chief, Science Policy Branch, Office of Science Policy and and Alcoholism (NIAAA). Cara Anjos Breeden, M.L.S., is Communications Jonathan Morgenstern, Ph.D., The Donald and the project officer. Opinions expressed in contributed Barbara Zucker School of Medicine at Hofstra/Northwell, articles do not necessarily reflect the views of NIAAA. Troy J. Zarcone, Ph.D. Great Neck, New York Editor in Chief, Alcohol Research: Current Reviews The U.S. government does not endorse or favor any specific commercial product or commodity. Trade or Health Science Administrator, Science Policy Branch, Steve Nelson, M.D., School of Medicine, Louisiana State proprietary names appearing in this publication are Office of Science Policy and Communications University Health Sciences Center, New Orleans, Louisiana used only because they are considered essential in the Subhash C. Pandey, Ph.D., Alcohol Research Center, context of the studies reported herein. Unless otherwise Scientific Review Editors University of Illinois at Chicago, Chicago, Illinois noted in the text, all material appearing in this journal Volume 39, Number 1 is in the public domain and may be reproduced without Marisa Roberto, Ph.D., Department of Neuroscience, The permission. Citation of the source is appreciated. Scripps Research Institute, La Jolla, California Shivendra D. Shukla, Ph.D., Margaret Proctor Mulligan Subscriptions can be ordered online at Endowed Professor in Medical Research, School of Shivendra D. Shukla, Ph.D., School of Medicine, University https://bookstore.gpo.gov or by using the form on Medicine, University of Missouri, Columbia, Missouri of Missouri, Columbia, Missouri the back cover of this issue. Recent issues of Alcohol Research: Current Reviews are available online at Susan Tapert, Ph.D., Professor of Psychiatry, School of Rajita Sinha, Ph.D., Department of Psychiatry, Yale https://www.arcr.niaaa.nih.gov. Back issues are archived Medicine, University of California, San Diego, California University School of Medicine, New Haven, Connecticut at https://www.arcr.niaaa.nih.gov/archives.htm.

Aaron M. White, Ph.D., Senior Scientific Adviser to the Edith V. Sullivan, Ph.D., Department of Psychiatry and Issues of Alcohol Research: Current Reviews are Director, Office of the Director, National Institute on Alcohol Behavioral Sciences, Stanford University School of indexed in PubMed at https://www.ncbi.nlm.nih. Abuse and Alcoholism, Rockville, Maryland Medicine, Stanford, California gov/pubmed. In addition, a topic index of journal articles from 2008 to the present is available at Jennifer Thomas, Ph.D., Center for Behavioral Teratology, https://www.arcr.niaaa.nih.gov/topics.htm. ICF San Diego State University, San Diego, California

Alcohol Research: Current Reviews is committed Steve Mitchell, M.S., Managing Editor to publishing only the most informative, accurate, Melinda Moyer, M.S., Program Manager and impartial information possible from the field Christy Vaughn, Senior Editor of alcohol research. We hold authors accountable Jane Colilla, Editor for the articles submitted to the journal and require Rajendra Patel, Layout/Production Specialist authors to declare any potentially competing financial interests that might be construed as influencing the results or interpretations of a reported study.

Alcohol Research: About the Cover

Current Reviews ALCOHOL RESEARCH Current Reviews , broadly defined as consuming a VOLUME 39 • NUMBER 1 • 2018 THE JOURNAL OF THE NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM large amount of alcohol in a short period of time, is a Binge Drinking: Predictors, Patterns, and Consequences dangerous—and sometimes fatal—practice. Despite the adverse consequences associated with it, far too many people, particularly young adults, binge drink. This issue of Alcohol Research: Current Reviews examines the predictors, prevalence, and patterns of binge alcohol consumption Volume 39 • Number 1 and its effects on health and well-being. TTABLEABLE OF CONTENTS

Binge Drinking: Predictors, Patterns, and Consequences

1 Editors’ Note Aaron M. White, Susan Tapert, and Shivendra D. Shukla

FEATURES 5 Adolescent Binge Drinking: Developmental Context and Opportunities for Prevention Tammy Chung, Kasey G. Creswell, Rachel Bachrach, Duncan B. Clark, and Christopher S. Martin

SIDEBAR 17 Drinking Patterns and Their Definitions Alcohol Research: Current Reviews Editorial Staff

SIDEBAR 19 Surveys That Include Information Relevant to Binge Drinking Alcohol Research: Current Reviews Editorial Staff 23 The Epidemiology of Binge Drinking Among College-Age Individuals in the Heather Krieger, Chelsie M. Young, Amber M. Anthenien, and Clayton Neighbors SIDEBAR 31 “Maturing Out” of Binge and Problem Drinking Matthew R. Lee and Kenneth J. Sher

FOCUS ON 43 NIAAA’s College Alcohol Intervention Matrix: CollegeAIM Jessica M. Cronce, Traci L. Toomey, Kathleen Lenk, Toben F. Nelson, Jason R. Kilmer, and Mary E. Larimer 49 High-Intensity Drinking Megan E. Patrick and Beth Azar 57 Differences in Binge Drinking: Prevalence, Predictors, and Consequences Richard W. Wilsnack, Sharon C. Wilsnack, Gerhard Gmel, and Lori Wolfgang Kantor 77 Binge Drinking’s Effects on the Developing Brain—Animal Models Susanne Hiller-Sturmhöfel and Linda Patia Spear 87 Effects of Binge Drinking on the Developing Brain: Studies in Humans Scott A. Jones, Jordan M. Lueras, and Bonnie J. Nagel SIDEBAR 97 NIH’s Adolescent Brain Cognitive Development (ABCD) Study Alcohol Research: Current Reviews Editorial Staff 99 Binge Drinking’s Effects on the Body Patricia E. Molina and Steve Nelson

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SM National Institute on Alcohol Abuse and Alcoholism Alcohol and your health Publications Distribution Center P.O. Box 10686 Research-based information from the National Institutes of Health U.S. DEPARTMENT OF HEALTH AND HUMAN SERVICES Rockville, MD 20849-0686 NIH...Turning Discovery Into Health® Phone: 888-MY-NIAAA (888-696-4222) https://www.RethinkingDrinking.niaaa.nih.gov EDITORS’ NOTE

Binge Drinking Predictors, Patterns, and Consequences

Aaron M. White, Susan Tapert, and Shivendra D. Shukla

Aaron M. White The National Institute on Alcohol Abuse and Alcoholism defines binge drinking as a pattern of consumption that causes blood alcohol concentration to rise to .08%—the legal limit for adults ages 21 or older operating a motor vehicle—or more. This level typically occurs after a woman consumes four drinks or a man consumes five drinks—in about 2 hours. Research suggests that three out of four adolescents who drink, and half of adults who drink, engage in binge drinking each month. Because of the impairments it produces, binge drinking increases the likelihood of a host of acute consequences, including injuries and deaths from falls, burns, drownings, car crashes, and alcohol overdoses. Of the roughly Susan Tapert 88,000 deaths that result from alcohol use in the United States each year, more than half stem from binge drinking,1 and binge drinking accounts for 77% ($191.1 billion) of the annual economic cost of alcohol misuse.2 Several important questions related to binge drinking warrant further explora- tion. For instance, how have patterns of binge drinking changed in recent years in the United States? What is known about drinking at levels far beyond the standard binge thresholds? How does the peak number of drinks a person con- sumes relate to risks for experiencing alcohol-related harm? Are there unique risks of binge drinking for women? How does binge alcohol consumption affect brain development and function? What is the effect of binge drinking on organs other Shivendra D. Shukla than the brain? The articles in this volume explore what is known about these and other topics related to binge drinking. In Adolescent Binge Drinking: Developmental Context and Opportunities for Prevention, Chung and colleagues examine binge drinking among adoles- Aaron M. White, Ph.D., is a senior cents. National surveys suggest that drinking, including binge drinking, is declin- scientific adviser to the director, ing among teens. The declines have been greater for young males than females, Office of the Director, National leading to a significant narrowing of differences in alcohol misuse between the Institute on Alcohol Abuse and . For instance, in the 1975 Monitoring the Future study, 49% of male Alcoholism, Rockville, Maryland. high school seniors reported binge drinking, compared to only 26% of female se- niors.3 By 2014, binge drinking declined in both genders, but more so for males, Susan Tapert, Ph.D., is a profes- with 22% of males and 17% of females crossing the binge threshold. The authors sor of psychiatry in the School of examine the consequences of binge drinking for teens and discuss the develop- mental context in which adolescent drinking occurs. Medicine, University of California, Considerable research has focused on alcohol use, particularly binge drinking, San Diego, California. among college students. Young adults in college are more likely to binge drink than their noncollege peers, though the differences are narrowing. Krieger and Shivendra D. Shukla, Ph.D., is colleagues, in The Epidemiology of Binge Drinking Among College-Age the Margaret Proctor Mulligan Individuals in the United States, explore current knowledge of binge drinking Endowed Professor in Medical and its consequences among college students and other young adults. As with Research at the School of binge drinking among high school students, binge drinking has declined among Medicine, University of Missouri, college students, but less so among college women. In contrast to the declines in Columbia, Missouri. binge drinking at colleges, binge drinking increased among young adults in the military and among young women in the general population. The authors exam- ine the characteristics (i.e., race and ethnicity, Greek affiliation, and drinking -mo tives) of young adults who engage in binge drinking relative to those who do not. Traditionally, binge drinking has been studied using a single threshold, typ- ically four or more drinks for females and five or more drinks for males, or just

Editors’ Note | 1 five or more drinks for both males and females. However, knowing that someone binge drank does not reveal how much alcohol he or she actually consumed. Using a single binge threshold has the unintended consequence of assigning the same level of potential risk to all binge drinkers, regardless of how much they drank. Recent studies have examined the prevalence and correlates of drink- ing at levels two and three times the standard binge thresholds, also known as high-intensity or extreme binge drinking. In High-Intensity Drinking, Patrick and Azar assess current knowledge of the prevalence of high-intensity drinking, the contexts in which it tends to occur (e.g., sporting events and 21st birthday celebrations), and the consequences of drinking at these high peak levels. Recent studies suggest that long-standing differences between men and wom- en in alcohol use are narrowing. This is concerning, given evidence that women might experience certain health effects of alcohol, such as of the liver and cardiovascular disease, at lower levels of consumption than men.4 In Gender Differences in Binge Drinking: Prevalence, Predictors, and Consequences, Wilsnack and colleagues examine changes in binge drinking and related out- comes in males and females, and they explore potential explanations for the con- vergence of alcohol misuse between the genders. Over the past few decades, a paradigm shift has occurred in our understanding of brain development. It is now clear that brain development, once thought to taper off with the end of childhood, enters a unique phase during the adoles- cent years. Changes in the brain during adolescence lead to improvements in the ability to engage in complex social behaviors and to make forward-thinking decisions.5 Hiller-Sturmhöfel and Spear, in Binge Drinking’s Effects on the Developing Brain—Animal Models, explore animal research findings demon- strating that repeated binge exposure during adolescence causes structural and functional damage in the brain that leads to social and cognitive deficits during adulthood. In Effects of Binge Drinking on the Developing Brain: Studies in Humans, Jones and colleagues discuss evidence from human research on the effects of repeated binge drinking on adolescent brain development and brain function, including lingering deficits in attention and memory. The chronic health effects of alcohol misuse are well-documented. Alcohol consumption is associated with roughly half the liver cirrhosis deaths in the United States and increases the risk of cancers of the mouth, throat, liver, and breast. Yet the health effects of binge drinking are less well-known. In Binge Drinking’s Effects on the Body, Molina and Nelson review what is known about the effects of binge drinking on organ systems, including the , gastro- intestinal tract, and brain. The research explored in this volume indicates that crossing the binge threshold increases the risk of acute harm, such as injuries, memory blackouts, and overdos- es, and that the risk of negative outcomes increases further at higher peak levels of consumption. Repeated binge drinking during the teen years can alter the tra- jectory of adolescent brain development and cause lingering deficits in attention, memory, and other cognitive functions. Binge drinking can damage organs other than the brain, including the , liver, and heart. While binge drinking declined in recent years for men in some age groups, women exhibited either smaller declines or increases, leading to gender convergence in alcohol use and related harms. Hopefully, insight into the prevalence and consequences of binge drinking, and the social and developmental contexts within which it occurs, will lead to improvements in prevention strategies aimed at minimizing binge drinking and the associated harms.

2 | Vol. 39, No. 1 Alcohol Research: Current Reviews References

1. Kanny D, Brewer RD, Mesnick JB, et al. Vital signs: Alcohol poisoning deaths—United States, 2010–2012. MMWR Morb Mortal Wkly Rep. 2015;63(53):1238-1242. PMID: 25577989. 2. Sacks JJ, Gonzales KR, Bouchery EE, et al. 2010 National and state costs of excessive alcohol consumption. Am J Prev Med. 2015;49(5):e73-e79. PMID: 26477807. 3. Johnston LD, O’Malley PM, Miech RA, et al. Demographic Subgroup Trends Among Adolescents in the Use of Various Licit and Illicit , 1975–2014. Ann Arbor, MI: Institute for Social Research, University of Michigan; 2015. Monitoring the Future Occasional Paper 83. http://monitoringthefuture.org/pubs/occpapers/mtf-occ83.pdf. Accessed October 11, 2017. 4. Nolen-Hoeksema S. Gender differences in risk factors and consequences for alcohol use and problems. Clin Psychol Rev. 2004;24(8):981-1010. PMID: 15533281. 5. Lamblin M, Murawski C, Whittle S, et al. Social connectedness, mental health and the adolescent brain. Neurosci Biobehav Rev. 2017;80:57-68. PMID: 28506925.

Editors’ Note | 3 Treatment for Alcohol Problems: Finding and Getting Help

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Follow us on Twitter @NIAAAnews ALCOHOL RESEARCH: Current Reviews Adolescent Binge Drinking Developmental Context and Opportunities for Prevention

Tammy Chung, Kasey G. Creswell, Rachel Bachrach, Duncan B. Clark, and Tammy Chung, Ph.D., is an asso- Christopher S. Martin ciate professor; Rachel Bachrach, Ph.D., is a postdoctoral fellow; Binge drinking, commonly defined as consuming five or more standard drinks per Duncan B. Clark, M.D., Ph.D., is occasion for men and four or more drinks for women, typically begins in adolescence. a professor; and Christopher S. Adolescents, although they may drink less often, tend to consume higher quanti- Martin, Ph.D., is an associate ties of alcohol per occasion compared with adults. This developmental difference in professor, all in the Department pattern of alcohol consumption may result, in part, from maturational changes that of Psychiatry, University involve an adolescent-specific sensitivity to certain alcohol effects and greater pro- pensity for risk-taking behaviors, such as binge drinking. Adolescent binge drinking is of Pittsburgh, Pittsburgh, associated with a range of acute alcohol-related harms, some of which may persist Pennsylvania. into adulthood. The prevalence of binge drinking, including high-intensity drinking (i.e., 10 or more and 15 or more drinks per occasion), has declined among ado- Kasey G. Creswell, Ph.D., is lescents in recent years. Overall, however, the proportion of youth who engage in an assistant professor in the binge drinking remains high. This article reviews the definition and prevalence of Department of Psychology, binge drinking in adolescence, trajectories of binge drinking and their correlates, and Carnegie Mellon University, implications for prevention. Pittsburgh, Pennsylvania. Key words: Alcohol consumption; binge drinking; brain development; college students; high-intensity drinking; underage drinking

Compared with adults, adolescent This article reviews various defi- Definitions of Binge Drinking drinkers tend to consume higher nitions of binge drinking, the acute for Youth quantities of alcohol per occasion but adverse consequences associated drink less frequently.1 Thus, underage with binge drinking, the prevalence Binge drinking, or an episode of drinkers ages 12 to 20 typically con- of adolescent binge drinking, and high-volume alcohol consumption, sume 4 to 5 drinks per drinking epi- demographic factors (e.g., gender has been defined in various ways.6,7 sode, which is nearly double the aver- and race/ethnicity) associated with (For more information, see Drinking age of the 2 to 3 drinks usually con- adolescent binge drinking. It then Patterns and Their Definitions in sumed by adults (older than age 25).1 discusses the developmental context this issue.) According to the National Most of the alcohol consumption of of adolescent binge drinking, includ- Institute on Alcohol Abuse and ing adolescent-specific sensitivity to 8 underage drinkers occurs during Alcoholism (NIAAA), “binge drink- certain alcohol effects that may con- ing” refers to alcohol consumption “binge” episodes characterized by 2,3 tribute to episodes of high-volume that brings the blood alcohol concen- drinking high quantities. This binge alcohol consumption in adolescence. tration (BAC) to .08 g/dL, which is pattern of consumption has been After a summary of trajectories of commonly associated with acute im- linked to serious alcohol-related harm, binge drinking in adolescence, tra- pairment in motor coordination and such as alcohol poisoning, as well as to jectory correlates representing risk cognitive functioning.9 BACs of more sometimes fatal injuries and accidents factors and young-adult outcomes, than .08 g/dL typically occur in men resulting from acute intoxication.4 The and possible neurocognitive conse- after consuming five or more drinks adverse consequences of adolescent quences of adolescent binge drink- in about 2 hours, and in women after binge drinking affect not only the ado- ing, the implications of research on consuming four or more drinks. This lescents but also their families, peers, adolescent binge drinking for pre- is known as the “5+/4+” binge defini- and community.5 vention efforts are briefly reviewed. tion. This definition is consistent with

Adolescent Binge Drinking | 5 epidemiological data indicating an more drinks for males, respectively, (2.7% of those ages 12 to 17), many association at the population level be- have been used to define high-inten- more youth report binge alcohol use tween greater frequency of 5+/4+ binge sity drinking.12-14 These definitions (6.1%)23 and may experience acute ad- episodes and more adverse drinking- specify thresholds that are two to three verse effects from binge drinking that related consequences.10 times higher than the 5+/4+ binge are not covered by diagnostic criteria. When applied to adolescents, definition and have been examined binge-drinking definitions based on in part because of limitations in the adult levels of alcohol intake (e.g., reliability of the 5+/4+ binge definition Prevalence of Adolescent 5+/4+ drinks per occasion) often are for identifying drinkers with BACs of Binge Drinking too high. Children and adolescents are more than .08 g/dL.15 As a point of likely to reach BACs of more than .08 reference, among adolescent drinkers, Numerous studies have assessed the g/dL at lower levels of consumption alcohol-related blackouts, or acute al- prevalence of adolescent binge drink- due, in part, to factors such as smaller cohol-related memory loss, may occur ing in the United States, as well as body size. Donovan used an updated after consuming nine or more drinks in other countries. These studies also Widmark equation and population per occasion for males and five or more have assessed the association between data on average body weight in boys drinks for females.16 binge-drinking rates and demographic and girls to estimate the levels of characteristics. drinking that would produce BACs of more than .08 g/dL in youth ages 9 to Acute Adverse Consequences Trends in the Prevalence of 17.11 For those ages 9 to 13, a binge of Binge Drinking Adolescent Binge Drinking in the episode was estimated to occur with United States intake of 3 or more drinks within a Acute negative alcohol-related con- 2-hour period; for those ages 14 to 15, sequences generally show a dose- Three national surveys in the United with 4 or more drinks for boys and 3 response relationship with binge drink- States provide data on the prevalence or more drinks for girls; and for those ing,17 such that greater risk for many of adolescent binge drinking, includ- ages 16 to 17, with 5 or more drinks adverse consequences has been associ- ing the National Survey on Use for boys and 3 or more drinks for girls. ated with higher drinking quantities and Health (NSDUH), which until These proposed binge-drinking thresh- and more frequent binge episodes.18-20 2015 defined binge drinking as con- olds for youth are theoretical and based A significant literature has examined sumption of five or more drinks on the on estimated, rather than observed, the diverse acute health harms associ- same occasion;* the Monitoring the BACs. Nevertheless, the identification ated with binge drinking, such as alco- Future (MTF) survey, which defines it of lower drinking-quantity thresholds hol poisoning, alcohol-related black- as five or more drinks in a row; and the to define binge drinking for younger outs and injury, involvement in car Youth Risk Behavior Survey (YRBS), drinkers suggests that the use of stan- crashes and fatalities, alcohol-related which defines it as five or more drinks dard adult-based binge definitions physical and sexual assault, increased of alcohol in a row—that is, within a may underestimate the prevalence of risk for sexually transmitted infection, couple of hours. (For more informa- drinking behavior that leads to BACs and problems at school or work.4,21 tion on these surveys, see Surveys That of more than .08 g/dL, particularly Risk behaviors associated with binge Include Information Relevant to among females and youth. drinking may include, for example, Binge Drinking in this issue.) Thus, Extreme binge, or high-intensity, simultaneous use of other substances until 2015, these surveys all used the drinking involves the intake of dan- (e.g., marijuana) and greater likelihood same threshold to define binge drink- gerously high quantities of alcohol of riding with an intoxicated driver.22 ing in males and females, albeit with per occasion. (For more information, Although many of the acute adverse slightly different wording and with see High-Intensity Drinking in this consequences of binge drinking are not differences in the time frame used issue.) Thresholds of 10 or more drinks unique to adolescents, young drinkers to assess binge drinking (i.e., within (i.e., double the usual definition of may be at higher risk than adult drink- the past month for the NSDUH and binge drinking of 5 or more drinks) ers for certain acute alcohol-related YRBS, and within the past 2 weeks for and 15 or more drinks per occasion harms (e.g., alcohol poisoning) because the MTF). The NSDUH has collected (i.e., triple the usual definition of of their relative inexperience with al- annual data since 1991 on individuals binge drinking of 5 or more drinks), cohol’s effects. Importantly, although ages 12 and older using interviews as well as gender-specific cutoffs of 8 some adolescent heavy drinkers meet conducted in the home.5 In contrast, or more drinks for females and 10 or the criteria for an alcohol use disorder both MTF and YRBS are school-based

*Since 2015, the NSDUH defines binge drinking as consumption of 4 or more drinks for women or 5 or more drinks for men on the same occasion on at least 1 day in the past 30 days.

6 | Vol. 39, No. 1 Alcohol Research: Current Reviews surveys. MTF has collected annual of all high school students reported drinking day. Thus, students in Nordic data since 1975 from 12th graders, binge drinking in the past month, countries and the British Isles generally and since 1991 from 8th, 10th, and increasing from 10.4% in 9th graders reported consuming a higher average 12th graders.24 YRBS has collected to 24.6% in 12th graders.29 According quantity than did students in south- data biennially since 1991 from 9th to to the 2015 MTF survey, 4.6% of eastern Europe (e.g., Greece or Italy).30 12th graders.25 8th graders, 10.9% of 10th graders, By comparison, the 2011 ASSAD All three surveys show similar time and 17.2% of 12th graders reported survey found that among students ages trends in adolescent binge drinking.26 binge drinking in the 2 weeks prior to 12 to 17 who reported drinking in the The MTF data indicate a peak in the the survey.24 week prior to the survey (17.5% of all prevalence of youth binge drinking in The results from these three na- students queried), more than one-third the late 1970s to early 1980s, followed tional surveys are broadly consistent (36.2%) drank 5 or more drinks in by a decrease from 41% in 1983 to in a given year, although YRBS data a day.31 28% in 1992.24 In the 2015 MTF sur- generally indicate somewhat higher In general, countries with lower vey, binge drinking in the past 2 weeks binge prevalences compared with legal drinking ages have a higher prev- was reported by 4.6% of 8th graders, NSDUH and MTF, and MTF tends alence of adolescent binge drinking 10.9% of 10th graders, and 17.2% to report higher prevalences compared compared with countries with higher of 12th graders.24 This reduction in with NSDUH.26 The differences in legal drinking ages.32 Also, rates of youth binge-drinking prevalence over binge-drinking prevalence across the adolescent binge drinking generally are time may reflect factors such as en- surveys may result from methodologi- higher in many European countries4 actment of a minimum legal drinking cal differences, such as sampling strat- and Australia31 than in the United age of 21 and other alcohol regulatory egy used, survey location (e.g., school States. However, such variations in policies.4,27 Time-trend data from or home), type of data collection (e.g., binge-drinking prevalence across stud- the YRBS (from 1999 to 2013) and paper survey or self-administered ies need to be interpreted with caution NSDUH (from 2002 to 2014) indi- computer assessment), item wording, because methodological differences cate a similar decrease in youth binge and time frames for querying binge (e.g., in sampling method, ages cov- 5,25 drinking in recent years. drinking.26 Interpretation of results ered, item wording, time frames, and The prevalence of high-intensity from these national surveys also needs the definition of a ) exist drinking (10 or more or 15 or more to consider that use of the “5+” binge across surveys. drinks in a row in the past 2 weeks) definition in these surveys may un- was relatively stable among high school derestimate the prevalence of binge Adolescent Binge-Drinking seniors in the MTF from 2006 to drinking in younger adolescents and Prevalence by Demographic 2012, but, like binge drinking, has females, because, as mentioned earlier, Characteristics shown a decline in recent years. Thus, lower drinking-quantity thresholds to In general, males tend to report the prevalence of consuming 10 or define binge drinking are indicated in higher rates of binge drinking in more drinks in a row declined from this age group.11 10.4% in 2012 to 6.1% in 2015, and adolescence than do females (see the prevalence of consuming 15 or Figure 1).13,14,23,24 These gender dif- International Surveys of Adolescent ferences typically increase with age more drinks in a row declined from Binge-Drinking Prevalence 5.5% in 2012 to 3.5% in 2015.24 during adolescence.22,30,33 However, In all three national surveys, International data on the prevalence time-trend data from MTF have binge-drinking prevalence increases of adolescent binge drinking are avail- indicated a narrowing of the gender with age during adolescence. For ex- able from sources such as the European gap starting in the mid-1970s, par- ample, in 2015, the most recent year School Survey Project on Alcohol ticularly among high school seniors. in which all three national surveys and Other Drugs (ESPAD) and the Thus, in the 1975 MTF, 49% of male collected data on binge drinking, Australian School Students Alcohol high school seniors, but only 26% of NSDUH indicated that 9.6% of youth and Drug (ASSAD) survey. In 2011, females, reported binge drinking, cor- ages 12 to 17 reported alcohol use the ESPAD report on 15- to 16-year- responding to a 23-percentage-point in the past month, with roughly half old students in 36 European countries difference. By 2014, in contrast, a (i.e., 5.8%) of these drinkers reporting indicated that the average prevalence mere 5-percentage-point difference binge drinking in the past month.28 of consuming 5 or more drinks on at existed between male (22%) and fe- Among respondents ages 12 to 17 least 1 occasion in the past 30 days male (17%) high school seniors who in the 2015 NSDUH, past-month was 39% across countries.30 However, reported binge drinking.33 Conversely, binge-drinking prevalence increased ESPAD countries differed in the aver- NSDUH time-trend data from 2002 from 0.5% at ages 12 to 13 to 15.3% age alcohol quantity that students re- to 2012 for youth ages 12 to 17 in- at age 17. In the 2015 YRBS, 17.7% ported consuming on their most recent dicate that although binge drinking

Adolescent Binge Drinking | 7 decreased for both males (from 11.3% Latinos (6.3%) compared with Blacks in the District of Columbia, with an in 2002 to 7.4% in 2012) and females (3.6%) and Asians (1.5%).23 MTF overall estimate of 18.0%.35 High- (from 10.2% in 2002 to 6.8% in time-trend data from 1975 to 2014 intensity or extreme binge-drinking 2012), with more males than females suggest that these race/ethnic dif- prevalence was especially high among reporting binge drinking at both time ferences may differ by year in high high school seniors in the Midwest.13 points, there was little support for school.33 For example, among 8th- Binge-drinking prevalence also differed a narrowing of the gender gap over grade students, more Hispanics tended by urban versus rural setting, with high these years.34 The time-trend results to report binge drinking compared school students living in rural areas for gender differences from the MTF with Whites and Blacks. Among 10th- tending to report the highest rates of and NSDUH surveys are not directly and 12th-grade students, however, binge drinking.33 These regional differ- comparable because of differences in Hispanics and Whites were more likely ences suggest that factors such as local the ages covered, as well as in item to report binge drinking than were and regional norms regarding alcohol wording and time frames assessed Blacks. use, as well as local alcohol regulatory (i.e., the MTF asked about 5 or more In the United States, binge-drink- policies and enforcement, have an drinks in a row in the past 2 weeks, ing prevalence also varies by region, important influence on prevalence of whereas the NSDUH asked about 5 or with differences observed between and binge drinking. more drinks on an occasion in the past within states (see Figure 2).33 For ex- month). Nevertheless, both surveys ample, based on recent NSDUH data, indicate greater binge-drinking preva- past-month binge-drinking prevalence Developmental Context of lence among male than among female among underage drinkers ages 12 to Adolescent Binge Drinking adolescents.22 20 at the state level was highest in four The prevalence of adolescent binge states in the Northeast, four states in During adolescence, ongoing brain drinking in the United States also the Midwest, the District of Columbia, development and rapid changes in differs by race/ethnicity (see Figure 1). and one state in the West.35 Even physical maturation occur in the Among adolescents ages 12 to 17 in within a region, such as the District of context of a shift from parents and the 2014 NSDUH, the prevalence of Columbia, subregions differed in the family to peers as a primary source of past-month binge drinking was higher prevalence of past-month binge drink- support and guidance.36,37 These nor- among Whites (7.1%) and Hispanics/ ing, ranging from 10.8% to 42.4% mative, adolescent-specific changes in

Figure 1 Prevalence of binge drinking in the past 30 days among 12- to 20-year-olds, by age, , and race/Hispanic origin, as reported in the 2013 NSDUH.

8 | Vol. 39, No. 1 Alcohol Research: Current Reviews physical maturation and social context can contribute to the risk for binge drinking. In particular, the fine tun- ing of the neural circuitry that occurs during this developmental period is associated with an adolescent-specific elevation in the ability to consume alcohol, which appears to be conserved across species.38 Animal (e.g., rodent) models indicate that neural changes occurring in adolescence may tem- porarily increase sensitivity to certain alcohol effects (e.g., rewarding effects) that promote consumption within a drinking episode, while reducing sen- sitivity to other effects (e.g., sedative effects) that may help to limit drinking during an episode.38 Evidence for such an adolescent-specific sensitivity to alcohol effects in humans is sparse but aligns with animal models to suggest that compared with their adult coun- Figure 2 Binge alcohol use in the past month among individuals ages 12 to 20, by substate terparts, human adolescents may be region in the United States. Note: For substate region definitions, see the 2012–2014 more sensitive to alcohol’s rewarding NSDUH, substate region definitions at www.samhsa.gov/data. Source: SAMHSA, and effects39 and less sen- Center for Behavioral Health Statistics and Quality, 2012, 2013, and 2014 NSDUH. sitive to its sedative effects.40 Related research has found that, among college students, high-intensity binge drinking of high-volume consumption through can increase the likelihood of high- (i.e., 8 or more/10 or more drinks for mechanisms such as peers providing volume consumption, rapid intoxica- females/males) is experienced as more access to alcohol, peer norms that are tion, and risk for certain alcohol- rewarding than non–high-intensity favorable to binge-drinking behav- related harms, such as blackouts.50 drinking (i.e., less than 8/10 drinks for 41 ior, and positive feelings generated Other contextual factors relevant to females/males). Furthermore, many by social activities that involve al- adolescent binge drinking include the college students reported willingness to cohol use.37,47 places where drinking occurs and the tolerate adverse alcohol effects in order Binge drinking among underage temporal patterning (e.g., weekend or to experience the positive effects associ- drinkers in the United States of- seasonal) of drinking. For example, ated with high-intensity drinking.41 ten involves distilled spirits, with certain places where adolescent binge The adolescent-specific shift from consumption of reported in less drinking occurs, such as at someone family to peers as important sources 48 of influence on youth attitudes and than one-third of binge episodes. For else’s home without parental super- behavior also can contribute to some youth, consumption of vision or at a bar or nightclub, have may reflect the intent to drink to been associated with greater risk for risk-taking behaviors, such as binge 51 drinking.42,43 Higher levels of sensation get drunk as quickly as possible. The alcohol-related violence. With regard seeking and impulsivity, which are as- preferential consumption of liquor to temporal patterning, the timing of sociated with risk-taking behaviors and by adolescents during binge episodes adolescent binge drinking shows some binge drinking, tend to be endorsed is particularly concerning because it predictability: Binge drinking may be more often by adolescent males than has been linked with increased risk for more likely to occur during weekends, by females, which may help explain the alcohol-related consequences, such as summer and spring breaks, holidays generally greater prevalence of binge blackouts or injury.49 (e.g., New Year’s Eve), and occasions drinking among males.44 Risk-taking Young drinkers also often lack such as prom and sports events.52 behavior may be facilitated by the pres- knowledge regarding standard drink These contextual factors, in combi- ence of peers.43 Consistent with this servings, particularly for spirits, which nation with an adolescent-specific observation, adolescent binge drinking can result in overpouring—that is, sensitivity pattern to alcohol effects tends to occur in social contexts with pouring greater volumes than used for and the peer social context of drinking, peers.45,46 This may encourage episodes standard drink servings.50 Overpouring may interact with individual difference

Adolescent Binge Drinking | 9 factors, such as heritable risk and ex- trajectories. In some studies, non- Developmental factors associated posure to trauma, in contributing to binge trajectories may include youth with an increase in binge drinking increased risk for binge drinking and who drink but do not report binge during adolescence include, for exam- related harm in adolescence.38 episodes, as well as abstainers.59,60 ple, reduced parental monitoring as Trajectories indicating persistence of youth mature37,66 and greater indepen- binge drinking from adolescence into dence (e.g., obtaining a driver’s license) Binge-Drinking Trajectories young adulthood, which typically in daily activities.36 In addition, for in Adolescence represent a minority of youth in com- some youth, onset of binge drinking munity samples, tend to show onset may be associated with important The onset of alcohol use peaks of binge drinking in early adolescence school transitions (e.g., junior high to during grades 7 to 11.24 By 8th (i.e., at ages 12 to 13) and an increase high school or high school to college), grade, 11% of students report having to weekly or more frequent binges which can involve restructuring of peer been drunk (a self-report proxy for by late adolescence (i.e., at ages 17 to groups and increased opportunities to high-quantity consumption) at least 18).7 Other binge-drinking trajectories engage in alcohol use.36 Importantly, once in their lifetime, with an increase are characterized by earlier (e.g., age processes of peer selection and peer to 29% among 10th graders and 47% 16 and younger) versus later (e.g., age influence have been associated with among high school seniors.24 Reports 17 and older) onset of binge drinking changes in binge drinking in adoles- of the onset of consuming 3 or more or by a pattern of adolescent-limited cence.67-69 In particular, selection of drinks per occasion begin to increase binge drinking, in which binge drink- peers who engage in binge drinking between ages 13.5 and 15.5, and re- ing peaks in adolescence, then declines has been associated with an adoles- ports of an episode of binge drinking in early adulthood.7 One study that cent’s initiation and frequency of (5 or more drinks per occasion) start to followed a high-risk sample of youth binge drinking.69 rise around age 16.53 Although rates of into young adulthood identified four Several studies analyzed factors binge drinking peak between ages 18 types of binge-drinking† trajectories, associated with binge trajectories, rel- and 25,54 the onset of binge drinking including nonbinger (39.5%), infre- ative to nonbinge trajectories, at the (i.e., 3 or more or 5 or more drinks per quent (9.6%), late-onset moderate individual level. Nonbinge trajectories occasion) and episodes of being drunk (30.0%), and early-onset heavy drink- in these studies included youth who 57 typically occur in early to mid-adoles- ing (20.9%). Studies vary in the rel- abstained and youth who reported cence (i.e., ages 12 to 16). Early age ative proportions of youth in each tra- alcohol use below a given binge thresh- of first intoxication (younger than 15 jectory type because of methodological old. Risk factors identified in these years old) and rapid progression from factors, such as differences in sampling studies included, for example, engag- first drink to first intoxication both are (e.g., community vs. high-risk sample), ing in delinquent behavior, exposure early warning signs of heavy, particu- age range, binge-drinking definition, to more stressful life events, and lower larly binge, drinking.55,56 and whether nonbinge trajectories in- task persistence.61-63 Some of these Longitudinal studies that span ado- clude both abstainers and drinkers who risk factors may be associated with lescence through emerging adulthood do not report binge episodes. gender; for example, females may be (i.e., ages 12 to 25) have identified more likely to experience certain stress- three to five prototypical trajectories ful life events (e.g., sexual trauma), of binge drinking (see Figure 3).57-63 Correlates of Adolescent whereas males may be more likely to The trajectories derived in these studies Binge-Drinking Trajectories: be involved in delinquent behavior or provide useful heuristics for under- Risk Factors and Young- to show lower levels of impulse con- standing different patterns of change Adult Outcomes trol.44,70 Moreover, in contrast to youth in binge drinking across adolescence. in binge-drinking trajectories, youth in They highlight heterogeneity in course, Distinct trajectories of binge drink- nonbinge trajectories were more likely and differ with respect to age at onset ing are thought to reflect different to report greater self-efficacy to resist of binge drinking; timing, rate, and etiologic mechanisms.64 According to social pressure to engage in substance direction of change in binge drinking an ecological systems model,36,65 these use,62 as well as greater religiosity.63 (e.g., escalation and desistance); and etiologic mechanisms represent mul- With regard to the social context in frequency of binge drinking. tiple systems (e.g., family, peer group, which youth are nested, parental alco- Most youth in community sam- and community) that interact across holism and disrupted family relations ples fall into the low-frequency development to influence binge-drink- (e.g., parental separation or divorce) binge-drinking and nonbinge-drinking ing trajectories. each were associated with binge-drink-

†The study defined binge drinking as “5+ drinks in a row.”

10 | Vol. 39, No. 1 Alcohol Research: Current Reviews 5.0 Early-heavy Late-moderate 4.0 Infrequent

3.0 Nonbinger

2.0 Binge Drinking 1.0

0.0 12 13 14 15 16 17 18 19 20 21 22 23 Age in Years

Figure 3 Trajectories of binge drinking from adolescence through emerging adulthood. Estimated growth trajectories for the three groups are indicated by solid lines. Dashed black lines represent observed means of binge drinking at each age for each group. Observed frequencies of binge drinking (past year) ranged from 0 (none) to 5 (one to two times a week). Note: Early-heavy group, n = 99, 20.9% of the sample. Late-moderate group, n = 134, 30.0% of the sample. Infrequent group, n = 43, 9.6% of the sample. Nonbinger group, n = 176, 39.5% of the sample. Source: Chassin L, Pitts SC, Prost J. Binge drinking trajectories from adolescence to emerging adulthood in a high-risk sample: Predictors and outcomes. J Consult Clin Psychol. 2002;70(1):67-78. Copyright © 2002 by the American Psychological Association. Reprinted with permission. ing trajectories.57,62 Conversely, an include factors such as neighborhood ily, peer, and community influences on adolescent’s perception of high pa- and school environments, as well as youth binge drinking emphasize the rental disapproval of substance use local alcohol regulatory policies and need for coordinated, developmentally was prospectively associated with a enforcement. For example, one study tailored prevention programs that ad- nonbinge trajectory.60 Peer relations found that youth living in neigh- dress each of these multiple interacting also had an impact, because changes borhoods with higher densities of social systems to reduce risk. in binge drinking tended to occur in on-premise alcohol outlets (e.g., bars Compared with nonbinge trajec- parallel with changes in affiliation with and nightclubs) were more likely to tories, binge-drinking trajectories in drinking peers.60 However, despite the report binge drinking, controlling for adolescence, particularly frequent and robust influence of peers on drinking neighborhood-level socioeconomic chronic binge drinking, have been behavior, an adolescent’s report of high status.71 However, neighborhood risks associated with poorer functioning in parental disapproval of substance use may be buffered by protective factors. young adulthood. For example, youth weakened the effect of peers on binge In particular, a recent study found that in binge trajectories were more likely drinking,60,69 indicating the important a supportive school environment (e.g., to have an alcohol or other drug use role that parents play in providing alcohol prevention incorporated into disorder in young adulthood than clear messages to their children regard- the curriculum) was associated with re- those in nonbinge trajectories (which ing disapproval of underage drinking. duced adolescent binge drinking over may include abstainers and youth who It is important to note, however, that and above individual, family, and peer drink, but do not report binge epi- many individual and social risk factors risk factors.72 Further, comprehensive sodes, depending on the study).57,62,74,75 associated with adolescent alcohol and and stringent local alcohol control pol- In contrast, youth in nonbinge other substance use have a more gen- icies and enforcement have been asso- trajectories had better young-adult eral influence and are not necessarily ciated with lower levels of youth binge outcomes across domains such as edu- specific to binge drinking. drinking, highlighting the importance cational attainment and employment, Community-level influences on of these community-level factors.73 The family and peer relations, and mental adolescent binge-drinking trajectories unique and cumulative effects of fam- and physical health than did those in

Adolescent Binge Drinking | 11 binge trajectories, particularly those and aberrations in brain structure Adolescence,94 the IMAGEN study in who engaged in frequent, chronic and functioning.85-88 Some research Europe,95 and the Adolescent Brain binge drinking.57,59,62,76 suggests possible gender-specific ad- and Cognitive Development Study Other analyses have compared verse consequences of binge alcohol (https://abcdstudy.org), which are different binge-drinking trajectories consumption on neurocognition.89 examining the effects of alcohol and (e.g., chronic vs. adolescent-limited). However, other research has found no other substance use on the developing Such studies found that compared difference between adolescent heavy brain in adolescence, are poised to with adolescent-limited trajectories, drinkers (defined as 5+/6+ glasses, 10 g address these gaps in knowledge. chronic binge-drinking trajectories alcohol per glass, per occasion for fe- exhibited stronger associations with males/males at least weekly) and light/ other substance use75 and with stressful nondrinkers in the maturation of basic Implications for Prevention life events.63 Further, compared with executive functions (e.g., working and Intervention alcohol use that did not meet defini- memory).90 Overall, binge drinking in tions of binge drinking (i.e., less than human adolescents may have relatively To reduce binge drinking, coor- five drinks per occasion), adolescent subtle effects on neuropsychological dinated prevention and intervention binge drinking (five or more drinks per measures at the level of behavioral per- efforts that operate across multi- occasion) was associated with adverse formance; given relatively short drink- ple levels (e.g., individual, family, outcomes, such as lower academic ing histories among youth, differences community, and national policy), as performance, greater likelihood of between young binge drinkers and well as continue across the life span, reporting in the past their healthy counterparts more readily are needed.1,21 Such prevention ef- month, and other substance use.58 In are observed at the level of brain struc- forts should be timed to begin by late sum, a pattern of relatively frequent ture and functioning.86 Importantly, childhood and should be tailored to and chronic binge drinking during research suggests that after controlling address risks most salient to specific adolescence, compared to nonbinge for overall quantity of alcohol con- developmental periods and individual trajectories, was associated with worse sumed, a binge pattern (i.e., consum- circumstances. For example, gender young-adult outcomes across multiple ing five or more drinks per occasion vs. differences in risk factors for under- domains, including risk for substance consuming fewer than five drinks per age drinking44,70 suggest the potential use disorder. occasion), in particular, was associated utility of gender-specific interventions. with adverse effects on brain function- Increasingly, developmental neurosci- ing in young adults.91 ence provides the basis for novel pre- Neurocognitive Consequences Because most of the existing vention and intervention approaches of Adolescent Binge Drinking studies on binge drinking and that strengthen the social-emotional neurocognition in human adolescents and decision-making skills needed to In the context of the ongoing brain have been cross-sectional, the extent refrain from binge drinking, such as maturation that occurs in adolescence to which the findings reflect pre- emotion regulation or resisting peer and young adulthood,77,78 binge existing characteristics or persistent pressure to engage in risky behav- drinking could result in potentially (vs. possibly transient) consequences ior.95,96 Additional interventions for long-lasting neural alterations. For ex- of heavy or binge alcohol use are youth are needed that address alcohol’s ample, in rodent models, a binge pat- unclear. However, emerging research strongly perceived positive effects. One tern of alcohol exposure in adolescence suggests that aberrations in the approach may be to support alternative has been associated with disrupted hip- brain circuitry underlying decision- socially based rewarding and healthy pocampal functioning.79 Further, ani- making may not only signal risk activities, because experiencing adverse mal models indicate that binge alcohol for binge drinking in adolescence alcohol-related consequences may exposure during adolescence can have prior to heavy drinking92 but also not reduce binge drinking in young downstream effects on cognition and may be adversely affected by binge populations.12 behavior through epigenetic mecha- drinking in adolescence and young Ideally, prevention should include nisms.80,81 The specific effects of binge adulthood.93 The reversibility of the routine alcohol screening and brief drinking during adolescence on the effects of adolescent binge drinking on intervention for all youth, as well as brain and neurocognition may depend brain structure and functioning with supportive guidance for parents and on the timing, dose, and chronicity of sustained abstinence warrants study, caregivers.97,98 Community-based alcohol exposure.38,82 particularly because brain maturation prevention and intervention pro- Similar to animal research, in studies continues into young adulthood.78 grams have shown effects in reducing of human adolescents, heavy drinking Large ongoing multisite studies, underage drinking.99 School-based has been associated with deficits in such as the National Consortium on programs100 and easy access to a con- neuropsychological functioning83,84 Alcohol and Neurodevelopment in tinuum of services4 are other examples

12 | Vol. 39, No. 1 Alcohol Research: Current Reviews of community-level supports for youth Acknowledgments https://pubs.niaaa.nih.gov/publications/Newsletter/ winter2004/Newsletter_Number3.pdf. Accessed and families. At the level of public July 28, 2017. policy, strong alcohol policy environ- This work was supported by NIAAA 101 and other National Institutes of 9. Fillmore MT. Acute alcohol-induced impairment ments and enhanced enforcement of cognitive functions: Past and present findings. 102 of local alcohol regulatory policies, Health (NIH) grants: Int J Disabil Hum Dev. 2011;6(2):115-126. such as the minimum legal drinking R01-DA-012237 (Dr. Chung), T32-AA-007453 (Dr. Bachrach), 10. Dawson DA, Grant BF, Li TK. Quantifying the risks age and social-hosting laws, have de- associated with exceeding recommended drinking terred underage drinking.4 R01-AA-016482 and limits. Alcohol Clin Exp Res. 2005;29(5):902-908. U01-AA-021690 (Dr. Clark), PMID: 15897737. R01-AA-021721 and K24-AA-020840 11. Donovan JE. Estimated blood alcohol concentrations Conclusions (Dr. Martin), and L30-AA-022509 for child and adolescent drinking and their (Dr. Creswell). implications for screening instruments. Pediatrics. Adolescence is a critical period of 2009;123(6):e975-e981. PMID: 19482748. risk for binge drinking. An adoles- 12. Patrick ME. A call for research on high-intensity Financial Disclosure alcohol use. Alcohol Clin Exp Res. 2016;40(2):256- cent-specific sensitivity to alcohol’s 259. PMID: 26842244. effects may interact with a normative The authors declare that they have 13. Patrick ME, Schulenberg JE, Martz ME, et al. Extreme propensity for greater risk-taking be- no competing financial interests. binge drinking among 12th-grade students in the havior and peer social environment in United States: Prevalence and predictors. JAMA contributing to risk for binge drinking Pediatr. 2013;167(11):1019-1025. PMID: 24042318. during this developmental period. 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SAGE Open. 2012;2(3):1-8. oxfordhb/9780199735662.013.007. reducing-underage-drinking-a-collective- doi:10.1177/2158244012459742. responsibility. Accessed July 28, 2017. 38. Spear LP. Alcohol consumption in adolescence: A 28. SAMHSA, Center for Behavioral Health Statistics and translational perspective. Curr Addict Rep. 2016;3:50- 53. Donovan JE, Molina BS. Types of alcohol use experience from childhood through adolescence. Quality. Results from the 2015 National Survey on 61. doi:10.1007/s40429-016-0088-9. J Adolesc Health. 2013;53(4):453-459. PMID: Drug Use and Health: Detailed Tables. Rockville, MD: 39. Miranda R Jr, Monti PM, Ray L, et al. Characterizing 23763961. U.S. Department of Health and Human Services; subjective responses to alcohol among 2016. https://www.samhsa.gov/data/sites/default/ adolescent problem drinkers. J Abnorm Psychol. 54. SAMHSA. Binge Drinking: Terminology and Patterns files/NSDUH-DetTabs-2015/NSDUH-DetTabs-2015/ 2014;123(1):117-129. PMID: 24661164. of Use. 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Alcohol Clin in 36 European Countries. Stockholm, Sweden: The and positive and negative alcohol-related Exp Res. 2013;37(2):308-314. PMID: 23240610. Swedish Council for Information on Alcohol and consequences. Addict Behav. 2016;58:110-116. Other Drugs; May 2012. http://www.espad.org/ PMID: 26922158. 56. Morean ME, Kong G, Camenga DR, et al. First drink to sites/espad.org/files/The_2011_ESPAD_Report_ first drunk: Age of onset and delay to intoxication are 42. Schriber RA, Guyer AE. Adolescent neurobiological FULL_2012_10_29.pdf. Accessed July 28, 2017. associated with adolescent alcohol use and binge susceptibility to social context. Dev Cogn Neurosci. drinking. Alcohol Clin Exp Res. 2014;38(10):2615- 31. White V, Bariola E. Australian Secondary Students’ 2016;19:1-18. PMID: 26773514. 2621. PMID: 25257574. Use of , Alcohol and Over-the-Counter and 43. Steinberg L. A social neuroscience perspective on Illicit Substances in 2011. Victoria, : Centre 57. Chassin L, Pitts SC, Prost J. 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Psychol Addict Behav. 2001;15(4):341-349. national comparison of adolescent drinking and 45. Friese B, Grube JW, Moore RS. Youth acquisition of PMID: 11767267. alcohol and drinking contexts: An in-depth look. J use in the United States, Canada, and the 59. Hill KG, White HR, Chung IJ, et al. Early adult Drug Educ. 2013;43(4):385-403. PMID: 25445811. Netherlands. Int J . 2010;21(1):64-69. outcomes of adolescent binge drinking: Person- PMID: 19303761. 46. Mayer RR, Forster JL, Murray DM, et al. Social settings and variable-centered analyses of binge drinking trajectories. 2000;24(6):892- 33. Johnston LD, O’Malley PM, Miech RA, et al. and situations of underage drinking. J Stud Alcohol. Alcohol Clin Exp Res. 1998;59(2):207-215. PMID: 9500308. 901. PMID: 10888080. Demographic Subgroup Trends Among Adolescents in the Use of Various Licit and Illicit Drugs, 1975–2014. 47. Hong T, Beaudoin CE, Johnson C. A panel study of 60. Martino SC, Ellickson PL, McCaffrey DF. 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Clark TT, Yang C, McClernon FJ, et al. Racial in Adolescence (NCANDA): A multisite study of 80. Guerri C, Pascual M. Mechanisms involved in the differences in parenting style typologies and heavy adolescent development and substance use. J neurotoxic, cognitive, and neurobehavioral effects of episodic drinking trajectories. Health Psychol. Stud Alcohol Drugs. 2015;76(6):895-908. PMID: alcohol consumption during adolescence. Alcohol. 2015;34(7):697-708. PMID: 25222086. 26562597. 2010;44(1):15-26. PMID: 20113871. 67. Hahm HC, Kolaczyk E, Jang J, et al. Binge drinking 95. Conrod P, Nikolaou K. Annual research review: 81. Pandey SC, Sakharkar AJ, Tang L, et al. Potential role On the developmental neuropsychology of trajectories from adolescence to young adulthood: of adolescent alcohol exposure-induced amygdaloid substance use disorders. J Child Psychol Psychiatry. The effects of peer social network. Subst Use Misuse. histone modifications in anxiety and alcohol intake 2016;57(3):371-394. PMID: 26889898. 2012;47(6):745-756. PMID: 22452735. during adulthood. Neurobiol Dis. 2015;82:607-619. 68. Leung RK, Toumbourou JW, Hemphill SA. The PMID: 25814047. 96. Riggs NR. Translating developmental neuroscience to substance use prevention. Curr Addict Rep. effect of peer influence and selection processes 82. Spear LP. Adolescent alcohol exposure: Are there 2015;2(2):114-121. PMID: 26236576. on adolescent alcohol use: A systematic review separable vulnerable periods within adolescence? of longitudinal studies. Health Psychol Rev. Physiol Behav. 2015;148:122-130. PMID: 25624108. 97. NIAAA. Alcohol Screening and for 2014;8(4):426-457. PMID: 25211209. . Rockville, MD: NIAAA, U.S. 83. Jacobus J, Tapert SF. Neurotoxic effects of alcohol in Youth: A Practitioner’s Guide Department of Health and Human Services; 2011. 69. Mundt M. Social network analysis of peer effects on adolescence. Ann Rev Clin Psychol. 2013;9:703-721. binge drinking among U.S. adolescents. In: Greenberg PMID: 23245341. https://pubs.niaaa.nih.gov/publications/Practitioner/ A, Kennedy W, Bos N, eds. Social Computing, YouthGuide/YouthGuide.pdf. Accessed July 28, 2017. 84. Lisdahl KM, Gilbart ER, Wright NE, et al. Dare to delay? Behavioral-Cultural Modeling and Prediction. Berlin, The impacts of adolescent alcohol and marijuana 98. Patton R, Deluca P, Kaner E, et al. Alcohol screening Germany: Springer; 2013:123-134. use onset on cognition, brain structure, and function. and brief intervention for adolescents: The how, 70. Hammerslag LR, Gulley JM. Sex differences in Front Psychiatry. 2013;4:53. PMID: 23847550. what and where of reducing alcohol consumption behavior and neural development and their role in and related harm among young people. Alcohol. 85. Feldstein Ewing SW, Sakhardande A, Blakemore SJ. adolescent vulnerability to substance use. Behav 2014;49(2):207-212. PMID: 24232178. The effect of alcohol consumption on the adolescent Brain Res. 2016;298(pt A):15-26. PMID: 25882721. brain: A systematic review of MRI and fMRI studies of 99. Saltz RF, Grube JW, Treno AJ. Lessons from 71. Shih RA, Mullins L, Ewing BA, et al. Associations alcohol-using youth. Neuroimage Clin. 2014;5:420- comprehensive environmental community prevention between neighborhood alcohol availability and 437. PMID: 26958467. trials. In: Scheier LM, ed. Handbook of Adolescent Drug Use Prevention: Research, Intervention young adolescent alcohol use. Psychol Addict Behav. 86. Hermens DF, Lagopoulos J, Tobias-Webb J, et al. Strategies, and Practice. Washington, DC: American 2015;29(4):950-959. PMID: 26415057. Pathways to alcohol-induced brain impairment in Psychological Association; 2015:313-328. 72. Lo CC, Weber J, Cheng TC. A spatial analysis of young people: A review. Cortex. 2013;49(1):3-17. student binge drinking, alcohol-outlet density, and PMID: 22789780. 100. Foxcroft DR, Tsertsvadze A. Universal alcohol misuse social disadvantages. Am J Addict. 2013;22(4):391- 87. 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Alcohol Research: Current Reviews Editorial Staff

The number of drinks a person con- sumers follow low-risk drinking trations listed above are typical, there sumes and the rate at which he or guidelines. is considerable variability in alcohol she consumes them influence how content within and across beverage much alcohol enters the brain and type (e.g., beer, , and distilled how impaired that person becomes. What Is a Standard Drink? spirits). For example, some light Many people are surprised to learn contain half as much alcohol what counts as a drink. The amount In the United States, a standard as a regular beer, while some craft of liquid in one’s glass, can, or bottle drink is defined as a drink with and specialty beers contain twice as does not necessarily match up to 14 grams (0.6 fluid ounces) of pure much. Similarly, the alcohol content how much alcohol is in the drink. alcohol. This is found in: in can vary from 5% to 15%.1 To facilitate research and clinical • 12 ounces of regular beer, which care and to help individuals make is usually about 5% alcohol informed choices about how much Moderate Alcohol alcohol they are consuming, public • 5 ounces of wine, which is Consumption health agencies in the United States typically about 12% alcohol have established a definition of a According to the Dietary Guidelines standard drink, as well as definitions • 1.5 ounces of distilled spirits, for Americans, which are intended of various alcohol consumption pat- which is about 40% alcohol to help individuals improve and terns. These definitions facilitate Although the standard drink maintain overall health and reduce objective assessments of how much a amounts are helpful for following chronic disease risk, moderate drink- person is drinking, enable compari- health guidelines, they may not ing is defined as up to 1 drink per sons of alcohol consumption within reflect customary serving sizes. In day for women and up to 2 drinks and across studies, and help con- addition, while the alcohol concen- per day for men.2

What Is a Standard Drink?

12 fl oz of 8–9 fl oz of 5 fl oz of 1.5 fl oz shot of regular beer malt liquor table wine distilled spirits (shown in a (gin, rum, tequila, 12 oz glass) vodka, whiskey, etc.)

about 5% about 7% about 12% about 40% alcohol alcohol alcohol alcohol

Each beverage portrayed above represents one standard drink of “pure” alcohol, defined in the United States as 0.6 fl oz or 14 grams. The percentage of pure alcohol, expressed here as alcohol by volume (alc/vol), varies within and across beverage types. Although the standard drink amounts are helpful for following health guidelines, they may not reflect customary serving sizes.

Drinking Patterns and Their Definitions | 17 Drinking Patterns and Their Definitions(continued)

Low-Risk Drinking and Though definitions vary, some stud- • Individuals taking medications Alcohol Use Disorder (AUD) ies define extreme binge drinking as that interact with alcohol 2 or more times the gender-specific • People driving vehicles or oper- As defined by the National Institute binge drinking thresholds (i.e., 10 or ating machinery (or who plan to on Alcohol Abuse and Alcoholism more standard drinks for men, and do so shortly after drinking) (NIAAA), for women, low-risk 8 or more for women).5 Other stud- drinking is no more than 3 drinks ies use a higher threshold that may6 on any single day and no more than or may not7 be gender specific. 7 drinks per week. For men, it is References defined as no more than 4 drinks on 1. What is a standard drink? National Institute on any single day and no more than 14 Heavy Drinking Alcohol Abuse and Alcoholism (NIAAA) Alcohol & drinks per week. NIAAA research Your Health website. https://www.niaaa.nih.gov/ shows that only about 2 in 100 peo- SAMHSA defines heavy drinking as alcohol-health/overview-alcohol-consumption/ ple who drink within these limits binge drinking on each of 5 or more what-standard-drink. Accessed July 14, 2017. 4 meet the criteria for AUD. Even days in the past 30 days. 2. Dietary Guidelines for Americans 2015–2020. 8th within these limits, people can have ed. Washington, DC: U.S. Department of Health problems if they drink too quickly and Human Services and U.S. Department of or if they have other health issues.3 International Drink Definitions Agriculture; December 2015. http://health.gov/ dietaryguidelines/2015/guidelines. Accessed Standard-drink definitions vary July 14, 2017. Binge Drinking widely across countries, from 8 3. Drinking levels defined. NIAAA Alcohol &Your grams of alcohol in Iceland and the Health website. https://www.niaaa.nih.gov/ NIAAA defines binge drinking as a to 20 grams in alcohol-health/overview-alcohol-consumption/ moderate-binge-drinking. Accessed July 14, 2017. pattern of drinking that brings Austria. To assess the prevalence of blood alcohol concentration to high-risk drinking globally, the 4. Substance Abuse and Mental Health Services 0.08 grams per deciliter (0.08%) or World Health Organization uses a Administration, Center for Behavioral Health Statistics and Quality. Key Substance Use and higher. This typically occurs after a measure called heavy episodic drink- Mental Health Indicators in the United States: woman consumes 4 drinks or a man ing, defined as consuming 60 grams Results from the 2015 National Survey on Drug consumes 5 drinks in a 2-hour of alcohol or more on at least one Use and Health. Rockville, MD: U.S. Department of time frame.3 occasion in the past 30 days. In the Health and Human Services. https://www.samhsa. The Substance Abuse and Mental United States, where a standard gov/data/sites/default/files/NSDUH-FFR1-2015/ Health Services Administration NSDUH-FFR1-2015/NSDUH-FFR1-2015.pdf. drink equals 14 grams, that would Accessed July 14, 2017. (SAMHSA), which conducts the be 4.25 standard drinks. In China, annual National Survey on Drug France, Ireland, and Spain, where a 5. Patrick ME, Cronce JM, Fairlie AM, et al. Day-to-day variations in high-intensity drinking, expectancies, Use and Health (NSDUH), defines standard drink equals 10 grams, binge drinking as 4 or more drinks and positive and negative alcohol-related 6 drinks on a single occasion would consequences. Addict Behav. 2016;58:110-116. for a woman or 5 or more drinks for constitute heavy episodic drinking. PMID: 26922158. a man on the same occasion on at Because of the risks of drinking, least 1 day in the past 30 days.4 6. Patrick ME, Terry-McElrath YM. High-intensity certain people should avoid alcohol drinking by underage young adults in the United completely: States. Addiction. 2017;112(1):82-93. PMID: 27514864. Extreme Binge Drinking • Individuals under the minimum of 21 7. Johnston LD, O’Malley PM, Miech RA, et al. Moni- Extreme binge drinking, also known toring the Future National Survey Results on Drug as high-intensity drinking, refers to • Women who are pregnant or try- Use, 1975–2015: 2015 Overview, Key Findings ing to become pregnant on Adolescent Drug Use. Ann Arbor, MI: Institute drinking at levels far beyond the for Social Research, University of Michigan; 2016. binge threshold, resulting in high • People who have a medical con- http://monitoringthefuture.org/pubs/monographs/ peak blood alcohol concentrations. dition that alcohol can aggravate mtf-overview2015.pdf. Accessed July 14, 2017.

18 | Vol. 39, No. 1 Alcohol Research: Current Reviews Surveys That Include Information Relevant to Binge Drinking

Alcohol Research: Current Reviews Editorial Staff

This table provides a brief overview of selected surveys administered in the United States and internationally that collect information that can be used to study binge drinking. This list reflects relevant surveys referenced in this issue of Alcohol Research: Current Reviews. It is not a comprehensive compilation of all of the surveys relevant to this topic.

Select U.S. Surveys Survey Name and Population Surveyed Binge Drinking Measure* and Notes Frequency Definition of a Drink • Behavioral Risk Civilian • Binge drinking is measured as The survey was first administered in 15 states. Factor Surveillance noninstitutionalized 5+ drinks for males or 4+ drinks for It became a nationwide surveillance system in System (BRFSS) adults ages 18 and females on an occasion in the past 1993 and is now administered in all 50 states, • Every year since older 30 days. the District of Columbia, and 5 U.S. territories. 1984 • One drink is equivalent to a 12-ounce Since 2011, this survey has included adult beer, a 5-ounce glass of wine, or a students living in college housing. drink with one shot of liquor. https://www.cdc.gov/brfss

• Core Alcohol and College students • Binge drinking is measured for males http://core.siu.edu/results/index.php Drug Survey and females as 5+ drinks in one • Every year from sitting in the past 2 weeks. 2006 to 2013 • A drink is defined as a bottle of beer, a glass of wine, a wine cooler, a shot glass of liquor, or a mixed drink.

• Harvard School 4-year college • Binge drinking is measured as http://archive.sph.harvard.edu/cas/About of Public Health students 5+ drinks for males or 4+ drinks for College Alcohol females once in the past 2 weeks. Study • A drink is defined as a 12-ounce beer, • Conducted four a 4-ounce glass of wine, a 12-ounce times (1993, wine cooler, or a shot of liquor taken 1997, 1999, and straight or in a mixed drink. 2001)

• Health Related Active-duty service • Binge drinking is measured as Most recent report available: https://www. Behaviors Survey and U.S. Coast Guard 5+ drinks for males or 4+ drinks for documentcloud.org/documents/694942-2011- of Active Duty members females on the same occasion in the final-department-of-defense-survey-of.html Military Personnel past 30 days. • About every 3 • A drink is defined as a can or bottle of years since 1980 beer, a glass of wine or a wine cooler, a shot of liquor, or a mixed drink with liquor in it.

*Surveys may not explicitly use the term binge drinking.

Surveys That Include Information Relevant to Binge Drinking | 19 Surveys That Include Information Relevant to Binge Drinking (continued)

Select U.S. Surveys Survey Name and Population Surveyed Binge Drinking Measure* and Notes Frequency Definition of a Drink • Monitoring the 8th, 10th, and 12th • Binge drinking is measured for males This survey began with 12th graders in 1975. Future (MTF) study graders in public and females as 5+ drinks in a row in Since 1991, surveys of 8th and 10th graders • Every year since and private schools, the past 2 weeks. have been conducted annually. Beginning with 1975 college students, and • The definition of a drink varies slightly the class of 1976, a randomly selected sample young adults among survey forms, although a drink from each senior class has received biennial is generally defined as a bottle of follow-up surveys. beer, a glass of wine, a wine cooler, a http://www.monitoringthefuture.org shot glass of liquor, a mixed drink, etc.

• National Civilian • NESARC does not explicitly measure Three NESARC waves have been conducted. Epidemiologic noninstitutionalized binge drinking, although respondents Wave 1 was from 2001 to 2002, Wave 2 was Survey on Alcohol adults ages 18 and are asked about drinking at or above from 2004 to 2005, and NESARC-III was from and Related older levels commonly used to assess 2012 to 2013. Conditions binge drinking. For males ages 65 https://www.niaaa.nih.gov/research/nesarc-iii (NESARC) and younger, the level is 5+ drinks in • Three surveys a single day or in 2 hours or less. For conducted since males ages 65 and older and women, 2001 to 2002 the levels are 4+ drinks in 2 hours or less, 4+ drinks in a single day, and 5+ drinks in a single day. • One standard drink is defined as 0.6 ounces of ethanol.

• National Survey Civilian • Binge drinking is measured as Called the National Household Survey on Drug on Drug Use and noninstitutionalized 5+ drinks for males or 4+ drinks for Abuse (NHSDA) from 1979 to 2001, called Health (NSDUH) population ages 12 females on the same occasion on NSDUH since 2002. and older at least 1 day in the past 30 days. • 1979, 1982, https://www.samhsa.gov/data/population-data- NSDUH defined binge drinking as 1985, 1988, nsduh 1990, and every 5+ drinks for males and females year thereafter until 2015. • A drink is defined as a can or bottle of beer, a glass of wine or a wine cooler, a shot of liquor, or a mixed drink with liquor in it.

• Youth Risk 9th through • Binge drinking is measured as The YRBSS includes national surveys conducted Behavior 12th graders in public 5+ drinks for males or 4+ drinks for by the Centers for Disease Control and Surveillance and private schools in females on a single occasion in the Prevention. It also includes state, territorial, System (YRBSS) the United States past 30 days. Before 2017, YRBSS tribal government, and local surveys conducted • Every 2 years since surveys defined binge drinking for by departments of health and education, which 1993 males and females as 5+ drinks. provide data representative of mostly public • A drink includes beer, wine, wine high school students in each jurisdiction. coolers, and liquor such as rum, gin, https://www.cdc.gov/healthyYouth/data/yrbs/ vodka, or whiskey. index.htm

20 | Vol. 39, No. 1 Alcohol Research: Current Reviews Surveys That Include Information Relevant to Binge Drinking (continued)

Select International Surveys† Survey Name and Population Surveyed Binge Drinking Measure* and Notes Frequency Definition of a Drink • Australian School Students ages 12 to • Risky drinking is defined as drinking https://www.mhc.wa.gov.au/reports-and- Students Alcohol 17 who are in school 4+ standard drinks on any 1 day, resources/reports/australian-school-students- and Drug (ASSAD) years 7 to 12 and if alcohol was consumed in the national-alcohol-and-drug-survey survey are from government, previous week. • Every 3 years since Catholic, and • A standard drink is defined as any 1984 independent schools drink containing 10 grams of alcohol. in the state of Western Australia

• European School European students • Heavy episodic drinking is defined The ESPAD survey notes that its measure of Survey Project on ages 15 to 16 as drinking 5+ alcoholic beverages heavy episodic drinking corresponds to a cutoff Alcohol and Other on one occasion at least once in the of approximately 9 centiliters of pure alcohol. Drugs (ESPAD) past 30 days. http://www.espad.org • Every 4 years since • Nationally relevant examples of a 1995 drink are included in the surveys.

• Healthy Ireland Adults ages 18 and • Binge drinking is defined as Healthy Ireland is the successor to the Survey of • 1998, 2002, and older from private 6+ standard drinks on one occasion Lifestyle, Attitudes and Nutrition in Ireland. households in the in the past 12 months. 2007 http://www.healthyireland.ie/accessibility/ Republic of Ireland • A standard drink is defined as a half healthy-ireland-survey pint or a glass of beer, lager, or cider; a single measure of spirits; a single glass of wine, sherry, or port; or a bottle of (long neck).

†For a list of additional international surveys relevant to binge drinking, see Gender Differences in Binge Drinking: Prevalence, Predictors, and Consequences in this issue.

Surveys That Include Information Relevant to Binge Drinking | 21 Research Training & Career Development Opportunities by Education Level

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The Epidemiology of Binge Drinking Among College-Age Individuals in the United States

Heather Krieger, Chelsie M. Young, Amber M. Anthenien, and Heather Krieger, M.A., is a Clayton Neighbors graduate student; Chelsie M. Young, Ph.D., is a post-doctoral Rates of alcohol consumption continue to be a concern, particularly for individuals researcher; Amber M. Anthenien, who are college age. Drinking patterns have changed over time, with the frequency M.S., is a graduate student; and of binge drinking (consuming four/five or more drinks for women/men) remaining Clayton Neighbors, Ph.D., is a high (30% to 40%). Young adults in the college age range are developmentally and socially at higher risk for drinking at binge levels. Changes in autonomy, parental professor, all in the Department control, norms, and attitudes affect binge drinking behaviors. This article reviews of Psychology, University of those changes, as well as the individual and environmental factors that increase or Houston, Houston, Texas. decrease the risk of participating in binge drinking behaviors. Risk factors include risky drinking events (e.g., 21st birthdays), other substance use, and drinking to cope, while protective factors include religious beliefs, low normative perceptions of drink- ing, and use of protective behavioral strategies. Additionally, this article discusses the physical, social, emotional, and cognitive consequences of consuming alcohol at binge levels. Alcohol policies and prevention and intervention techniques need to incorporate these factors to reduce experiences of alcohol-related problems. Tar- geting policy changes and prevention and intervention efforts toward young adults may increase effectiveness and prevent both short- and long-term consequences of binge drinking.

Key words: Alcohol consumption; binge drinking; consequences; risk and protective factors; young adults

Binge drinking, particularly among ity of the literature regarding binge tion of consumption. When individu- college-age individuals, has been a sig- drinking focuses specifically on college als who met these binge drinking cri- nificant topic of research for more students. Further, there is variability in teria had consumed the alcohol over a than 20 years because of associations the definition of college students. long period of time, they did not reach between greater quantity and fre- Some studies sampled only full-time BACs higher than .08%.2,3 quency of alcohol consumption and students from four-year institutions, In 2004, the National Institute alcohol-related consequences. To iden- whereas other studies included part- on Alcohol Abuse and Alcoholism tify factors associated with binge time and community college students. (NIAAA) provided a revised definition drinking over time, several large-scale The term “binge drinking” has of binge drinking, acknowledging that studies have assessed trends in binge a somewhat controversial history. consuming 5/4+ drinks in a 2-hour drinking among young adults. This The term was originally defined by time period would result in a BAC article aims to summarize those trends Wechsler and colleagues as five or of at least .08% for most individuals. and the developmental and social fac- more drinks for men, or four or more Although subsequent questions con- tors that impact the likelihood of, the drinks for women (5/4+), on a single tinue to be raised regarding the validity risk and protective factors related to, occasion.1 Criticisms of this conceptu- of defining binge drinking at 5+ or and the negative alcohol-related conse- alization of binge drinking were based 5/4+ on one occasion, these are still quences of binge drinking behaviors. largely on the substantial variability in the most commonly used definitions Some studies examined young adults blood alcohol concentrations (BACs) in the literature. Research covered in who are not in college, but the major- due to differences in weight and dura- this review includes studies on binge

Binge Drinking Among College-Age Individuals | 23 drinking that use the 5/4+ criteria or a also attempted to assess student dents engaged in binge drinking in the BAC of at least .08%. drinking rates. At 120 colleges, the previous 30 days (31.6% of females CAS measured alcohol use among and 49.4% of males) than Hispanic college students at four time points students (22.6% of females and 39.9% Trends in Young Adult between 1993 and 2001.8 The survey of males).12 Also, African American Binge Drinking Rates included more than 14,000 students students (6.1% of males) were less like- and provided the first gender-specific ly to report binge drinking than White Binge drinking among young adults measure of binge drinking (i.e., 5/4+ students (22.8% of males), although has concerned researchers and educa- drinks for males/females). Contrary to this difference was less pronounced tors for decades, prompting multiple findings from the MTF study and the among females. national initiatives to track patterns in Core Alcohol and Drug Survey, the Rates of binge drinking have also binge drinking. The longest continu- CAS found little change between 1993 been assessed in military samples. ous running national survey of drug (43.2%) and 2001 (44.5%) in the Starting in 1980, the U.S. Department and alcohol use among adolescents number of students reporting binge of Defense issued several large-scale, and young adults is the Monitoring drinking in the previous 2 weeks.9 anonymous health surveys (most the Future (MTF) study, which is The most recently initiated nation- recently called the Health Related funded by the National Institute on wide survey of college student alcohol Behaviors Survey) to active-duty Drug Abuse and conducted by the use is the National Epidemiologic military personnel, with the first as- University of Michigan’s Institute Survey on Alcohol and Related sessment of binge drinking appearing for Social Research.4 Approximately Conditions. This survey began the in 1998. Rates of binge drinking for 15,000 high school seniors in 133 first of three waves of data collection military personnel overall increased schools are surveyed each year, and, in 2001, which included data from from 35% in 1998 to 47% in 2008.13 since 1976, a subset of about 2,400 approximately 43,000 individuals.10 The 2008 survey sampled more than have been followed biennially by mail. Prevalence rates, only reported for 28,000 service members and found Survey results indicate that the rate 2001, indicate that 57% of 18- to that young adult military personnel of self-reported college student binge 24-year-olds binge drank in the previ- (ages 18 to 25) had the highest rates of drinking in the previous 2 weeks ous year, and 40% binge drank 12 or frequent binge drinking (once a week dropped from 1980 (44%) to 1993 more times in the previous year. or more) at 26%.14 This is significantly (40%) and continued to decrease College attendance, gender, and higher than the rate for same-age ci- through 2014 (35%). Estimates for ethnic variations in binge drinking vilians (16%), as reported in the 2007 college student engagement in extreme have been identified. A number of NSDUH.15 Rates of binge drinking binge drinking, defined as consuming studies have examined differences in also differ by military branch.14 10 or more drinks on one occasion in alcohol use between college and same- the previous 2 weeks, varied from 14% age noncollege peers, consistently in 2005 to 20% in 2014. finding higher rates of heavy drinking Developmental and Another national survey assessing and alcohol-related problems among Social Factors college student binge drinking is the college students than among noncol- Substance Abuse and Mental Health lege peers.11 The annual prevalence of Developmental and social factors Services Administration’s (SAMHSA) alcohol use reported in the MTF study are important contributors to binge National Survey on Drug Use and suggested small differences between drinking among college-age adults. Health (NSDUH), which includes male and female drinking rates and The college-age years (approximately yearly assessments of 60,000 to 70,000 modest decreases over time.4 However, ages 18 to 24) correspond with the individuals ages 12 and older. Results a declining gender gap exists for binge developmental stage widely referred to indicate that for young adults ages drinking rates, with female binge as “emerging adulthood.”16,17 Dramatic 18 to 25, rates of binge drinking in drinking (i.e., 4+) decreasing from cultural changes in the United States the previous 30 days decreased slight- 31% in 1988 to 26% in 2014, and and other countries with similar so- ly from 44.6% in 1988 to 37.7% male binge drinking (i.e., 5+) decreas- cioeconomic structures have occurred in 2014.5 ing more substantially, from 52% to over time. Arnett notes that post–high The Core Alcohol and Drug Survey 43%. school education rose from 14% in sampled more than 140,000 students Currently, the MTF study does 1940 to more than 60% in the mid- and found a slight decline in the not report racial or ethnic differenc- 1990s.16 College attendance has re- percentage of students who binge es in binge drinking among college sulted in the delay of traditional adult drank in the previous 2 weeks, from students. However, the U.S. Centers responsibilities. Consequently, in re- 45.9% in 2006 to 43.9% in 2013.6,7 for Disease Control and Prevention cent decades this developmental period The College Alcohol Survey (CAS) reported that more White college stu- has become a time when individuals

24 | Vol. 39, No. 1 Alcohol Research: Current Reviews explore new freedoms and experiment changes in alcohol problems, attitudes age is not a strong predictor of norma- with behaviors that were previously regarding heavy drinking, and heavy tive perceptions of drinking. less accessible, including alcohol con- drinking or drug-using peers. The MTF study collected data (for sumption.18,19 Interrelated factors associated with ages 18 to 30) on perceived close- In their seminal paper, “Getting increased heavy drinking and alcohol- friend disapproval of respondents’ Drunk and Growing Up: Trajectories related problems include moving out binge drinking once or twice per of Frequent Binge Drinking During of the parent home, going to college, weekend. Respondents ages 19 to 22 the Transition to Young Adulthood,” and decreased parental involvement, and 23 to 26 reported less disapproval Schulenberg and colleagues identified each of which has a unique from their friends (54.5% and 52.3%, five distinct trajectories of binge drink- contribution. Moving out of the respectively) relative to respondents ing that occur in young adults ages 18 parent home contributed to the risk of ages 18 (65.6%) and ages 27 to 30 to 24.20 This analysis was one of the increased drinking, but additional risk (57.1%).4 Few studies have directly first to use a national sample to identi- was found for students who lived on examined perceived norms and their fy distinct patterns of changes in binge campus.21 White and colleagues found influence on college versus noncollege drinking over time. The national sam- that living in a college environment young adult binge drinking, but the ple included four consecutive waves contributed to increases in heavy available evidence suggests perceived of data from the MTF study. More drinking more than all the other norms have less influence on noncol- than 90% of the sample was catego- developmental factors they examined.22 lege young adults.31 rized as engaging in no binge drinking Further, although peer influences are Related to social norms, member- during any wave (35.9%). Or, they paramount among college students, ship in specific groups has been associ- were categorized as one of five binge one study found that parental ated with higher rates of binge drink- drinking trajectories: involvement played a protective role ing. Foremost among these are college in reducing the likelihood of problem fraternity or sorority affiliation,32-34 1. Rare (16.7%): binge drinking drinking.23 participation in collegiate athletics,35,36 during at least one wave but no For young adults ages 18 to 24, and being in the military, especially the frequent binge drinking, defined as many of the factors attributed to high U.S. Army or U.S. Marines.14,37,38 two or more binge episodes in the rates of binge drinking are social in past 2 weeks. nature. Perceptions and overestima- 2. Decreasing (11.7%): frequent tions of the prevalence and approval Risk and Protective Factors binge drinking during Wave 1 and of heavy drinking among one’s peers decreasing or no frequent binge have been consistently documented Person-level risk factors. Demo- drinking by Wave 4. and associated with heavier drinking. graphic factors such as age, sex, Reducing normative misperceptions and race have been linked to binge 3. Fling (9.9%): frequent binge drink- has been the most consistently sup- drinking rates among college students. ing during Wave 2 or Wave 3 but ported brief intervention strategy for Individuals who began drinking no binge drinking in Wave 1 or reducing heavy drinking among young before age 16 were found to be more Wave 4. adults. Most studies that successfully likely to binge drink in college.39 An 4. Increasing (9.5%): no frequent used such interventions to reduce per- examination of MTF data found that, binge drinking during Wave 1 in- ceived norms also demonstrated reduc- among recent cohorts, individuals creasing to frequent binge drinking tions in drinking.24-28 entering the 18 to 26 age range by Wave 4. The vast majority of research on reported less binge drinking than previous cohorts, and individuals 5. Chronic (6.7%): frequent binge the influence of social norms on leaving the 18 to 26 age range reported drinking throughout Waves 1, 2, 3, heavy drinking has been done using college samples. Similar results have more binge drinking than previous and 4. been found in the general adult pop- cohorts.40 Several longitudinal studies Most young adults reported binge ulation, with heavy drinkers more found that male college students were drinking during at least one of the four likely to view heavy drinking as nor- more likely than female students to assessment waves, but less than half of mative and to overestimate drinking binge drink.41,42 Also, studies have the sample drank at rates that could norms.29 In a large general population shown that White college students be considered problematic.20 Young study of adults who drank alcohol were more likely to engage in binge adults in the Increasing and Chronic at least monthly (N = 14,009), age drinking than non-White students.39,43 categories were identified as having the was negatively associated with nor- Personality traits and individual most difficulty navigating the transi- mative misperceptions of drinking.30 difference variables have also been tion to adulthood. Identified trajecto- However, the magnitude of the cor- identified as risk factors for binge ries were associated with stability and relation was only .07, suggesting that drinking. A longitudinal investigation

Binge Drinking Among College-Age Individuals | 25 using MTF data from 18- to 24-year- in binge drinking at an earlier age binge drinking have been identified. olds found that individuals lower in during young adulthood.46 Gender is one of these factors. Females self-efficacy had a greater likelihood of In conclusion, several consistent risk tend to drink less than males.62 Also, engaging in binge drinking over time.42 factors for binge drinking have been females and individuals with higher Similarly, another longitudinal study identified, including early onset of grade point averages tend to use among adults ages 18 to 31 found that, alcohol use, being male, identifying as more protective behavioral strategies, across time points, problem drinkers White, having low self-efficacy, scoring such as alternating drinking alcohol scored higher on disinhibition.41 high on disinhibition, scoring high and water.63 Protective behavioral Binge drinking also has been on neuroticism-anxiety (for women), strategies have been shown to reduce positively correlated with neuroticism- being impulsive and sensation-seeking the likelihood of experiencing negative anxiety and impulsive sensation- (especially for men), having higher alcohol-related consequences.62,64 seeking. In particular, one study found scores on antisocial personality disor- Protective contexts and events. that women who engaged in binge der measures, using alcohol to cope Certain cultural climates that promote drinking tended to score higher on or fit in with others, using alcohol for a normative perception of disapproval neuroticism-anxiety, and men who sex-seeking purposes, drinking to get toward excessive drinking can protect engaged in binge drinking were more drunk, exhibiting problem behavior, their adherents against binge drinking. likely to score highly on impulsivity scoring low on , and engag- For example, parental disapproval 44 ing in other substance use. of alcohol use protects against binge and sensation-seeking. Another study 39,61 found that binge drinkers tended to Risky contexts and events. Specific drinking. Many religions disap- be less conscientious and more thrill- events and contexts that promote prove of drinking heavily and promote seeking than those who did not engage heavy drinking are additional factors drinking only in moderation or ban in binge drinking.45 Also, individuals that contribute to high rates of binge drinking among members altogether. who scored higher on measures drinking. Such events include New As such, religion can exert a protective Year’s Eve, St. Patrick’s Day, and influence on college student binge of antisocial personality disorder 47,48 61,65 were more likely to engage in binge Halloween. Some high-risk drink- drinking. Neighborhood norms drinking.46 ing events tend to be more prevalent in against heavy drinking have also young adulthood. For example, home- been found to protect against binge Other studies report that motiva- coming, athletic events, weddings, and drinking.66 tions for drinking and attitudes toward graduations are all relatively common College environments tend to en- drinking can influence the likelihood events for people in this age range and courage heavy drinking; however, of binge drinking. Drinking to cope have been associated with heavy drink- some contextual factors surrounding with negative affect and drinking to fit ing.49,50 In addition, 21st birthdays,51 students can protect against binge in with peers have both been associated 48 52 45 spring break, football tailgating, drinking and negative alcohol-related with binge drinking. Sex-seeking as pregame partying,53-55 and drinking consequences. Drinking in college is a motivation for drinking has been games56,57 have all been associated with often a social activity among friends. associated with binge drinking among 45 excessive drinking among college stu- Close friends who encourage safe college men. Individuals who report- dents. For undergraduates, weekends drinking can help protect against the ed drinking alcohol for the purpose of and the beginning of a semester have negative consequences of excessive getting drunk were also more likely to 67 42 been associated with higher levels of drinking. College drinking that oc- engage in binge drinking. Positive at- drinking.47,49 curs in locations that provide food and titudes toward drinking have also been Social influences, often from close water or that accompanies a meal has associated with an increased likelihood relationships, can contribute to in- been shown to reduce negative alcohol of binge drinking among college creased risk of binge drinking among consequences.68 Additionally, drinking students.39 college students. For example, having that occurs in bars is somewhat regu- Problem behaviors and other sub- parents who are alcoholics, having lated, because bartenders can stop serv- stance use also have been associated friends who drink, and participating in ing individuals who appear drunk.69 with binge drinking. For example, Greek life have all been associated with These specific college drinking contexts one longitudinal study found that, a greater likelihood of binge drink- allow for use of protective behavioral across ages 18 to 31, heavy drinkers ing.46,58-60 Also, peer drinking and use strategies, such as eating food, drinking were more likely to exhibit problem of cigarettes and marijuana have been water, limiting the number of drinks behavior.41 A longitudinal examination associated with an increased likelihood consumed, and drinking with close of trajectories of binge drinking found of binge drinking.61 friends.62 that adolescents who reported using Person-level protective factors. Other factors specific to certain col- drugs and scored low on measures of Several protective factors associated leges have been associated with lower depression were more likely to engage with a lower likelihood of engaging in rates of binge drinking. For instance,

26 | Vol. 39, No. 1 Alcohol Research: Current Reviews college students who attended schools Consequences of lowing a binge drinking episode than with higher social capital (defined as Binge Drinking a nonbinge episode.1 Few longitudinal the average time students spent vol- studies have examined associations unteering) were less likely to engage Overall, binge drinking and frequent between emotions and binge drinking; in binge drinking.70 Furthermore, binge drinking have been consistently, however, frequent binge drinking in research has suggested that attending significantly, and positively associated young adulthood has been found to commuter schools, all-female colleges, with alcohol-related problems.78,79 increase risk for depression 5 years and Protestant religious colleges is These problems impact multiple later.88 associated with lower rates of binge aspects of life for young adults and Social outcomes related to binge drinking.39 the people around them and include drinking often involve negative Certain social roles and their inher- physical, legal, emotional, social, and interpersonal interactions and failure ent responsibilities can lead to lower cognitive consequences, as well as an to meet relational obligations. When likelihood of binge drinking. For increased likelihood of having an alco- compared to infrequent and non– example, studies have found that co- hol use disorder. binge drinkers, frequent binge drinkers habitation, getting married, and hav- Physical and legal outcomes. Binge are twice as likely to experience drinking is associated with significant interpersonal consequences, including ing children all protect against heavy 1 drinking.71-75 increased risk for experiencing con- arguing with friends, experiencing sequences, including physical harm, strain on relationships,89 and getting Alcohol-related laws and policies 38 and their connections to the likelihood legal problems, and failure to meet role into physical fights. Binge drinkers of binge drinking have been examined. obligations (e.g., work responsibilities). in college were two to three times as Plunk, Cavazos-Rehg, Bierut, and Active-duty military personnel who likely to miss class and twice as likely binge drink are about five times as to perform poorly or get behind on Grucza found that more permissive 1,80 laws regarding the minimum legal likely to report drinking and driving schoolwork. Among active-duty or riding with someone who has been military personnel, frequent binge drinking age were associated with 38 more binge drinking.76 Using MTF drinking. College students who binge drinking was associated with failure to data collected from 1976 to 2011 drank in the previous year were more be promoted and substandard work performance.38 from high school seniors who were than twice as likely to be taken advan- tage of sexually or have unplanned sex, Cognitive outcomes. Binge drink- followed up to age 26, Jager, Keyes, and they were four times as likely to be ing results in high concentrations and Schulenberg found that laws dic- physically injured.80 Additionally, indi- of alcohol entering the bloodstream tating the minimum legal drinking age viduals who engaged in frequent binge quickly, which can affect cognitive were associated with decreases in binge drinking reported experiencing more processing. One of the most prevalent drinking for 18-year-olds, but those sick days and having poorer overall cognitive effects of binge drinking laws were associated with increases in physical and mental health than non– is blacking out, a failure to encode binge drinking rates across all male 81 40 binge drinkers. Binge drinkers also memories. Frequent binge drinkers participants ages 18 to 22. Another reported having greater sleep prob- are twice as likely as infrequent binge study found that lower age require- lems, including having more trouble drinkers to experience blackouts.1 ments for purchasing and consuming falling asleep and staying asleep than Several studies reported that the con- alcohol were associated with more those who did not binge drink.82 Binge sumption of alcohol at binge levels was hazardous and problematic drinking. drinking also increases an individual’s associated with poor performance on These findings have clear implications likelihood of driving after drinking.80,83 cognitive tasks, such as recall, spatial 76 for alcohol policy. Emotional and social outcomes. recognition, search, and planning Another study investigated whether Binge drinking has been associated tasks.86,90-92 Also, gender differences in personal endorsement of alcohol poli- with a variety of negative emotional cognitive function have been noted, cies was associated with college student and social outcomes. For exam- with women being more susceptible to drinking. The authors found that col- ple, binge drinkers tended to score the negative cognitive effects of binge lege students who personally endorsed higher on measures of depression drinking.87,93 the alcohol laws and policies were and anxiety84-86 and reported lower Research suggests that binge significantly less likely to binge drink.77 positive mood than nondrinkers.86,87 drinking affects the and Thus, laws that set a minimum drink- Furthermore, students who binge , and that repeated ing age or a low BAC level for drivers, drank in the previous year were more binge drinking can damage these brain and personal endorsements of college than twice as likely to report having structures.94 One study reported that alcohol policies, can serve as protective serious thoughts of .80 Another extreme binge drinkers (those who contextual factors against college stu- study reported that feelings of remorse consumed 10 or more drinks per occa- dent binge drinking. after drinking were more common fol- sion) displayed

Binge Drinking Among College-Age Individuals | 27 (EEG) spectral patterns similar to the consuming alcohol at binge levels. Core-Executive-Summary-Report-2014.pdf. Accessed patterns displayed in individuals with This review summarized individual July 20, 2017. alcohol use disorder, suggesting that and environmental factors associated 8. Wechsler H, Dowdall GW, Maenner G, et al. Changes extreme binge drinking can alter the with increased or decreased risk for in binge drinking and related problems among 95 American college students between 1993 and brain negatively and permanently. binge drinking. Understanding these 1997: Results of the Harvard School of Public Examination of the effects of binge factors is important in guiding future Health College Alcohol Study. J Am Coll Health. drinking on cognitive structures and prevention and intervention efforts 1998;47(2):57-68. PMID: 9782661. on performance in young adults con- and in shaping alcohol policies. 9. 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Core Alcohol and Drug Survey 19. Schulenberg JE, Maggs JL. A developmental over time. Despite this trend, rates Long Form—Form 194: Executive Summary. perspective on alcohol use and heavy drinking 2010. http://core.siu.edu/_common/documents/ during adolescence and the transition to young still remain high, with 30% to 40% report0608.pdf. Accessed July 11, 2017. adulthood. J Stud Alcohol. 2002;14(suppl):54-70. of young adults reporting binge PMID: 12022730. 7. Core Institute. Core Alcohol and Drug Survey Long drinking at least once in the previous Form—Form 194: Executive Summary. Carbondale, IL: 20. Schulenberg J, O’Malley PM, Bachman JG, et month. Developmentally and socially, Southern Illinois University Carbondale/Core Institute; al. Getting drunk and growing up: Trajectories of this age range is at higher risk for 2014. https://www.eou.edu/health/files/2016/09/ frequent binge drinking during the transition to young

28 | Vol. 39, No. 1 Alcohol Research: Current Reviews adulthood. J Stud Alcohol. 1996;57(3):289-304. 35. Leichliter JS, Meilman PW, Presley CA, et al. Alcohol college students. J Stud Alcohol. 2006;67(6):911- PMID: 8709588. use and related consequences among students with 916. PMID: 17061009. varying levels of involvement in college athletics. 21. Merrill JE, Carey KB. Drinking over the lifespan: Focus 49. Del Boca FK, Darkes J, Greenbaum PE, et al. Up close J Am Coll Health. 1998;46(6):257-262. PMID: on college ages. Alcohol Res. 2016;38(1):103-114. and personal: Temporal variability in the drinking of 9609972. PMID: 27159817. individual college students during their first year. 36. Martens MP, Dams-O’Connor K, Beck NC. A systematic J Consult Clin Psychol. 2004;72(2):155. PMID: 22. White HR, McMorris BJ, Catalano RF, et al. Increases review of college student-athlete drinking: Prevalence 15065951. in alcohol and marijuana use during the transition rates, sport-related factors, and interventions. J Subst out of high school into emerging adulthood: The 50. Neighbors C, Atkins DC, Lewis MA, et al. Event-specific Abuse Treat. 2006;31(3):305-316. PMID: 16996393. effects of leaving home, going to college, and drinking among college students. Psychol Addict high school protective factors. J Stud Alcohol. 37. Mattiko MJ, Olmsted KLR, Brown JM, et al. Alcohol Behav. 2011; 25(4):702. PMID: 21639597. 2006;67(6):810-822. PMID: 17060997. use and negative consequences among active duty 51. Rutledge PC, Park A, Sher KJ. 21st birthday military personnel. Addict Behav. 2011;36(6):608- 23. Abar C, Turrisi R. How important are parents during the drinking: Extremely extreme. J Consult Clin Psychol. 614. PMID: 21376475. college years? A longitudinal perspective of indirect 2008;76(3):511. PMID: 18540744. 38. Stahre MA, Brewer RD, Fonseca VP, et al. Binge influences parents yield on their college teens’ 52. Neal DJ, Fromme K. Hook’em horns and heavy alcohol use. 2008;33(10):1360-1368. drinking among U.S. active-duty military personnel. Addict Behav. drinking: Alcohol use and collegiate sports. Addict PMID: 18635318. Am J Prevent Med. 2009;36(3):208-217. PMID: Behav. 2007;32(11):2681-2693. PMID: 17662537. 19215846. 24. Borsari B, Carey KB. Peer influences on college 53. Pedersen ER, LaBrie JW. Normative misperceptions 39. Weitzman ER, Nelson TF, Wechsler H. Taking up drinking: A review of the research. J Subst Abuse. of drinking among college students: A look at the binge drinking in college: The influences of person, 2001;13(4):391-424. PMID: 11775073. specific contexts of prepartying and drinking games. social group, and environment. J Adolesc Health. J Stud Alcohol Drugs. 2008;69(3):406. PMID: 25. Borsari B, Carey KB. Descriptive and injunctive norms 2003;32(1):26-35. PMID: 12507798. in college drinking: A meta-analytic integration. J Stud 18432383. 40. Jager J, Keyes KM, Schulenberg JE. Historical Alcohol. 2003;64(3):331. PMID: 12817821. 54. Read JP, Merrill JE, Bytschkow K. Before the party variation in young adult binge drinking trajectories starts: Risk factors and reasons for “” in 26. Miller MB, Leffingwell T, Claborn K, et al. Personalized and its link to historical variation in social roles college students. J Am Coll Health. 2010;58(5):461- feedback interventions for college alcohol misuse: and minimum legal drinking age. Dev Psychol. 472. PMID: 20304758. An update of Walters and Neighbors (2005). Psychol 2015;51(7):962-974. PMID: 26010381. Addict Behav. 2013;27(4):909. PMID: 23276309. 55. Zamboanga BL, Casner HG, Olthuis JV, et al. Knowing 41. Bennett ME, McCrady BS, Johnson V, et al. Problem where they’re going: Destination‐specific pregaming 27. Neighbors C, Lee CM, Lewis MA, et al. Are social drinking from young adulthood to adulthood: behaviors in a multiethnic sample of college norms the best predictor of outcomes among heavy- Patterns, predictors and outcomes. J Stud Alcohol. students. J Clin Psychol. 2013;69(4):383-396. drinking college students? J Stud Alcohol Drugs. 1999;60(5):605-614. PMID: 10487729. 2007;68(4):556. PMID: 17568961. PMID: 23044716. 42. Schulenberg J, Wadsworth KN, O’Malley PM, et al. 56. Borsari B. Drinking games in the college environment: 28. Reid AE, Carey KB. Interventions to reduce college Adolescent risk factors for binge drinking during A review. J Alcohol Drug Educ. 2004;48(2):29. student drinking: State of the evidence for the transition to young adulthood: Variable- and mechanisms of behavior change. Clin Psychol Rev. pattern-centered approaches to change. Dev 57. Zamboanga BL, Olthuis, JV, Kenney SR, et al. Not just 2015;40:213-224. PMID: 26164065. Psychol. 1996;32(4):659-674. doi:10.1037/0012- fun and games: A review of college drinking games 29. Wild TC. Personal drinking and sociocultural drinking 1649.32.4.659. research from 2004 to 2013. Psychol Addict Behav. 2014;28(3):682. PMID: 25222171. norms: A representative population study. J Stud 43. Wade J, Peralta RL. Perceived racial discrimination, Alcohol. 2002;63(4):469-475. PMID: 12160106. heavy episodic drinking, and alcohol abstinence 58. Chauvin CD. Social norms and motivations 30. Cunningham JA, Neighbors C, Wild TC, et al. among African American and White college students. associated with college binge drinking. Sociol Normative misperceptions about alcohol use in a J Ethn Subst Abuse. March 2016:1-16. PMID: Inq. 2012;82(2):257-281. doi:10.1111/ general population sample of problem drinkers from 26979299. j.1475682X.2011.00400.x. a large metropolitan city. Alcohol. 2012;47(1):63-66. 44. Adan A, Navarro JF, Forero DA. Personality profile of 59. Park A, Sher KJ, Krull JL. Risky drinking in college PMID: 22028458. binge drinking in university students is modulated by changes as fraternity/sorority affiliation changes: 31. Quinn PD, Fromme K. Event-level associations sex. A study using the Alternative Five Factor Model. A person-environment perspective. Psychol Addict between objective and subjective Drug Alcohol Depend. 2016;165:120-125. PMID: Behav. 2008;22(2):219-229. PMID: 18540719. 27262897. and driving after drinking across the college years. 60. Wechsler H, Kuh G, Davenport AE. Fraternities, Psychol Addict Behav. 2012;26(3):384. PMID: 45. Ichiyama MA, Kruse MI. The social contexts of binge sororities and binge drinking: Results from a 21688876. drinking among private university freshmen. J Alcohol national study of American colleges. NASPA J. . 1998;44(1):18-33. 1996;46(3):395-416. 32. Cashin JR, Presley CA, Meilman PW. Alcohol use in Drug Educ the Greek system: Follow the leader? J Stud Alcohol. 46. Chassin L, Pitts SC, Prost J. Binge drinking trajectories 61. Jessor R, Costa FM, Krueger PM, et al. A 1998;59(1):63-70. PMID: 9498317. from adolescence to emerging adulthood in a developmental study of heavy episodic drinking high-risk sample: Predictors and substance abuse among college students: The role of psychosocial 33. Larimer ME, Turner AP, Mallett KA, et al. Predicting outcomes. J Consult Clin Psychol. 2002;70(1):67-78. and behavioral protective and risk factors. J Stud drinking behavior and alcohol-related problems PMID: 11860058. Alcohol. 2006;67(1):86-94. PMID: 16536132. among fraternity and sorority members: Examining the role of descriptive and injunctive norms. Psychol 47. Greenbaum PE, Del Boca FK, Darkes J, et al. Variation 62. Benton SL, Schmidt JL, Newton FB, et al. College Addict Behav. 2004;18(3):203. PMID: 15482075. in the drinking trajectories of freshmen college student protective strategies and drinking students. J Consult Clin Psychol. 2005;73(2):229. consequences. 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Binge Drinking Among College-Age Individuals | 29 Women Health. 1992;19(2-3):69-85. PMID: 76. Plunk AD, Cavazaos-Rehg P, Bierut LJ, et al. The 88. Paljärvi T, Koskenvuo M, Poikolainen K, et al. 1492412. persistent effects of minimum legal drinking age laws Binge drinking and depressive symptoms: A 5‐ on drinking patterns later in life. Alcohol Clin Exp Res. year population‐based cohort study. . 64. Martens MP, Taylor KK, Damann KM, et al. Protective Addiction 2013;37(3):463-469. PMID: 23347177. behavioral strategies when drinking alcohol and 2009;104(7):1168-1178. PMID: 19438420. their relationship to negative alcohol-related 77. Reyna VF, Croom K, Staiano-Coico L, et al. 89. Plant MA, Plant ML, Miller P, et al. The social consequences in college students. Psychol Addict Endorsement of a personal responsibility to adhere to consequences of binge drinking: A comparison of Behav. 2004;18(4):390-393. PMID: 15631613. the minimum drinking age law predicts consumption, young adults in six European countries. J Addict Dis. risky behaviors, and alcohol-related harms. Psychol 65. Burke A, Van Olphen J, Eliason M, et al. Re-examining 2009;28(4):294-308. PMID: 20155600. Public Policy Law. 2013;19(3):380-394. PMID: religiosity as a protective factor: Comparing alcohol 24078780. 90. Crego A, Holguín SR, Parada M, et al. Binge drinking use by self-identified religious, spiritual, and secular affects attentional and visual working memory college students. J Relig Health. 2014;53(2):305- 78. Borsari B, Neal DJ, Collins SE, et al. Differential utility processing in young university students. Alcohol Clin 316. PMID: 22706922. of three indexes of risky drinking for predicting Exp Res. 2009;33(11):1870-1879. PMID: 19673739. 66. Ahern J, Galea S, Hubbard A, et al. “Culture of alcohol problems in college students. Psychol Addict drinking” and individual problems with alcohol use. Behav. 2001;15(4):321. PMID: 11767264. 91. Verster JC, van Duin D, Volkerts ER, et al. Alcohol effects on memory functioning and Am J Epidemiol. 2008;167(9):1041-1049. PMID: 79. Carlson SR, Johnson SC, Jacobs PC. Disinhibited vigilance performance after an evening of 18310621. characteristics and binge drinking among university binge drinking. . student drinkers. Addict Behav. 2010;35(3):242-251. Neuropsychopharmacology 67. Fillo J, Rodriguez LM, Anthenien AM, et al. The angel 2003;28(4):740-746. PMID: 12655320. and the devil on your shoulder: Friends mitigate PMID: 19926401. and exacerbate 21st birthday alcohol-related 80. Cranford JA, McCabe SE, Boyd CJ. A new measure 92. Weissenborn R, Duka T. Acute alcohol effects consequences. Psychol Addict Behav. In press. of binge drinking: Prevalence and correlates in a on cognitive function in social drinkers: Their relationship to drinking habits. Psychopharmacology. 68. DiGrande L, Perrier MP, Lauro MG, et al. Alcohol use probability sample of undergraduates. Alcohol Clin 2003;165(3):306-312. PMID: 12439627. and correlates of binge drinking among university Exp Res. 2006;30(11):1896-1905. PMID: 17067355. students on the island of Sardinia, Italy. Subst Use 81. Okoro CA, Brewer RD, Naimi TS, et al. Binge drinking 93. Squeglia LM, Schweinsburg AD, Pulido C, et al. Misuse. 2000;35(10):1471-1483. PMID: 10921435. and health-related quality of life: Do popular Adolescent binge drinking linked to abnormal spatial 69. Clapp JD, Shillington AM, Segars LB. Deconstructing perceptions match reality? Am J Prev Med. working memory brain activation: Differential gender contexts of binge drinking among college students. 2004;26(3):230-233. PMID: 15026103. effects. Alcohol Clin Exp Res. 2011;35(10):1831- 1841. PMID: 21762178. Am J Drug Alcohol Abuse. 2000;26(1):139-154. 82. Popovici I, French MT. Binge drinking and sleep PMID: 10718169. problems among young adults. Drug Alcohol Depend. 94. Stephens DN, Duka T. Cognitive and emotional 70. Weitzman ER, Kawachi I. Giving means receiving: 2013;132(1):207-215. PMID: 23466223. consequences of binge drinking: Role of amygdala The protective effect of social capital on binge 83. Naimi TS, Brewer RD, Mokdad A, et al. Binge drinking and prefrontal cortex. Philos Trans R Soc London drinking on college campuses. Am J Public Health. among U.S. adults. JAMA. 2003;289(1):70-75. PMID: B Biol Sci. 2008;363(1507):3169-3179. PMID: 2000;90:1936-1939. PMID: 11111272. 12503979. 18640918 71. Duncan GJ, Wilkerson B, England P. Cleaning up their 84. Bell S, Britton A, Kubinova R, et al. Drinking pattern, 95. Courtney KE, Polich J. Binge drinking in young adults: act: The effects of marriage and cohabitation on licit abstention and problem drinking as risk factors Data, definitions, and determinants.Psychol Bull. and illicit drug use. Demography. 2006;43:691-710. for depressive symptoms: Evidence from three 2009;135(1):142-156. PMID: 19210057. PMID: 17236542. urban Eastern European populations. PloS One. 96. White AM, Kraus CL, Swartzwelder HS. Many college 2014;9(8):e104384. PMID: 25118714. 72. Eitle D, Taylor J, Eitle TM. Heavy episodic alcohol freshmen drink at levels far beyond the binge use in emerging adulthood: The role of early risk 85. Chou KL, Liang K, Mackenzie CS. Binge drinking and threshold. Alcohol Clin Exp Res. 2006;30(6):1006- factors and young adult social roles. J Drug Issues. Axis I psychiatric disorders in community-dwelling 1010. PMID: 16737459. 2010;40:295-320. middle-aged and older adults: Results from the 97. Fillmore MT, Jude R. Defining “binge” drinking as 73. Kerr DCR, Capaldi DM, Owen LD, et al. Changes in National Epidemiologic Survey on Alcohol and five drinks per occasion or drinking to a .08% at-risk American men’s crime and substance use Related Conditions (NESARC). J Clin Psychiatry. BAC: Which is more sensitive to risk? Am J Addict. trajectories following fatherhood. 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30 | Vol. 39, No. 1 Alcohol Research: Current Reviews “Maturing Out” of Binge and Problem Drinking

Matthew R. Lee and Kenneth J. Sher

Matthew R. Lee, Ph.D., is research This article reviews literature rates, alcohol use disorder (AUD) assistant professor, Department of aiming to explain the widespread is among the most prevalent men- Psychological Sciences, University of reductions in binge and problem tal health disorders in the United Missouri, Columbia, Missouri. drinking that begin around the States. An estimated 15.7 million transition to young adulthood (5.9%) of Americans age 12 or older Kenneth J. Sher, Ph.D., is curators’ (i.e., “maturing out”). Whereas have a past-year AUD diagnosis.1 distinguished professor, Department most existing literature on matur- These rates are a public health con- of Psychological Sciences, University ing out emphasizes contextual cern, as problem drinking in the effects of transitions into adult of Missouri, Columbia, Missouri. United States costs an estimated roles and responsibilities, this $249 billion per year2 and is the article also reviews recent work fourth-leading cause of preventable demonstrating further effects of mortality.3 young adult personality matura- Perhaps the most striking demo- tion. As possible mechanisms of graphic feature of problem drink- naturally occurring desistance, ing (and various other risky or these processes could inform deviant behaviors) is its nonlinear both public health and clinical association with age, characterized interventions aimed at spurring by increases during adolescence, similar types of drinking-related peaks around ages 18 to 22, and behavior change. This article also reductions beginning in the mid- draws attention to evidence that 20s.4 However, studies showing age the normative trend of age-related differences in drinking-related rates reductions in problem drinking for epidemiologic purposes tend to extends well beyond young adult- contrast relatively broad age groups, hood. Specific factors that may be and a finer-grained depiction is particularly relevant to problem informative from a developmental drinking desistance in these later standpoint. Figure 1 shows the periods are considered within a results of the authors’ descriptive broader life span developmental analyses of age-prevalence gradients framework. for different drinking-related out- Binge drinking is strikingly comes (and other drug-related out- prevalent in the United States. An comes included for contrast). estimated 66.7 million (24.9%) of As shown in Figure 1, prevalence Americans age 12 or older report rates for a variety of drinking-related binge drinking in the past month, outcomes peak in the early 20s. according to the National Survey on Specifically, in the early 20s, past- Drug Use and Health (NSDUH).1 year binge drinking and intoxication This estimate is based on a binge rates both reach peaks of around drinking definition of 4 or more 45%, and past-year AUD rates drinks on the same occasion for reach a peak of 19%. Although not women, and 5 or more drinks on depicted, similar drinking-related the same occasion for men, on at peaks are observed for college stu- least 1 day in the past 30 days (see dents and their noncollege peers, Drinking Patterns and Their suggesting the peaks are at least Definitions in this issue for a review partially driven by more general of binge drinking definitions). In mechanisms beyond college atten- addition to high binge drinking dance.5 Regarding historic trends,

“Maturing Out” of Binge and Problem Drinking | 31 “Maturing Out” of Binge and Problem Drinking (continued)

drinking-related declines have researchers have also observed the This robust age-prevalence curve been observed across adolescent age-prevalence curve in a number motivates and informs the conceptu- cohorts in recent years. For instance, of longitudinal studies assessing alization of problem drinking from 12th-grade rates of past 2-week how prevalence rates change as a a developmental psychopathology binge drinking decreased from a cohort ages.7 standpoint.8,9 Other articles in this peak of 32% in 1998 to an historic low of 17% in 2015.6 However, col- lege students and young adults have had far more modest cohort declines in binge drinking (i.e., from a 39% peak in 2008 to 32% in 2015 for college students, and from a 41% peak in 1997 to 32% in 2015).6 Similar conclusions regarding his- toric changes across adolescent and young adult cohorts can be drawn from NSDUH data on AUD.1 Figure 1 also shows that, follow- ing peak prevalences in the early 20s, reliable age-related reductions in a variety of drinking-related outcomes occur beginning in the mid-20s and continue through- out the remainder of the life span. For instance, after the peak binge drinking rate of 45% in the early 20s, the rate declines to 38% by the late 20s, 29% by the late 30s, 22% by the late 40s, and 14% by the late 50s. For AUD, reductions Figure 1 Age-prevalence gradients showing U.S. past-year rates of alcohol-related indi- ces and other drug-related indices across age groups. Prevalence rates for appear especially dramatic in young a variety of drinking-related outcomes peak in the early 20s. Following this adulthood. Specifically, after peaking peak, reliable age-related reductions in a variety of drinking-related outcomes at 19% in the early 20s, the rate occur beginning in the mid-20s and continue throughout the remainder of decreases rapidly to 13% by the late the life span. Note: Binge drinking was defined as four or more drinks on one 20s, then more gradually to 10% by occasion for females and five or more drinks on one occasion for males. the late 30s, 8% by the late 40s, and Disorder rates reflect Diagnostic and Statistical Manual of Mental Disorders 3% by the late 50s. Of course, such (DSM-IV) criteria for abuse or dependence except for disorder, which cross-sectional age differences must reflects DSM-IV criteria for . Source: Prevalence rates be interpreted with caution, as dif- for ages 12 to 17 are based on NSDUH 2002 data from Substance Abuse ferential mortality of problem drink- and Mental Health Services Administration, Center for Behavioral Health Statistics and Quality. Key Substance Use and Mental Health Indicators ers and secular changes in prevalence in the United States: Results From the 2015 National Survey on Drug Use rates could artifactually create the and Health. Rockville, MD: U.S. Department of Health and Human Services; appearance of a developmental age September 2016. Prevalence rates for ages 18 to 70+ are based on gradient. However, it is unlikely National Epidemiologic Survey on Alcohol and Related Conditions (NESARC) that such factors could plausibly 2001 to 2002 data from Grant BF, Moore TC, Shepard J, et al. Source and explain the magnitude of the rate Accuracy Statement: Wave 1 National Epidemiologic Survey on Alcohol and changes with age, given the some- Related Conditions. Bethesda, MD: National Institute on Alcohol Abuse and what limited extent of overall mor- Alcoholism, U.S. Department of Health and Human Services; 2003. tality and secular variation. Further,

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special issue describe factors contrib- decreased impulsivity and neurot- Young adulthood is marked by uting to the escalation and eventual icism) during young adulthood. widespread adoption of such roles,15 peak of problem drinking leading up Further sections then discuss the and well-established developmental to the early 20s. This article focuses need for more life span develop- theory views these transitions as key on factors contributing to the later mental research to explain the later young adult developmental tasks.16 trends toward problem-drinking drinking reductions observed in Role incompatibility theory is often reductions beginning around young developmental periods beyond referenced to explain how these adulthood. young adulthood, noting some roles influence maturing out.17 The mechanisms that may be particularly theory holds that, when a state of relevant to desistance in these peri- conflict (i.e., incompatibility) exists Maturing Out of ods (i.e., “natural recovery” processes between a behavior (e.g., drinking) Problem Drinking and health issues). A key point per- and demands of a social role, this taining to all mechanisms reviewed can initiate a process called role The dramatic age-related reductions here is that more research is needed socialization, whereby conflict is in problem drinking that begin in on possible historic changes in how resolved through changes in the young adulthood have motivated these mechanisms have operated. behavior. However, the theory also empirical efforts to understand Preliminary descriptive evidence posits role selection effects in the desistance from a developmental suggests historic differences across perspective. Despite the overall trend cohorts in the age-related trend of opposite direction, whereby individ- toward maturing out after young escalation followed by maturing ual characteristics and behaviors can adulthood, a substantial subset of out.5(pp221-222) Key public policy influence the likelihood of later role individuals show persistent or esca- insights could be gleaned from adoption. These are two very differ- lating problem drinking beyond this in-depth analyses of such cohort ent processes through which roles developmental period.10 Knowledge changes in age trends and how they and drinking behaviors can become of what differentiates develop- may relate to cohort changes in associated, so research investigating mentally limited versus persistent desistance mechanisms (e.g., the possible role socialization effects patterns of problem drinking can prevalence, life-course timing, and must consider role selection as an help clarify the nature of problem impact of adult role transitions). alternative explanation. drinking and inform public health It is also noteworthy that evidence and clinical interventions.11 Indeed, exists for gender, racial, and ethnic Evidence for Role Socialization in addition to the above evidence differences in both patterns and With few exceptions,18-20 both mar- that maturing out can include desis- mechanisms of age-related drinking riage and parenthood during young tance of syndromal AUD, research reductions.4,7,14 Although discussion adulthood are generally predictive of also suggests that problem-drinking of such differences is largely beyond reductions during young adult- the scope of the current brief review, later problem-drinking reductions. hood are particularly likely to occur this should be noted as another Further, although many studies have tested only effects of either marriage among those who were relatively important topic in need of further 21-28 severe problem drinkers prior to this exploration in future research. or parenthood in isolation, there developmental period.12,13 These is also research demonstrating that findings support the importance both marriage and parenthood can of research aimed at understanding Young Adult Role Transitions contribute uniquely to these reduc- 15,29,30 maturing out as a means of guiding and Maturing Out tions. In contrast, research future interventions. has often failed to show that The following sections review The most commonly offered expla- employment contributes to reduced evidence for different possible mech- nation for maturing out of problem problem drinking in young adult- anisms of maturing out, beginning drinking during young adulthood is hood,15,24,27 although some evidence with effects of adult role transitions that it is driven by transitions into for this effect has been found within (e.g., marriage and parenthood) adult roles like marriage, parent- certain occupational categories (e.g., and personality maturation (e.g., hood, and full-time employment.15 “professional” jobs).30

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Evidence for Role Selection mediation via changes in drink- sociability),46 whereas “Big Five” ing-related attitudes and increased models typically include neuroti- Most studies have failed to show 27,28,30,42 that alcohol use reduces the like- religiosity. Mediation via peer cism, extraversion, conscientious- lihood of young adult marriage, involvement is particularly consis- ness, agreeableness, and openness tent with the popular role incom- 47,48 parenthood, or employment,21,27 (or intellect). Within Big Five patibility explanation of family role with some findings even suggest- models, distinct components of effects on maturing out (described ing the opposite effect.15 However, impulsivity and constraint (e.g., above), as role demands may restrict results appear more mixed for more lack of perseverance and negative socializing opportunities. However, severe indices of problem drinking as articulated in Platt’s commentary affect urgency) are represented as and for illicit substance use. For on how to achieve “strong infer- smaller facets of the larger broad- example, research has shown that ence,” future studies should conduct band traits (e.g., conscientiousness AUD can prevent marriage and 49 “riskier” tests of role incompatibility and neuroticism). It is beyond 31,32 and that illicit sub- parenthood, theory.43 This means testing hypoth- this brief review’s scope to broadly stance use can prevent marriage and eses that could potentially provide review the many ways these and employment.15,33-35 discriminating support for role other models of personality have incompatibility theory over other been linked to drinking, but see Practical Implications of Role plausible explanations, and testing Effects on Maturing Out Sher and colleagues for an in-depth hypotheses that could potentially review of personality and alcohol In addition to evidence that fam- disconfirm the theory in favor of research.45 ily roles can spur desistance from other explanations. For instance, 24,36 This review focuses on one par- AUD, there is even evidence that an explicit assessment of conflict ticularly relevant burgeoning area between drinking and role demands these roles may have especially dra- of personality research that has (role incompatibility) could pro- matic effects among those who were emphasized movement beyond a particularly severe problem drinkers vide discriminating support for prior to role adoption.37 These find- role incompatibility theory,37 and static view of personality, acknowl- ings support the clinical significance, this should be tested against other edging that normative changes in not only of maturing out in gen- plausible mechanisms, such as the personality occur throughout the eral, but of role-driven pathways to interpersonal support, security, and life span. Importantly, findings maturing out in particular. Further, satisfaction that family roles can include evidence for adaptive (i.e., beyond family role effects on drink- provide.44 presumably beneficial) changes ing-related maturing out, there is in personality traits that have mounting evidence from diverse been linked closely to heavy and literatures that family roles convey Young Adult Personality problematic drinking, including various protective effects that can Development and impulsivity, conscientiousness, and cascade across many domains of life Maturing Out neuroticism. Further, maturational to broadly spur adaptation and miti- 38-41 changes in these traits appear par- gate pathology. A vast, long-standing literature links ticularly rapid during the transition However, given the potential personality and drinking, although to young adulthood (i.e., the 20s importance of these processes from variability in personality models, and 30s), the period when norma- a public health standpoint, it is definitions, and terminology can surprising how little is known about sometimes complicate interpreta- tive age-related declines in drink- the mechanisms through which tion of this work.45 For instance, ing generally begin. For instance, roles influence substance-related “Big Three” models of the traits Figure 2 depicts meta-analytic maturing out. Existing mediational that compose personality typically evidence for age-related increases findings show the most robust sup- include constraint (related to impul- throughout the adult life span in port for mediation of role effects sivity and risk taking), neuroticism both emotional stability (akin to via reduced socializing with peers, (e.g., anxiety, depression, and stress lack of neuroticism) and conscien- with additional mixed evidence for reactivity), and extraversion (e.g., tiousness.39,50,51

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Correlated Change in Personality follow-up study using the same data Directional Effects of Personality and Problem Drinking also showed that age-related changes on Drinking Over the Course of in drinking motives mediated effects Perhaps motivated by the above Young Adulthood of age-related personality change evidence for personality matura- The above studies of correlated on age-related problem-drinking tion, a subsequent series of studies reductions.54 Specifically, reductions change between personality and has shown that the normative in neuroticism and impulsivity pre- problem drinking have forged an age-related drinking reductions of dicted reductions in coping-related entirely new avenue for research on young adulthood may be partially drinking motives, which in turn pre- drinking-related maturing out, with explained by age-related personality one important next step being inves- 52,53 dicted reductions in problem drink- change. Longitudinal growth ing. These are the only studies, to tigation of different possible direc- models showed a reduction in our knowledge, analyzing correlated tions of effects. Toward this objec- average levels of problem drinking change in personality and drinking tive, Lee and colleagues estimated from ages 18 to 35, along with as an explanation for the norma- cross-lag models testing bidirectional corresponding reductions in impul- tive drinking reductions observed effects between personality and sivity and neuroticism and increases around the developmental transition problem drinking across four waves in conscientiousness. Further, to young adulthood (i.e., maturing spanning ages 21 to 34.56 Results parallel-process growth models out), although other studies have showed some prospective effects of showed correlated change such that shown similar correlated change personality on problem drinking, those with greater age-related mat- in earlier developmental periods with lower impulsivity and higher uration in these three personality of normative drinking-related conscientiousness at age 29 both domains also had greater age-related escalation (i.e., adolescence to the predicting lower problem drinking reductions in problem drinking. A early 20s).55 at age 34 (see Figure 3). In contrast,

Figure 2 Developmental personality maturation across the life span. Results from a meta-analysis, demonstrating age-related increases throughout the adult life span in both emotional stability and conscientiousness. Source: Adapted from Roberts BW, Walton KE, Viechtbauer W. Patterns of mean-level change in personality traits across the life course: A meta-analysis of longitudinal stud- ies. Psychol Bull. 2006;132(1):1-25.

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results did not show prospective adaptive response to age-increasing dicted lower problem drinking at effects of neuroticism on subsequent contextual demands (e.g., from fam- age 29 (see Figure 3). In contrast, problem drinking (nor prospective ily roles).39 These alternative views personality was not found to medi- effects in the opposite direction). imply different predictions regard- ate role effects, as role transitions ing possible mediated pathways consistently failed to predict later Integrating Adult Role involving role and personality effects personality. and Personality Effects on on problem-drinking reductions. Maturing Out To investigate these possibilities, Practical Implications of Beyond the largely separate bodies the cross-lag models of Lee and Personality Development Effects of evidence for family role and per- colleagues (discussed above) also on Maturing Out sonality maturation effects on young included transitions into family The notion of interventions target- 56 adult drinking reductions, little roles (marriage or parenthood). ing personality change has received work exists advancing an integrated Results showed that family role increased attention in recent litera- model of these ameliorative pro- transitions mediated personality ture.57 The above-discussed research cesses. Differing views conceptualize effects, with higher conscientious- on personality and maturing out personality maturation as unfolding ness and lower impulsivity at age 21 has especially highlighted the poten- either (1) due to biologically pro- predicting transitions into a family tial utility of reducing impulsivity grammed maturation or (2) as an role by age 25, which in turn pre- and increasing conscientiousness.

Figure 3 An integrative model of family role and personality effects on young adult maturing out of problem drinking, showing results of a cross-lagged panel model of marriage and parenthood, conscientiousness, and problem drinking across four longitudinal time points. Results of cross-lag models showed some prospective effects of personality on problem drinking, with higher conscientiousness at age 29 predicting lower problem drinking at age 34. Family role transitions mediated personality effects, with higher conscientiousness at age 21 predicting transitions into a family role by age 25, which in turn predicted lower problem drinking at age 29. Note: Colors highlight parts of the model testing hypothesized mediation paths. Red variables and paths highlight results confirming the hypothesized mediation of conscientiousness effects on problem drinking via marriage and parenthood. Blue variables and paths highlight results failing to confirm the hypothesized mediation of marriage and parenthood effects on problem drinking via conscientiousness. For marriage/parenthood: 0 = remained never married and a nonparent, 1 = became married or a parent. For family AUD: 0 = family history negative, 1 = family history positive. For sex: 0 = male, 1 = female. *p < .05. **p < .01. Source: Adapted from Lee MR, Ellingson JM, Sher KJ. Integrating social-contextual and intrapersonal mechanisms of “maturing out”: Joint influences of familial-role transitions and personality maturation on problem-drinking reductions. Alcohol Clin Exp Res. 2015;39(9):1775-1787.

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Littlefield and colleagues specu- ious task-based measures of impul- life span. Vergés and colleagues lated that interventions fostering sivity/disinhibition,60 a key objective assessed changes across the life span maturity in these domains might should be to confirm age-related in rates of persistence, new onset, spur relatively durable changes in changes in these measures and their and recurrence of alcohol depen- drinking behaviors.52 Lee and col- associations with age-related drink- dence to understand their unique leagues noted, based on the above ing reductions. Such research could contributions to overall age-related mediation findings, that pre–young confirm conclusions from survey reductions in adult personality interventions could findings and further inform the rates.20 Results showed especially convey protective effects, in part by practical application of this work. marked age reductions in new onsets aiding successful transitions to fam- Further, although clear links have (see Figure 4, middle panel). Thus, ily roles in young adulthood.56 Based been established among personality although the term “maturing out” on evidence for persistent effects maturation, adult role adoption, may be taken to imply age increases of childhood impulsivity even on and drinking reductions, more work in desistance, the continual declines midlife outcomes, Moffitt and col- is needed to establish directional- in AUD rates observed throughout leagues argued that universal preven- ity of effects within analyses that the life span instead appear mainly tion programs fostering childhood unambiguously capture develop- attributable to reductions in new self-control could confer substantial mental change in these constructs. onsets. In contrast, although not and lasting benefits to most individ- For instance, the cross-lagged emphasized by Vergés and col- uals and to an entire population.58 panel study by Lee and colleagues56 leagues, rates of desistance appeared Indeed, early prevention and inter- addressed the unknown directional- to peak in young adulthood. Based vention programs fostering personal- ity in the growth-modeling studies on persistence rates in their study, ity-related maturity could influence of Littlefield and colleagues,52-54 but it can be inferred that the rate of many etiologic pathways, thereby personality effects in the analyses by desistance peaked at 72% by ages conveying protective effects that cas- Lee and colleagues did not isolate 28 to 32, then declined to a low of cade across multiple developmental influences of age-related change in 55% by ages 43 to 52 and remained stages and domains of life. personality traits. Thus, creative ana- somewhat low thereafter (see Figure However, to bolster confidence in lytic applications are needed to com- 4, upper panel). Thus, an interesting the above implications, additional bine the separate strengths of past possibility is that risk for AUD onset research is needed to confirm and research. This work also may require may continually decline throughout further characterize the phenome- careful conceptualization of the the life span, whereas potential for non of personality maturation and predicted timings and durations of desistance from an existing AUD its effects on age-related drinking the developmental processes under may peak in young adulthood. reductions. Caution is perhaps investigation. Perhaps confirming and extending warranted regarding the use of sur- the latter notion, ongoing data vey measures to show personality analyses by the authors62 have inves- change, as measurement invariance Maturing Out of Problem tigated desistance across the life span across ages can spuriously influence Drinking Beyond while differentiating among mild, apparent age-related changes.59 Young Adulthood moderate, and severe AUD (per the However, given the magnitude of Diagnostic and Statistical Manual of personality change observed across As discussed above, age-related Mental Disorders [DSM-5] severity the life span,39(p15) and its associa- drinking reductions are not confined grading).63 Results showed that for tions with changes in various life to young adulthood, but instead those with a severe AUD, desistance circumstances,50 it is unlikely that begin in young adulthood and con- rates were substantially higher in this phenomenon is largely attrib- tinue throughout the remaining life young adulthood than in later devel- utable to a measurement artifact. span. Beyond the earlier-reviewed opmental periods (e.g., severe AUD Nonetheless, confidence could be epidemiologic evidence, some desistance rates of 46% to 49% at bolstered by showing this phenom- additional research offers a more ages 25 to 34 versus 25% to 29% at enon with alternative methods. For precise account of changes in ages 35 to 55). Of course, given that instance, given the existence of var- problem drinking across the adult both above studies used data from

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the U.S. National Epidemiologic Survey on Alcohol and Related Conditions (NESARC), these anal- yses should be replicated in other data sets. The above evidence for differences across the life span in patterns of desistance suggests there may also be important differences across the life span in mechanisms of desistance. Assessing this possibility should be a key goal of future research, as researchers have clearly gleaned insights through similar attention to developmental variability in etiologic processes of earlier devel- opmental periods (i.e., childhood and adolescence).64 The following sections consider some specific ways that the mechanisms influencing problem drinking desistance may vary across periods of the adult life span.

Maturing Out Versus Natural Recovery Models of Desistance Predictions regarding develop- mental variability in desistance mechanisms can perhaps be made based on Watson and Sher’s review highlighting dramatic differences in how desistance is viewed between the “maturing out” and “natural Figure 4 Deconstructing the overall pattern of age differences in alcohol dependence 65 recovery” literatures. As discussed rates, showing separate plots of age differences in persistence (upper earlier, the maturing out literature panel), onset (middle panel), and recurrence (lower panel) of alcohol focuses on young adulthood and dependence, using NESARC data.61 Brackets show 95% confidence intervals has largely viewed desistance as around estimates. Note: Persistence rate was defined as the percentage of stemming from contextual changes participants with a past-year alcohol dependence diagnosis at baseline who in this developmental period (e.g., also had a past-year alcohol dependence diagnosis at the 3-year follow-up. marriage)15 and accompanying role New onset rate was defined as the percentage of participants with no lifetime history of alcohol dependence at baseline who had a diagnosis of past-year demands that conflict with alcohol alcohol dependence at the 3-year follow-up. Recurrence rate was defined as 17 involvement. Importantly, these the percentage of participants with lifetime but no past-year alcohol depen- processes are rarely conceptualized dence at baseline who had a diagnosis of past-year alcohol dependence by as involving acknowledgment or the 3-year follow-up. Source: Adapted from Vergés A, Jackson KM, Bucholz concern regarding one’s drinking.4,65 KK, et al. Deconstructing the age-prevalence curve of alcohol dependence: A starkly different view of desistance Why “maturing out” is only a small piece of the puzzle. J Abnorm Psychol. comes from the natural recovery 2012;121(2):511-523. literature, which has investigated

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precursors of desistance mostly in point of overlap between natural vance of affect- and coping-related midlife samples (e.g., mean age = recovery and personality maturation issues to older adult drinking.78 41 years [SD = 9.1] in a review by research. Thus, personality matura- For instance, there is evidence that Sobell and colleagues).66 Informed tion in young adulthood (e.g., con- health problems can spur drinking in part by models of behavior scientiousness increases) may distally reductions except among those who change (e.g., Stall and Biernacki’s potentiate later natural recovery drink to cope, for whom health stages of spontaneous remission),67 processes of problem recognition problems can have the opposite this literature often views desistance and effortful change. Although effect.77,79 as stemming from an accumulation quite speculative, if the above pre- Future studies should expand of drinking consequences that can dictions are supported, this would upon the relative dearth of research prompt (1) deliberate reappraisals help bridge divides among different in this area. This work should of one’s drinking, followed by (2) highly influential, yet ostensibly dis- include further study of how self-identification as a problem crepant, views of desistance. More affect- and coping-related factors drinker (i.e., problem recognition), generally, investigating these predic- may impede adaptive responding and then (3) targeted efforts to tions could help advance the field to drinking-related health issues. change drinking habits.68 toward a more unified understand- Attention should also be paid to Predictions can perhaps stem ing of desistance across the life span how these processes are influenced from an overarching premise that and thereby inform developmental by aging-related increases in alcohol the maturing out and natural recov- tailoring of public health and clini- sensitivity80,81 and changes in social ery literatures may both offer valid cal interventions. support systems.73 These questions conceptualizations of desistance, are particularly important given with maturing out models applying Older Adult Health and Problem the increases in older adult prob- predominantly to young adulthood Drinking Desistance lem drinking that are projected to and natural recovery models apply- coincide with the aging of the “baby ing predominantly to midlife and Although health and drinking are, boomer” generation.82 Indeed, these later developmental periods. That is, of course, interrelated throughout 71,72 projections suggest a great future desistance in young adulthood may the life span, older adulthood need for research informing policy more often stem from the broad brings various health-related phys- and clinical interventions for older cascade of maturational contextual ical and cognitive challenges that adult problem drinkers. changes that occurs in this period, may increase in importance as whereas desistance in later periods desistance mechanisms in this late may more often stem from more developmental stage.73 There is evi- Summary of Key Points direct processes of deliberate prob- dence that more than 50% of U.S. lem recognition and change efforts. seniors drink at levels deemed risky Although a distinct peak in prob- These predictions are consistent in the context of co-occurring medi- lem drinking rates is observed in with the general idea that contex- cal conditions.74 Further, along with the early 20s, the reductions that tual effects are stronger earlier in these health issues comes increased follow (i.e., maturing out) are not development, whereas intrapersonal use of medications that could inter- confined to the subsequent period of effects increase with age69 as indi- act harmfully with alcohol, with a young adulthood. Problem-drinking viduals increasingly construct their striking 76% of U.S. seniors using reductions continue throughout own environments.70 It is also note- multiple prescription medications.75 all remaining stages of the adult worthy that there is conceptual sim- Of the small extant literature on life span. ilarity between the deliberate reap- older adult drinking, health issues In addition to robust evidence praisal of one’s drinking described are among the most commonly that young adult desistance is in the natural recovery literature reported reasons for desistance.76 spurred by transitions into family and the drinking attitude change However, studies of prospective roles, more recent work shows believed to mediate personality mat- effects of health problems on drink- additional likely influences of devel- uration effects on drinking-related ing changes are more equivocal,76,77 opmental personality maturation. desistance, suggesting a possible perhaps owing to the complex rele- Research is needed to further clarify

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these ameliorative influences, the 2. Sacks JJ, Gonzales KR, Bouchery EE, et al. 13. Lee MR, Chassin L, Villalta IK. Maturing out of 2010 national and state costs of excessive alcohol involvement: Transitions in latent drinking mechanisms through which they alcohol consumption. Am J Prev Med. statuses from late adolescence to adulthood. Dev operate, and how they are inter- 2015;49(5):e73-e79. PMID: 26477807. Psychopathol. 2013;25(4 pt 1):1137-1153. PMID: 24229554. related. Such work may yield key 3. Stahre M, Roeber J, Kanny D, et al. Contribution practical insights that could inform of excessive alcohol consumption to deaths 14. Chassin L, Colder CR, Hussong A, et al. Substance the design of clinical and public and years of potential life lost in the United use and substance use disorders. In: Cicchetti health interventions. States. Prev Chronic Dis. 2014;11:e109. PMID: D, ed. Developmental Psychopathology. Vol 3. In contrast with developmental 24967831. 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On the resolution of Students and Adults Ages 19–55. Ann Arbor, reconciling these ostensibly discrep- role incompatibility: A life event history analysis MI: Institute for Social Research, University of of family roles and marijuana use. Am J Sociol. ant models. Michigan; July 2015. http://monitoringthefuture. 1985;90(6):1284-1325. More research is needed on org/pubs/monographs/mtf-vol2_2014.pdf. health-related mechanisms of prob- Accessed July 18, 2017. 18. Gotham HJ, Sher KJ, Wood PK. Predicting stability and change in frequency of intoxication from the lem drinking desistance among 6. Miech RA, Johnston LD, O’Malley PM, et al. college years to beyond: Individual-difference Monitoring the Future National Survey Results older adults. and role transition variables. J Abnorm Psychol. on Drug Use, 1975–2014: Volume I, Secondary 1997;106(4):619-629. PMID: 9358692. School Students. Ann Arbor, MI: Institute for Social Research, University of Michigan; June 2015. 19. Overbeek G, Vollebergh W, Engels RC, et al. Young Acknowledgments http://monitoringthefuture.org/pubs/monographs/ adults’ relationship transitions and the incidence mtf-vol1_2014.pdf. Accessed July 19, 2017. of mental disorders: A three-wave longitudinal study. Soc Psychiatry Psychiatr Epidemiol. Writing of this review was sup- 7. Chen P, Jacobson KC. Developmental trajectories 2003;38(12):669-676. PMID: 14689170. ported by National Institute on of substance use from early adolescence to Alcohol Abuse and Alcoholism young adulthood: Gender and racial/ethnic 20. Vergés A, Jackson KM, Bucholz KK, et al. grant K99-AA-024236 to Dr. Lee differences. J Adolesc Health. 2012;50(2):154- Deconstructing the age-prevalence curve of and grants T32-AA-013526 and 163. PMID: 22265111. alcohol dependence: Why “maturing out” is only a small piece of the puzzle. J Abnorm Psychol. 8. Sher KJ, Gotham HJ. Pathological alcohol K05-AA-017242 to Dr. Sher. 2012;121(2):511-523. 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J Drug Issues. 47. Costa PT Jr, McCrae RR. Revised NEO Personality and the study of change. Res Hum Dev. 2007;37(3):569-596. Inventory (NEO-PI-R) and NEO Five-Factor 2009;6(2-3):74-96. Inventory (NEO-FFI) Professional Manual. Odessa, 36. Dawson DA, Grant BF, Stinson FS, et al. Maturing 60. Dick DM, Smith G, Olausson P, et al. Review: FL: Psychological Assessment Resources; 1992. out of alcohol dependence: The impact Understanding the construct of impulsivity and its of transitional life events. J Stud Alcohol. 48. Goldberg LR. An alternative “description of relationship to alcohol use disorders. Addict Biol. 2006;67(2):195-203. PMID: 16568565. personality”: The Big-Five factor structure. J Pers 2010;15(2):217-226. PMID: 20148781. Soc Psychol. 1990;59(6):1216-1229. PMID: 37. Lee MR, Chassin L, MacKinnon DP. Role transitions 61. Grant, BF, Moore TC, Shepard J, et al. Source 2283588. and young adult maturing out of heavy drinking: and Accuracy Statement: Wave 1 National Evidence for larger effects of marriage among 49. Whiteside SP, Lynam DR. The Five Factor Model Epidemiologic Survey on Alcohol and Related more severe premarriage problem drinkers. and impulsivity: Using a structural model of Conditions. Bethesda, MD: National Institute on

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Alcohol Abuse and Alcoholism, U.S. Department of 68. Klingemann HK, Sobell, LC, eds. Promoting data for 2007–2008. NCHS Data Brief No. Health and Human Services; 2003. Self-Change From Addictive Behaviors: Practical 42. Hyattsville, MD: National Center for Health Implications for Policy, Prevention, and Treatment. 62. Lee MR, Boness CL, McDowell YE, et al. Desistance Statistics; 2010:1-8. PMID: 20854747. New York, NY: Springer; 2007. and severity of alcohol use disorder: A lifespan- 76. Schutte KK, Moos RH, Brennan PL. Predictors developmental investigation. Clin Psychol Sci. 69. Kendler KS, Jacobson KC, Gardner CO, et al. of untreated remission from late-life drinking In press. Creating a social world: A developmental twin problems. J Stud Alcohol. 2006;67(3):354-362. study of peer-group deviance. Arch Gen Psychiatry. 63. American Psychiatric Association. Diagnostic and PMID: 16608144. . 2007;64(8):958-965. PMID: 17679640. Statistical Manual of Mental Disorders: DSM-5 77. Moos RH, Brennan PL, Schutte KK, et al. Older 5th ed. Washington, DC: American Psychiatric 70. Scarr S, McCartney K. How people make their own adults’ health and late-life drinking patterns: Association; 2013. environments: A theory of genotype greater than A 20-year perspective. Aging Ment Health. 64. Chassin L, Sher KJ, Hussong A, et al. The environment effects. Child Dev. 1983;54(2):424- 2010;14(1):33-43. PMID: 20155519. developmental psychopathology of alcohol use 435. PMID: 6683622. 78. Schulte MT, Hser YI. Substance use and associated and alcohol disorders: Research achievements 71. Knott CS, Coombs N, Stamatakis E, et al. All health conditions throughout the lifespan. Public and future directions. Dev Psychopathol. cause mortality and the case for age specific Health Rev. 2014;35(2):1-27. PMID: 28366975. 2013;25(4 pt 2):1567-1584. PMID: 24342856. alcohol consumption guidelines: Pooled analyses 65. Watson AL, Sher KJ. Resolution of alcohol of up to 10 population based cohorts. BMJ. 79. Brennan PL, Schutte KK, Moos RH. Patterns and problems without treatment: Methodological 2015;350:h384. PMID: 25670624. predictors of late-life drinking trajectories: A 10-year longitudinal study. Psychol Addict Behav. issues and future directions of natural recovery 72. Plunk AD, Syed‐Mohammed H, Cavazos‐Rehg research. Clin Psychol Sci Pract. 1998;5:1-18. P, et al. Alcohol consumption, heavy drinking, 2010;24(2):254-264. PMID: 20565151. 66. Sobell LC, Ellingstad TP, Sobell MB. Natural and mortality: Rethinking the J‐shaped curve. 80. Dowling GJ, Weiss SR, Condon TP. Drugs of abuse recovery from alcohol and drug problems: Alcohol Clin Exp Res. 2014;38(2):471-478. PMID: and the aging brain. Neuropsychopharmacology. Methodological review of the research with 24033586. 2008;33(2):209-218. PMID: 17406645. suggestions for future directions. Addiction. 73. White W. Recovery across the life cycle. Alcohol 2000;95(5):749-764. PMID: 10885050. 81. Heuberger RA. Alcohol and the older adult: Treat Q. 2006;24(1-2):185-201. A comprehensive review. J Nutr Elder. 67. Stall R, Biernacki P. Spontaneous remission from 74. Moore AA, Giuli L, Gould R, et al. Alcohol use, 2009;28(3):203-235. PMID: 21184367. the problematic use of substances: An inductive comorbidity, and mortality. J Am Geriatr Soc. model derived from a comparative analysis of 82. Han B, Gfroerer JC, Colliver JD, et al. Substance 2006;54(5):757-762. PMID: 16696740. the alcohol, opiate, tobacco, and food/obesity use disorder among older adults in the United literatures. Int J Addict. 1986;21(1):1-23. PMID: 75. Gu Q, Dillon CF, Burt VL. Prescription drug use States in 2020. Addiction. 2009;104(1):88-96. 3710636. continues to increase: U.S. prescription drug PMID: 19133892.

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social consequences and other risk behaviors, including NIAAA’s College Alcohol missing class (53.8%), driving after drinking (40.6%), or engaging in unplanned (49.7%) or unprotected (52.3%) sex (percentages represent the proportion of individuals Intervention Matrix engaging in frequent binge drinking that endorsed experi- encing each consequence). These behaviors have long-term consequences that students can readily identify, includ- CollegeAIM ing academic failure, injury, legal complications, sexually transmitted disease, and death. Binge drinking also has lasting effects on the brain that produce less recognizable Jessica M. Cronce, Traci L. Toomey, Kathleen Lenk, consequences, such as impaired working memory and other Toben F. Nelson, Jason R. Kilmer, and Mary E. Larimer changes in mental processes that may be less apparent to the individual engaging in binge drinking or others as long as the person is generally functional, but which nonetheless The College Alcohol Intervention Matrix (CollegeAIM) is a user- may derail or impair optimal development.3 The prevalence friendly, interactive decision tool based on a synthesis of the of binge drinking, paired with the significant potential for substantial and growing literature on campus alcohol use both short-term and lasting harm, is why prevention is para- prevention. It includes strategies targeted at both the individual mount in this population. and environmental levels. Commissioned by the National Institute The National Institute on Alcohol Abuse and Alcoholism on Alcohol Abuse and Alcoholism (NIAAA), CollegeAIM reflects the (NIAAA) is at the forefront of efforts to prevent underage collective knowledge of 16 separate experts in the field, which and harmful alcohol use among college students. NIAAA makes it unique relative to other summaries of the science. funds research to develop and evaluate prevention strategies CollegeAIM is designed to help college stakeholders compare and contrast different evidence-based prevention strategies to select a mix of individual and environmental strategies that will work best on and around their campuses. CollegeAIM is Jessica M. Cronce, Ph.D., is an assistant professor in a living document, which will be updated to keep pace with the Department of Counseling Psychology and Human the science. Colleges are therefore encouraged to ensure that Services, College of Education, University of Oregon, evaluations of individual- or environmental-focused strategies Eugene, Oregon. on their campuses or in their communities make it into the Traci L. Toomey, Ph.D., is a professor in the Division published literature. of Epidemiology and Community Health, School of Key words: CollegeAIM; college drinking; literature review; Public Health, University of Minnesota, Minneapolis, prevention; research; underage drinking Minnesota. Kathleen Lenk, M.P.H., is a senior research fellow in the Division of Epidemiology and Community Health, Most students (81.4%) have consumed alcohol on at least one occasion by the time they reach college or at some School of Public Health, University of Minnesota, point during their college career.1 Many college students Minneapolis, Minnesota. (63.2%) report alcohol consumption within the past 30 Toben F. Nelson, Sc.D., is an associate professor in days, with 38.4% reporting “being drunk” at least once the Division of Epidemiology and Community Health, 1 during that same time frame. Rates of heavy episodic School of Public Health, University of Minnesota, drinking (i.e., binge drinking), defined in this sample as Minneapolis, Minnesota. consuming five or more drinks in a row on at least one occasion in the past 2 weeks for both men and women, Jason R. Kilmer, Ph.D., is an assistant director of Health roughly mirror the reported rates of being drunk (31.9%).1 and Wellness for Alcohol and Other Drug Education and Of course, students who engage in binge drinking may an associate professor in the Department of Psychiatry do so more than once during a 2-week period. In fact, and Behavioral Sciences, School of Medicine, University Wechsler and colleagues found that, of the 43% of students of Washington, Seattle, Washington. who said they engaged in binge drinking (defined in this study as four or more drinks in a row for women or five Mary E. Larimer, Ph.D., is a professor in the Department or more drinks in a row for men during the past 2 weeks), of Psychiatry and Behavioral Sciences, School nearly half reported three or more such occasions (44%, of Medicine, University of Washington, Seattle, or 19% of the total sample).2 In this study, frequent binge Washington. drinking was associated with a host of negative health and

NIAAA’s College Alcohol Intervention Matrix | 43 FOCUS ON

and creates dissemination tools to put evidence-based pre- both individual and environmental strategies as part of an vention approaches into the hands of college stakeholders. overall prevention approach. In 2002, NIAAA’s Task Force on College Drinking released a report, A Call to Action: Changing the Culture of Drinking at U.S. Colleges, outlining the state of alcohol mis- CollegeAIM use and prevention science in this area.4 The report included specific recommendations to help colleges and universities In the 10 years following the 2002 publication of A Call determine which strategies were most likely to produce to Action, there was an explosion of research on college alco- meaningful changes in alcohol use and consequences on hol use prevention. There were more than 151 studies pub- their campuses. The Task Force categorized strategies into lished just on individual-focused approaches between 2002 and 2012, compared with only 45 in all the years before one of four tiers, based on evidence of their effectiveness and 7-10 the nature of the evidence available. The strategies that met 2002. This exponential increase in the available science criteria for inclusion in Tier 1 had evidence of effectiveness prompted a re-evaluation of the Task Force recommenda- among college students and were individual-focused strat- tions: What did the science say about the effectiveness of egies shown to reduce high-risk drinking behavior and/or the recommended strategies now? What new strategies had negative drinking-related consequences. The strategies that been shown to be effective and should be added to the list? met criteria for inclusion in Tier 2 had evidence of success Was the information provided as part of the original recom- with general populations and could be applied to college mendations sufficient for colleges to effectively weigh their options, thus adequately supporting adoption and imple- environments, but had not been specifically tested with mentation of evidence-based approaches? college students. The multiple strategies assigned to Tier 2 NIAAA had these questions in mind when it commis- were all environmental in nature, targeting the student body sioned and oversaw creation of CollegeAIM, tapping the as a whole. Tier 3 strategies were defined as, and comprised, expertise of two teams of three researchers: a team at the strategies that had logical and theoretical promise but had University of Washington examining individual-focused not been fully evaluated. Tier 4 comprised strategies where strategies, and a team at the University of Minnesota exam- there was evidence of ineffectiveness. ining environmental-focused strategies. Both teams worked In 2004, NIAAA mailed the 2002 report to the president together to create a comprehensive list of the practical of every college and university in the United States and factors that colleges would likely want to consider when made it available at no cost to anyone who requested a print choosing an evidence-based approach, including amount copy. The report also was made available online on a ded- of research support, cost, and potential barriers to adoption icated website, www.collegedrinkingprevention.gov, along and implementation. Each team then reviewed the extant with a host of resources and supporting documentation. research in their area through 2012, rating each strategy In 2008, Nelson and colleagues assessed the influence of that met their inclusion criteria. For the individual-focused these dissemination efforts and found that 23% of colleges strategies, inclusion criteria required that a strategy had been were not employing any recommended Tier 1 or Tier 2 the subject of at least two peer-reviewed, randomized, con- strategies, and 45% were only employing a single recom- 5 trolled clinical trials. In addition, a strategy could only be mended strategy. Two-thirds of institutions surveyed rated on effectiveness if there were at least three trials. For offered a Tier 1 strategy (67%), but most did not report the environmental-focused strategies, ratings were based on implementing any recommended Tier 2 strategies. This review articles, when available, and all identified studies in suggests a trade-off between individual and environmental other areas. approaches. One possible reason for this is that environ- After the teams completed the ratings, they sent them mental approaches often are not self-contained within the to 10 leading experts within the alcohol prevention field campus and rely on building partnerships with local law for multiple rounds of peer review. The teams made edits enforcement, businesses within the community, community (e.g., adding specific studies from 2013 that would inform members, and lawmakers. It also is possible that the tier ratings and clarifying how ratings were applied) until they system created a false hierarchy, making individual strategies achieved consensus across the teams and reviewers. Thus, assigned to Tier 1 appear more effective than environmental CollegeAIM reflects the collective knowledge of 16 separate strategies assigned to Tier 2, simply because the latter had experts in the field (see Table 1), which makes it unique rel- not been tested specifically within college populations. This, ative to other summaries of the science. of course, was not the intent of the tier system, as stated in CollegeAIM is organized into two matrices, one summa- a report on college drinking research: “Central to the Task rizing individual-focused strategies and one summarizing Force findings was the recognition that successful interven- environmental-focused strategies, divided into levels of tions occur at three distinct levels . . . [that] must operate si- effectiveness and cost. Each matrix also has a companion multaneously to reach individual students, the student body table that offers more in-depth information on the specific as a whole, and the greater college community.”6 Thus, strategies. CollegeAIM also helps colleges consider both dissemination efforts need to adopt organizational structures individual and environmental strategies by including a that make readily apparent the importance of employing planning worksheet that facilitates a direct comparison of

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Table 1 CollegeAIM Contributors “see if any new, effective approaches might replace . . . existing strategies.”11 Information in the online version of Individual-Focused Strategies Team CollegeAIM directs users to outside resources that can assist • Jessica M. Cronce, Ph.D., assistant professor of psychiatry and with planning and taking action to adopt, implement, and behavioral sciences, School of Medicine, University of Washington evaluate a given strategy. Each of these steps is necessary • Jason R. Kilmer, Ph.D., associate professor of psychiatry and for effective campus prevention. Evaluation is of particular behavioral sciences, School of Medicine; assistant director importance, since local realities (e.g., differences in campus of health and wellness for alcohol and other drug education, and community culture, available staff) may influence how University of Washington effective a strategy actually is on a given campus. A college • Mary E. Larimer, Ph.D., professor of psychiatry and behavioral or university’s experience may diverge (for better or worse) sciences, School of Medicine; director, Center for the Study of Health from the effectiveness rating in CollegeAIM, which is based and Risk Behaviors; and professor, Department of Psychology, on the observed aggregate effect across the campuses and University of Washington communities where they were tested. Environmental-Focused Strategies Team • Kathleen Lenk, M.P.H., senior research fellow, Division of Individual-Focused Strategies Epidemiology and Community Health, School of Public Health, University of Minnesota CollegeAIM identified 14 strategies as having some ef- • Toben F. Nelson, Sc.D., associate professor of epidemiology and fectiveness in the individual-focused strategy matrices. Of community health, School of Public Health, University of Minnesota these, the researchers deemed 8 to have higher effectiveness, • Traci L. Toomey, Ph.D., professor of epidemiology and community based on the requirement that 75% or more of the studies health, School of Public Health, University of Minnesota evaluating a given strategy reported a reduction in alcohol use and/or alcohol-related consequences. Consistent with Independent Reviewers A Call to Action, the science supported multicomponent • David S. Anderson, Ph.D., professor of education and human alcohol skills training that includes information on what development; director, Center for the Advancement of Public Health, constitutes a standard drink, how to calculate and moderate George Mason University blood alcohol concentration through protective behavioral • Kate B. Carey, Ph.D., professor of behavioral and social sciences, strategies such as monitoring and setting limits on con- Center for Alcohol and Addiction Studies, School of Public Health, sumption, how alcohol outcome expectancies shape behav- Brown University ior following alcohol use, and how perceptions of other peo- • John D. Clapp, Ph.D., associate dean for research, College of Social ple’s drinking influences personal drinking. This approach is Work; director, Higher Education Center for Alcohol and Other Drug typified by the Alcohol Skills Training Program (ASTP),12 Misuse Prevention and Recovery, The Ohio State University which is generally delivered to small groups of students. • William DeJong, Ph.D., professor, School of Public Health, The ASTP was the precursor to the Brief Alcohol Screening Boston University and Intervention for College Students (BASICS),13 which • Mark S. Goldman, Ph.D., distinguished university professor of is the basis for the majority of current brief motivational psychology, University of South Florida interventions (BMIs). BMIs are generally one-on-one ses- • Ralph Hingson, Sc.D., M.P.H., director, Division of Epidemiology and sions facilitated by a professional in training (i.e., a graduate Prevention Research, NIAAA student in psychology) or professional (e.g., a master’s- or • Donald Kenkel, Ph.D., Joan K. and Irwin M. Jacobs professor of doctoral-level counselor) using personalized feedback sum- policy analysis and management, College of Human Ecology, marizing the student’s alcohol-related behaviors, beliefs, and Cornell University experiences to guide the conversation. Although limited • Robert F. Saltz, Ph.D., senior scientist, Prevention Research Center, research has examined whether undergraduate students Pacific Institute for Research and Evaluation (e.g., peer health educators) can deliver BMIs effectively, • Helene R. White, Ph.D., distinguished professor of sociology, Rutgers, results are generally favorable; however, there is not enough The State University of New Jersey evidence to conclusively determine the conditions under • Mark Wolfson, Ph.D., professor of social sciences and health policy, which peers are as effective as professionals. One factor that School of Medicine, Wake Forest University is thought to be central to the efficacy of BMIs is fidelity Note: Contributors are listed in alphabetical order by surname. Affiliations are current as of the to a motivational interviewing (MI) style,14 which requires launch of CollegeAIM in September 2015. Jessica M. Cronce, Ph.D., is now assistant professor of counseling psychology and human services, College of Education, University of Oregon. regular supervision and review of taped or audio-recorded sessions that have been rated for adherence to the therapeu- tic spirit and skills of MI. That said, four of the eight highly strategies along the various rated factors, both across and effective programs are delivered entirely remotely, in the within these two broad categories. Although CollegeAIM absence of an MI-trained facilitator. is largely a selection tool, institutions can use the planning Relative to BMIs, these nonfacilitated programs have worksheet to organize assessment of currently employed been found to be comparable on most outcomes,7 although prevention strategies. CollegeAIM urges stakeholders to in-person BMIs may hold an advantage over feedback-only

NIAAA’s College Alcohol Intervention Matrix | 45 FOCUS ON

programs in terms of reducing alcohol quantity and nega- work with community coalitions to ensure the drinking age tive consequences.15 Two of these four programs are con- is not lowered. Furthermore, retaining MLDA laws alone is sidered personalized feedback interventions (PFIs), which not sufficient; the MLDA must be enforced through mech- offer the feedback from a BASICS session delivered online, anisms such as underage compliance checks. Colleges can by email or text, or by mail. It is worth noting that some directly encourage local law enforcement agencies to regu- individual-focused strategies that would be considered larly conduct compliance checks at alcohol establishments PFIs are included as having “too few studies to rate effec- most likely to be frequented by their underage students. tiveness,” since only two studies had been published when Increasing taxes on alcohol sales, retaining a ban on Sunday CollegeAIM was launched. Given the success of generic alcohol sales (if applicable), and bans on happy hours or PFIs, as well as eCHECKUP TO GO (the only named and other price promotions are all policies enacted at the state commercially available PFI with higher effectiveness), more or local levels. Colleges can partner with other organizations research on these approaches is warranted. Another com- or coalitions that influence policymakers to implement or mercially named program rated as having higher effective- retain these policies. In addition, college representatives ness—AlcoholEdu for College—contains personalized feed- can talk individually with local bars and other venues near back but is not considered a PFI, because it incorporates a campus that serve alcohol and ask them to restrict happy number of other interactive elements that go beyond merely hours and other price promotions. Bars surrounding a cam- providing feedback. pus may attempt to attract students to their establishments The fourth remotely delivered program constitutes a by underbidding nearby competitors, which can create a single component of a PFI: correcting normative mispercep- dangerous situation that promotes heavy consumption (e.g., tions of peer alcohol use in relation to the individual’s own buying one drink and getting one for a discounted price, or alcohol use, that is, personalized normative feedback (PNF). promoting discounted shots). PNF in the form of birthday cards have been used to target 21st-birthday drinking, a known high-risk drinking event for many students; however, this use of PNF has had overall Conclusions lower effectiveness. The final two strategies rated as having demonstrated NIAAA developed CollegeAIM to offer colleges and higher effectiveness include goal/intention setting alone universities an array of evidence-based options to address and self-monitoring/self-assessment of drinking alone. alcohol use on their campuses. Because the evidence chang- Both of these strategies often are a part of the other strate- es with more scientific study, CollegeAIM is necessarily a gies listed above; however, like PNF, these are considered living document, and NIAAA has committed to updating it single-component interventions that, in the absence of every few years for the foreseeable future. The next update is other elements, decrease student drinking. As their names planned for the fall of 2018, reviewing literature published imply, the former involves helping students set goals or through December 2017. Campus stakeholders are encour- intentions that are contrary to high-risk drinking, while the aged to facilitate future iterations of CollegeAIM by ensur- latter requires students to complete a one-time assessment ing that evaluations of individual- or environmental-focused or longitudinal daily monitoring of their drinking behav- strategies on their campuses or in their communities make ior. Assessment is necessary to create the feedback used it into the published literature. Campus alcohol and drug for BMIs, PFIs, and PNFs, and creates an opportunity for prevention staff members could partner with graduate self-reflection that is thought to be amplified by the associ- students and faculty at their own or nearby institutions to ated feedback. conduct the evaluations and collaborate on the publications. Graduate students, in particular, may be a valuable resource, since they need data for theses and dissertations, and they Environmental-Focused Strategies may therefore be willing and able to contribute time to evaluate the strategies in exchange for use of the data. It is, CollegeAIM identified 19 strategies as having some de- of course, just as important to publish what doesn’t work as gree of effectiveness in the environmental-focused strategy what does. CollegeAIM also is meant to help colleges learn matrices. Of these, 5 were deemed to have high effective- what strategies are not effective, to avoid wasting resources. ness: retaining the minimum legal drinking age (MLDA) In sum, CollegeAIM is a user-friendly, interactive deci- of 21, enforcing the MLDA, increasing taxes on alcohol, sion tool based on a synthesis of the substantial and growing retaining a ban on Sunday alcohol sales, and enacting bans literature on campus alcohol use prevention, including strat- on happy hours and other price promotions. Retaining egies targeted at the individual and environmental levels. It the MLDA of 21 remains one of the most highly effective is designed to be a strategy selection tool; however, it also environmental interventions at the population level in offers resources to aid in strategy planning, implementation, terms of reducing alcohol consumption and alcohol-related and evaluation. The goal of CollegeAIM is to help colleges fatalities.16 Retaining the MLDA is beyond the control of and communities use their limited resources in the most any given college, but colleges can describe and promote cost-effective way possible. The hope is that by using a com- the existing evidence on the effectiveness of the MLDA and bination of effective individual- and environmental-focused

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strategies, colleges can create sustained reductions in risky 6. NIAAA, National Institutes of Health. What Colleges Need to Know Now: An Update on College Drinking Research. Bethesda, MD: U.S. Department of Health and alcohol use and related problems among their students. Human Services; November 2007. https://www.collegedrinkingprevention.gov/ media/1College_Bulletin-508_361C4E.pdf. Accessed July 31, 2017. 7. Cronce JM, Larimer ME. Individual-focused approaches to the prevention of college Acknowledgments student drinking. Alcohol Res Health. 2011;34(2):210-221. PMID: 22330220. This work was supported by NIAAA. 8. Larimer ME, Cronce JM. Identification, prevention and treatment: A review of individual-focused strategies to reduce problematic alcohol consumption by college students. J Stud Alcohol. 2002;(suppl 14):148-163. PMID: 12022721. Financial Disclosure 9. Larimer ME, Cronce JM. Identification, prevention, and treatment revisited: Individual-focused college drinking prevention strategies 1999–2006. Addict Behav. The authors declare that they have no competing 2007;32(11):2439-2468. PMID: 17604915. financial interests. 10. NIAAA, National Institutes of Health. CollegeAIM Alcohol Intervention Matrix: Individual-Level Strategies. Bethesda, MD: U.S. Department of Health and Human Services; 2015. https://www.collegedrinkingprevention.gov/CollegeAIM/ References IndividualStrategies/default.aspx. Accessed July 31, 2017. 11. NIAAA, National Institutes of Health. Planning Alcohol Interventions Using NIAAA’s 1. Johnston LD, O’Malley PM, Bachman JG, et al. Monitoring the Future National CollegeAIM Alcohol Intervention Matrix. Bethesda, MD: U.S. Department of Health Survey Results on Drug Use, 1975–2015. Vol 2. College students and adults and Human Services; 2015. https://www.collegedrinkingprevention.gov/CollegeAIM/ ages 19–55. Ann Arbor, MI: Institute for Social Research, University of Michigan Resources/NIAAA_College_Matrix_Booklet.pdf. Accessed July 31, 2017. 2016. http://monitoringthefuture.org/pubs/monographs/mtf-vol2_2015.pdf. Accessed July 31, 2017. 12. Baer JS, Marlatt GA, Kivlahan DR, et al. An experimental test of three methods of alcohol risk reduction with young adults. J Consult Clin Psychol. 1992;60(6):974- 2. Wechsler H, Molnar B, Davenport A, et al. College alcohol use: A full or empty glass? 979. PMID: 1460160. J Am Coll Health. 1999;47(6):247-252. PMID: 10368558. 13. Dimeff LA, Baer JS, Kivlahan DR, et al. Brief Alcohol Screening and Intervention for 3. Courtney KE, Polich J. Binge drinking in young adults: Data, definitions, and College Students (BASICS): A Approach. New York, NY: Guilford Press; determinants. Psychol Bull. 2009;135(1):142-156. PMID: 19210057. 1999.

4. Task Force of the National Advisory Council on Alcohol Abuse and Alcoholism, 14. Miller WR, Rollnick S. Motivational Interviewing: Helping People Change. New York, NY: National Institute on Alcohol Abuse and Alcoholism (NIAAA), National Institutes Guilford Press; 1992. of Health. A Call to Action: Changing the Culture of Drinking at U.S. Colleges. Bethesda, MD: U.S. Department of Health and Human Services; April 2002. 15. Carey KB, Scott-Sheldon LA, Elliott JC, et al. Face-to-face versus computer-delivered https://www.collegedrinkingprevention.gov/NIAAACollegeMaterials/publications/ alcohol interventions for college drinkers: A meta-analytic review, 1998 to 2010. calltoaction.aspx. Accessed July 31, 2017. Clin Psychol Rev. 2012;32(8):690-703. PMID: 23022767. 5. Nelson TF, Toomey TL, Lenk KM, et al. Implementation of NIAAA College Drinking Task 16. Wagenaar AC, Toomey TL. Effects of minimum drinking age laws: Review and analyses Force recommendations: How are colleges doing 6 years later? Alcohol Clin Exp Res. of the literature from 1960 to 2000. J Stud Alcohol. 2002;(suppl 14):206-225. 2010;34(10):1687-1693. PMID: 20626728. PMID: 12022726.

NIAAA’s College Alcohol Intervention Matrix | 47 THE COLLEGE ALCOHOL INTERVENTION MATRIX

CollegeAIM—the College Alcohol Intervention Matrix—is an easy-to-use and comprehensive resource to help schools address harmful and underage student drinking. Developed with leading college alcohol researchers and staff, CollegeAIM can help Planning schools choose interventions wisely—boosting Alcohol Interventions their chances for success and helping them

· National Institutee Using NIAAA’s on Alcohol Abus improve the health and safety of their students. AIM and Alcoholism COLLEGE CollegeAIM is distinctive because of the breadth of its research and analysis, the expertise of its contributors, and the convenience and accessibility of its presentation.

Download a free copy of CollegeAIM today at https://www.CollegeDrinkingPrevention.gov/CollegeAIM. ALCOHOL RESEARCH: Current Reviews High-Intensity Drinking

Megan E. Patrick and Beth Azar Megan E. Patrick, Ph.D., is a research associate professor Binge drinking thresholds have long been set at four or more drinks for women and at the University of Michigan five or more drinks for men over the course of a few hours. However, a significant Institute for Social Research, number of people regularly consume much higher amounts of alcohol: double Ann Arbor, Michigan. or even triple the standard binge drinking threshold. Researchers have begun to distinguish between typical binge drinking and this kind of “high-intensity drinking,” Beth Azar, M.A., is a science which is common among certain types of binge drinkers and is often associated with special occasions, including holidays, sporting events, and, notably, 21st birthdays. To writer for Alcohol Research: understand the social and physical influences of alcohol consumption, it is important Current Reviews. for researchers to set standard definitions for high-intensity drinking and distinguish it from other types of alcohol use.

Key words: Alcohol consumption; binge drinking; college drinking; drinking occasions; drinking patterns; heavy drinking; high-intensity drinking

Consuming alcohol until drunk by summarizes the most recent research for differences in metabolism related guzzling beers, slamming shots, and on high-intensity drinking. to body mass, age, and other factors.5,6 taking swigs from bottles of booze is In fact, Pearson and colleagues7 point common fare in movies and on televi- out that average-weight women (about sion, which often portray people Defining High-Intensity Drinking 163 lbs.) and men (about 190 lbs.)8 drinking to extremes. One study, pub- in the United States would not reach lished in the British Medical Journal, In the early 1990s, the College legal intoxication after consuming 4/5 calculated that James Bond, of book Alcohol Study first applied the term drinks in 2 hours. and movie fame, drank about 45 “binge drinking” to the pattern of Meanwhile, research indicates that drinks a week.1 In the 2006 movie drinking 4+/5+ drinks in a row during a substantial portion of binge drinkers 2 Casino Royale, Bond slugged down a the past 2 weeks. Drinking to this often drink at levels two or three times stunning 20 drinks just before a high- extent became a commonly used mea- the 4+/5+ binge threshold, suggesting speed car chase that left him in the sure of increased risk of alcohol-related the need for another term and clear hospital for 2 weeks. Researchers typi- problems. In 2004, the National definition for this heavier binge drink- cally define binge drinking as four or Institute on Alcohol Abuse and ing.9 Although some articles have used more drinks in a sitting for women Alcoholism (NIAAA) evaluated and the term “extreme binge drinking,”10 and five or more for men (4+/5+). approved defining binge drinking as the field is moving toward the term Due to evidence that some people, like 4+/5+ drinks in about 2 hours, because “high-intensity drinking” as the most the fictitious Bond, drink far above it typically leads to a blood alcohol accurate way to talk about this level of that cutoff, researchers have begun dis- concentration (BAC) of .08 g/dL, the alcohol use.11 tinguishing between typical binge legal cutoff for driving in the United There is no firm consensus on drinking and this kind of “high-inten- States.3 One advantage of the defini- exactly how many drinks qualify as sity drinking.” They have developed tion has been its use in many studies, high-intensity drinking. However, new definitions and have begun exam- making results comparable. However, researchers working in this relatively ining the special challenges of measur- this definition does not distinguish new area have coalesced around the ing high-intensity drinking, the fre- between drinking levels at or just above concept of at least twice the typical quency with which it occurs, when it this binge threshold and those that far binge drinking threshold (i.e., 10+ is most likely to occur and in which exceed it. It also assigns the same level drinks)10 or twice the gender-specific populations, and the consequences of of risk to everyone who crosses the binge threshold (i.e., 8+ for women/ this kind of drinking to the drinker threshold, regardless of how far beyond 10+ for men).9,12 Even using a more and to the community. This article it they go.4 And it does not account conservative measure of just two more

High-Intensity Drinking | 49 drinks over the typical binge drinking How Common Is drinks in a row.10,14 Those rates are cutoff (6+/7+ drinks), Read and col- High-Intensity Drinking? even higher among college students. leagues found significant differences Patrick and Terry-McElrath reported when comparing what they called To date, only a handful of binge- that 19- to 20-year-olds who attended “heavy binge drinkers” with typical drinking studies distinguish levels 4-year colleges and did not live with binge drinkers.13 Specifically, heavy of use above binge drinking at the their parents were significantly more binge drinkers typically got drunk- 4+/5+ rate. But those that do, find that likely to engage in high-intensity binge er than those closer to the standard a significant percentage of teens and drinking than other young adults: binge cutoff; when comparing both young adults engage in high-intensity 12.4% of college students consumed drinking at levels that far exceed that 10+ drinks, and 5.1% consumed binge drinking groups with drinkers cutoff. For example, according to stud- 15+ drinks, compared with 9% and who did not binge drink, only heavy ies reporting on data from the national 3.5% of 19- to 20-year-olds not binge drinkers differed significantly. Monitoring the Future (MTF) survey attending college (see Figure 1).14 In this study, compared with drinkers of high school students and young In a separate study using MTF data in either of the other categories, heavy adults, approximately 10% of U.S. to examine the developmental course binge drinkers reported, on average, 12th-grade high school students and of high-intensity drinking, Patrick and three additional unique types of conse- U.S. 19- and 20-year-olds reported colleagues found that high-intensity quences in the previous year, including consuming 10 or more drinks in a drinking peaks around age 21, and impaired control, risk behaviors, aca- row at least once in the previous 2 that the peak tends to be highest for demic or occupational consequences, weeks, and an additional 4% to 5% young adults who attend college.15 and . reported consuming 15 or more Another study found that, among a

5+ drinks 40 10+ drinks 15+ drinks 35 Moderate/high intoxication Sustained intoxication 30

25

20

15

10

5 Percentage of 19- to 20-year-olds to 19- of Percentage 0 Full time Full time Not attending Part time/other (2-year college) (4-year college) Total sample College status

Figure 1 College versus noncollege high-intensity drinking patterns. Young adults who attend a 4-year college full time are more likely to report engaging in high-intensity drinking and binge drinking during the previous 2 weeks than drinkers who do not attend college, attend a 2-year college, or attend college part time. Full-time students at 4-year colleges are also more likely to say that they usually attain moderate/high and sustained intoxication when they drink. Source: Figure adapted from Table 1 and Table 3 in Patrick ME, Terry-McElrath YM. High-intensity drinking by underage young adults in the United States. Addiction. 2017;112(1):82-93.

50 | Vol. 39, No. 1 Alcohol Research: Current Reviews sample of 10,424 college freshmen at Surveillance System.18 During their for Substance Abuse Treatment defines 14 schools, roughly 20% of males re- most recent binge drinking episode, binge drinking for older adults as four ported consuming 10 or more drinks, 70% of respondents said they con- or more drinks per occasion for both and 10% of females reported con- sumed 6 or more drinks, 38.4% con- women and men.23 If that is indeed suming 8 or more drinks at least once sumed 8 or more drinks, and 16.9% the case, high-intensity drinking may in the 2 weeks preceding the survey.9 consumed 11 or more drinks. Highest be more common among older adults Using the gender-specific high-inten- consumption was for respondents ages than is currently reported. Parikh and sity drinking cutoff of 8+/10+, Patrick 18 to 24, who reported drinking an colleagues calculated that almost 10% and colleagues found that, among a average of 9.5 drinks during a binge of a group of 4,815 participants age group of 342 college students followed drinking episode. Average amounts for 65 and older reported drinking above during four 2-week periods over the ages 25 to 34, 35 to 44, 45 to 54, and the 4+/5+ threshold over the previous course of a school year, 67% reported 55 and older were 8.0, 7.4, 7.4, and 30 days.22 To tease apart the rates of high-intensity drinking on at least one 6.7, respectively. high-intensity drinking, it will be criti- day, and 16.1% of 5,467 drinking What constitutes high-intensity cal for studies to use agreed-upon age- days recorded were high-intensity drinking may depend on who is drink- group thresholds for binge drinking drinking days.12 These high-intensity ing. It is largely established that the and high-intensity drinking. drinking days were associated with binge threshold for women should be negative consequences, such as injury, lower than for men, because women unplanned sex, and aggression. become more intoxicated than men Ritualized High-Intensity In addition, Wave 2 data from when consuming the same amount Drinking the National Epidemiologic Survey of alcohol (even when they weigh the on Alcohol and Related Conditions same). Research also suggests that Many studies find that people inten- (NESARC) reported that 13% of alcohol affects adolescents and young sify their drinking to celebrate special 18- to 20-year-olds drank 15 or more adults differently from adults. The occasions and to bond with friends drinks at some point in the previous brain undergoes significant growth and during holidays. As with much of the year, and 3% did so every 2 weeks.16 change well into young adulthood. binge-drinking research, most of the Among the 3,718 young adults fol- Due to developing brain function, studies examining when people are lowed in the MTF analysis by Patrick adolescents may be less sensitive to most likely to engage in high-intensity and colleagues, those who engaged in alcohol’s behavioral effects, such as drinking revolves around college stu- high-intensity drinking not only drank a staggering walk or sedation. At the dents. In a study examining the drink- more per occasion than typical binge same time, teens may be more recep- ing patterns across the seasons among drinkers, but they more often engaged tive to the social-interaction effects of 462 university students, Schuckit and in all levels of binge and high-intensity alcohol, including feeling more social colleagues found that maximum drinks drinking than those who only reported and having more fun with friends.6 per occasion increased 18% around binge drinking.15 In addition, adolescents have been the time of a popular 1-day campus Although high-intensity drinking shown to reach a BAC of .08 with spring festival, decreased 29% over appears to peak in the early 20s, it does fewer drinks.19 Studies in animals and the summer, and increased another not disappear. Terry-McElrath and humans suggest that binge doses of al- 31% as school resumed in the fall, Patrick recently reported that 12.4% cohol have more severe and potentially suggesting that alcohol consumption of young adults ages 25 and 26 report- permanent effects on adolescent brains by college students is highly influ- ed drinking 10 or more drinks in a row and can more readily lead to addic- enced by annual rhythms and social at least once in the previous 2 weeks.17 tion.20,21 As for older adults, studies context.24 Expanding beyond college This type of high-risk drinking was suggest that people over age 60 me- students, Bellis and colleagues found most common in people who were tabolize alcohol more slowly and are that estimates of average weekly drink- male, white, unmarried, employed, at higher risk of alcohol-related health ing among all drinkers in England in- nonparents, and who were alcohol us- problems.22 Although most studies use creased by nearly a quarter—from 13.6 ers during high school. the standard 4+/5+ definition of binge to 17.1 units per person per week— Among people who report binge drinking for all ages, this evidence sug- when they included survey questions drinking, consuming well in excess of gests that such a threshold may more on special occasion consumption.25 the five-drink threshold is the norm. accurately represent high-intensity Indeed, research finds that there Naimi and colleagues examined data drinking among older adults. Indeed, are occasions when high-intensity from the 14,143 adult binge drinkers some organizations have begun to rec- drinking is much more likely. Not sur- who responded to the 2003–2004 ommend that binge drinking thresh- prisingly, on and off college campuses, binge drinking module of the nation- olds be lowered for older adults. A drinking tends to peak on Fridays and ally conducted Behavioral Risk Factor consensus panel created by the Center Saturdays and is particularly high on

High-Intensity Drinking | 51 holidays such as the Fourth of July weekend, and students consumed an of female and 79% of male birthday and New Year’s Eve.26-29 Research on average of 8.2 drinks compared with a drinkers reached the legal limit of .08 event-specific drinking has indicated more typical 5.3 drinks.37 or higher; 35% of female and 49% of particularly high quantities of alcohol male birthday drinkers drank enough consumed surrounding collegiate Sporting Events to have eBACs of 0.26 or higher (a sporting events,30,31 spring break,32-34 level associated with potentially serious Sporting events are also associated and to celebrate 21st birthdays (at least medical outcomes). Another study 35,36 with particularly heavy drinking. One in the United States). suggests that birthday drinking is not study found that men, though not 42 women, drink more on Super Bowl without consequences. In Ontario, Holidays Sunday than on a typical Saturday.38 Canada, where the legal drinking age And among college football fans, is 19, hospital admissions data for Predictably, people tend to drink everyone ages 12 to 30 showed that more on certain holidays. However, particularly men, drinking on days of high-profile football games is as heavy alcohol-related hospital admissions increases in high-intensity drinking more than doubled during a person’s may depend on the holiday in ques- as alcohol consumption on other well- known drinking days, including New 19th-birthday week, compared with tion. For example, within a sample 31 other times during the year. of 576 young adults ages 18 and 19, Year’s Eve and Halloween weekend. In another study, Merlo and colleagues At least among college students, both in college and not, Goldman where most of the research on 21st and colleagues demonstrated that found high rates of heavy drinking, measured as a BAC of .08 or higher, birthdays takes place, the heaviest on family-oriented holidays such as drinking is associated with several Thanksgiving and Christmas, the among 466 tailgaters prior to football factors, including overestimating number of young people who con- games at two large universities: 40.2% of tailgaters at one school and 31.9% how much one’s peers drink during sumed alcohol increased but the 39 average number of drinks consumed at the other. In general, studies find 21st-birthday celebrations, drinking per person (counting only those who that athletes as well as sports fans shots, playing drinking games, cele- drank) actually decreased.27 In con- are more likely than nonathletes and brating with influential peers, and en- trast, on holiday weeks that included non–sports fans to engage in binge and gaging in 21st-birthday traditions such high-intensity drinking and to have a as free drinks at bars.43,44 a Halloween-like holiday, New Year’s 30,40,41 Eve, and the Fourth of July, the aver- heavy-drinking style. age number of drinks consumed per Spring Break drinker increased significantly com- 21st Birthdays College student spring break is a pared with nonholiday weeks. Because highly anticipated time of the year In the United States, according to the researchers measured drinks per when some college students intend to week, they could not estimate rates a number of studies, the day young adults become old enough to drink drink excessively. Studies find that col- of daily high-intensity drinking. lege students who travel with friends However, another study of 1,124 col- legally is a day they often take very dramatically increase their alcohol use lege students found that, compared high risks with their drinking. In fact, and face more alcohol-related conse- with a typical nonholiday weekend, more than 80% of study participants more students consumed alcohol and drink on their 21st birthdays,35,36 and quences, but those who stay home or vacation with their parents tend to reached higher BACs on their 21st many drink far more than typical 32,33,45 birthdays, New Year’s Eve, New Year’s binge drinking. In a survey of 2,518 drink moderately or not at all. Day, the Fourth of July, spring break, college students, for example, Rutledge For students who do drink during and graduation.29 and colleagues reported that 4 out of spring break, their drinking is posi- As these data suggest, there is some 5 study participants drank alcohol to tively associated with alcohol-related evidence that, at least for young adults, celebrate, drinking an average of 12.6 consequences, including having a high-risk drinking is more likely drinks.36 Moreover, 12% of male and hangover, , and being injured 34 during holidays that are centered on female birthday drinkers reported con- as a result of drinking. And, as with friends as opposed to family. Lefkowitz suming 21 drinks, and an additional the risk of binge drinking, alcohol- and colleagues examined drinking 22% of men and 12% of women re- related consequences are more likely if during a student-created holiday and ported that they drank more than 21 students travel: 32% of travelers and found that more students drank, and drinks. An estimate of blood alcohol 22% of nontravelers reported having students drank significantly more than content (eBAC) suggested that well a hangover, 23% of travelers and 15% they did on several typical weekend more than half of birthday drinkers of nontravelers reported being sick to days: 51% of students consumed alco- drank enough to raise their BAC to their stomach or vomiting, and 7.5% hol compared with 29% on a typical dangerous levels. Specifically, 68% of travelers and 4% of nontravelers

52 | Vol. 39, No. 1 Alcohol Research: Current Reviews reported being injured as a result related outcomes.49 Specifically, overall drinking levels and overall rates of drinking.34 students who binge drank three of consequences. Neal and Fromme In a longitudinal study of 651 or more times in a 2-week period attempted to assess whether alcohol freshmen undergraduate students, were twice as likely as students who consumption could be directly asso- Patrick and colleagues confirmed binge drank once or twice in the ciated with specific behavioral conse- the findings that binge drinking and same time period to experience quences by asking college students to negative consequences of drinking are alcohol-induced memory losses monitor their behavior over 30 days.31 common during spring break.46 They (27% vs. 54%), to not use protection Their analysis included data from also discovered that previous drinking during sex (10% vs. 20%), to engage 691 women and 422 men on a total behavior was among the strongest pre- in unplanned sex (22% vs. 42%), and of 30,224 days. They concluded that, dictors of alcohol consumption during to be injured (11% vs. 27%). Both on a global level, average BAC was spring break. In addition, students groups were at a 1% risk of needing significantly correlated with illicit drug were more likely to get drunk and medical treatment for an overdose. use, drinking and driving, engaging experience negative consequences of As mentioned earlier, students who in sexual behavior, having unsafe sex, drinking if, before spring break, they binge drink regularly drink well over being the victim of coerced sex, being and their friends agreed they would get the typical binge threshold, making the perpetrator of coerced sex, acting drunk. And although students going it difficult to determine, at a popu- aggressively, and gambling. Their on trips with friends were more likely lation level, whether the increase in analysis also found strong event-level to have these kinds of understandings, risk associated with frequent binging associations between BAC and several even students who did not go on trips results from the number of binge behavioral risks, with the strongest had understandings with their friends episodes per se, or from the number 4 correlations for vandalism, and the about drinking. These findings suggest of drinks consumed in an episode. weakest for aggressive behavior and that the relative freedom of spring Wechsler and Nelson concluded that, unsafe sex. They estimated that every break provides many students with the for individuals, the odds of experi- .01 increase in BAC was associated opportunity to experiment with alco- encing alcohol-related harms rise as with a 4% to 12% increase in the risk hol use. Litt and colleagues also found their level of alcohol consumption of engaging in these behaviors. Those increases.50 Mundt and colleagues that whether or not students were numbers become significant when peo- willing to engage in high-risk drinking reported that, among 2,090 college ple engage in high-intensity drinking, during spring break—drinking enough students, having an alcohol-related in- which can increase BAC quickly in a to black out or pass out—predicted jury became 19% more likely for men short amount of time. whether they followed through.47 with each additional day of consum- ing 8 or more drinks and 10% more Several studies indicate that college likely for women drinking 5 or more students who engage in high-intensity Consequences of drinks.51 Read and colleagues also drinking are motivated in large part High-Intensity Drinking found that when they distinguished by the expectation that it will lead between nonbinge drinkers, binge to positive consequences, including High-intensity drinking is of par- drinkers (4+/5+), and heavy binge being more social and having fun ticular concern because of the adverse drinkers (6+/7+) in a sample of 356 with friends. And these positive con- consequences associated with it. These college students, only the heavy binge sequences may outweigh any potential consequences include alcohol-related drinkers differed significantly from negative consequences. In a longitu- injuries, alcohol poisoning, risky sex- the nonbinge drinkers on measures of dinal study that surveyed 342 college ual behavior, vomiting, passing out, alcohol-related consequences, includ- students over a total of 4,645 days, blacking out, and long-term harm ing blacking out, impaired control, Patrick and colleagues found that to academic or occupational status. and alcohol dependence symptoms.13 students, in fact, both expected and Although this article focuses on alco- In a sample of 115 young adults, experienced more positive conse- hol’s short-term consequences, some Jackson found that a threshold of 10 quences on days that they engaged in studies have begun to show long-term or more drinks was most predictive high-intensity drinking.12 Students also effects of binge drinking. For example, of hangover when examining the expected and experienced more neg- longitudinal MTF data links binge relationship between alcohol-related ative consequences on high-intensity drinking at age 18 to higher incidence consequences and different drinking drinking days. Furthermore, the of alcohol abuse disorder at age 35.46,48 thresholds (from 1+ to 15+ drinks per positive consequences were rated as One study with a cohort of 15,000 occasion).52 better and the negative consequences college students concluded that the Much of the research on the adverse were rated as worse on high-intensity overall frequency of binge drinking consequences of consuming alcohol drinking days. Students may be moti- increases the risk of negative alcohol- examines global associations between vated by the positive consequences and

High-Intensity Drinking | 53 accept the negative consequences as (e.g., 8+/10+ and 12+/15+ drinks for publications/Newsletter/winter2004/Newsletter_ part of the drinking experience. women/men) and to include effects Number3.pdf. Accessed July 13, 2017. of age in relevant analyses. Indeed, 4. White A, Hingson R. The burden of alcohol use: Excessive alcohol consumption and related high-intensity drinking behavior consequences among college students. Alcohol Res. Self-Report of is particularly dangerous for teens, 2013;35(2):201-218. PMID: 24881329. whose brains are still developing and High-Intensity Drinking 5. Cederbaum AI. Alcohol metabolism. Clin Liver Dis. who may be more vulnerable to de- 2012;16(4):667-685. PMID: 23101976. When studying binge drinking, or veloping alcohol use disorder. 6. Spear LP. Adolescents and alcohol: Acute sensitivities, any type of alcohol consumption, it is Future research in this area should enhanced intake, and later consequences. critical that researchers have access to focus on the initiation and progres- Neurotoxicol Teratol. 2014;41:51-59. PMID: an accurate and straightforward meth- sion of high-intensity drinking.11 24291291. od for measuring how much alcohol Additional research is also needed 7. Pearson MR, Kirouac M, Witkiewitz K. We still question people ingest. Most studies rely on to determine whether existing pre- the utility and validity of the binge/heavy drinking self-reports, although questions have vention approaches are effective at criterion. Addiction. 2016;111(10):1733-1734. PMID: been raised about how valid those reducing high-intensity drinking, or 27137172. reports are at high quantities of alco- whether more prevention and inter- 8. Ogden CL, Fryar CD, Carroll MD, et al. Mean body hol. Recently, studies that compare vention programs are needed to ad- weight, height, and body mass index, United States 11,16 1960–2002. Adv Data. 2004;347:1-17. https:// self-reports with biological measures of dress this more extreme behavior. www.cdc.gov/nchs/data/ad/ad347.pdf. Accessed alcohol consumption have determined Understanding who is most likely December 22, 2016. that self-reports are a valid way to as- to engage in high-intensity drinking 9. White AM, Kraus CL, Swartzwelder H. Many college 53 sess alcohol consumption. That said, and when and where that drinking freshmen drink at levels far beyond the binge some evidence suggests that self-report occurs will help design prevention threshold. Alcohol Clin Exp Res. 2006;30(6):1006- data break down after people consume programs to specifically target this 1010. PMID: 16737459. large amounts of alcohol. Northcote behavior. 10. Patrick ME, Schulenberg JE, Martz ME, et al. Extreme and Livingston, for example, found binge drinking among 12th-grade students in the United States: Prevalence and predictors. JAMA that young adults accurately estimated Pediatr. 2013;167:1019-1025. PMID: 24042318. their alcohol consumption when it was Acknowledgments 11. Patrick ME. A call for research on high-intensity light or moderate but underestimated alcohol use. Alcohol Clin Exp Res. 2016;40(2):256- 54 This study was funded by support it after eight or more drinks. These 259. PMID: 26842244. discrepancies may result from a combi- from NIAAA (R01-AA- 023504 to Dr. Patrick). The content here 12. Patrick ME, Cronce JM, Fairlie AM, et al. Day-to-day nation of intoxication interfering with variations in high-intensity drinking, expectancies, memory and a desire to provide a more is solely the responsibility of the and positive and negative alcohol-related socially acceptable response. authors and does not necessarily consequences. Addict Behav. 2016;58:110-116. represent the official views of the PMID: 26922158. sponsors. 13. Read JP, Beattie M, Chamberlain R, et al. Beyond Conclusions the “binge” threshold: Heavy drinking patterns and their association with alcohol involvement indices in Financial Disclosure college students. Addict Behav. 2008;33(2):225-234. Research has established that PMID: 17997047. high-intensity drinking is relatively common, especially among teens and The authors declare that they have 14. Patrick ME, Terry-McElrath YM. High-intensity drinking no competing financial interests. by underage young adults in the United States. young adults, and it appears to peak Addiction. 2017;112(1):82-93. PMID: 27514864. around age 21. These findings suggest 15. Patrick ME, Terry-McElrath YM, Kloska DD, et al. 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J Am Coll Health. 23404667. No. 26. Rockville, MD: U.S. Department of Health and 2005;54(2):76-80. PMID: 16255318. Human Services; 1998. https://www.ncbi.nlm.nih. 48. Schulenberg JE, Patrick ME, Kloska DD, et al. gov/books/NBK64419. Accessed July 14, 2017. 36. Rutledge PC, Park A, Sher KJ. 21st birthday Substance use disorder in early midlife: A national drinking: Extremely extreme. J Consult Clin Psychol. prospective study on health and well-being correlates 24. Schuckit MA, Smith TL, Clausen P, et al. Drinking 2008;76(3):511-516. PMID: 18540744. patterns across spring, summer, and fall in and long-term predictors. Subst Abuse. 2016;9(suppl 462 university students. Alcohol Clin Exp Res. 37. Lefkowitz ES, Patrick ME, Morgan NR, et al. State 1):41-57. PMID: 27257384. Patty’s Day: College student drinking and local 2016;40(4):889-896. PMID: 27038597. 49. Wechsler H, Nelson TF. What we have learned from crime increased on a student-constructed holiday. J the Harvard School of Public Health College Alcohol 25. Bellis MA, Hughes K, Jones L. Holidays, celebrations, Adolesc Res. 2012;27(3):323-350. PMID: 22685369. and commiserations: Measuring drinking during Study: Focusing attention on college student alcohol feasting and fasting to improve national and 38. Dearing RL, Twaragowski C, Smith PH, et al. Super consumption and the environmental conditions that individual estimates of alcohol consumption. BMC Bowl Sunday: Risky business for at-risk (male) promote it. J Stud Alcohol Drugs. 2008;69(4):481- Med. 2015;13:113. PMID: 25998218. drinkers? Subst Use Misuse. 2014;49(10):1359- 490. PMID: 18612562. 1363. PMID: 24621086. 26. Del Boca FK, Darkes J, Greenbaum PE, et al. Up close 50. Wechsler H, Nelson TF. Binge drinking and the and personal: Temporal variability in the drinking of 39. Merlo LJ, Ahmedani BK, Barondess DA, et al. Alcohol American college student: What’s five drinks? individual college students during their first year.J consumption associated with collegiate American Psychol Addict Behav. 2001;15(4):287-291. PMID: football pre-game festivities. Consult Clin Psychol. 2004;72(2):155-164. PMID: Drug Alcohol Depend. 11767258. 15065951. 2011;116(1-3):242-245. PMID: 21288661. 51. Mundt MP, Zakletskaia LI, Fleming MF. Extreme college 40. Nelson TF, Wechsler H. School spirits: Alcohol and 27. Goldman MS, Greenbaum PE, Darkes J, et al. How drinking and alcohol-related injury risk. Alcohol Clin many versus how much: 52 weeks of alcohol collegiate sports fans. Addict Behav. 2003;28(1):1- Exp Res. 2009;33(9):1532-1538. PMID: 19485974. consumption in emerging adults. Psychol Addict 11. PMID: 12507523. 52. Jackson KM. Heavy episodic drinking: Determining Behav. 2011;25(1):16-27. PMID: 21219038. 41. Veliz P, McCabe SE, Boyd CJ. Extreme binge drinking the predictive utility of five or more drinks.Psychol 28. Kushnir V, Cunningham JA. Event-specific drinking among adolescent athletes: A cause for concern? Am Addict Behav. 2008;22(1):68-77. PMID: 18298232. in the general population. J Stud Alcohol Drugs. J Addict. 2016;25(1):37-40. PMID: 26688434. 2014;75(6):968-972. PMID: 25343654. 42. Callaghan RC, Sanches M, Gatley JM, et al. 53. Simons JS, Wills TA, Emery NN, et al. Quantifying 29. Neighbors C, Atkins DC, Lewis MA, et al. Event-specific Hazardous birthday drinking among young people: alcohol consumption: Self-report, transdermal drinking among college students. Psychol Addict Population-based impacts on emergency department assessment, and prediction of dependence Behav. 2011;25(4):702-707. PMID: 21639597. and in-patient hospital admissions. Addiction. symptoms. Addict Behav. 2015;50:205-212. PMID: 2014;109(10):1667-1675. PMID: 25047919. 26160523. 30. Green K, Nelson TF, Hartmann D. Binge drinking and sports participation in college: Patterns 43. Brister HA, Wetherill RR, Fromme K. Anticipated versus 54. Northcote J, Livingston M. Accuracy of self-reported among athletes and former athletes. Int actual alcohol consumption during 21st birthday drinking: Observational verification of “last Rev Sociol Sport. 2014;49(3/4):417-443. celebrations. J Stud Alcohol Drugs. 2010;71(2):180- occasion” drink estimates of young adults. Alcohol. doi:10.1177/1012690213509257. 183. PMID: 20230714. 2011;46(6):709-713. PMID: 21949190.

High-Intensity Drinking | 55

NIAAA Spectrum Volume 9, Issue 3

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Visit https://www.spectrum.niaaa.nih.gov. ALCOHOL RESEARCH: Current Reviews

Gender Differences in Binge Drinking

Prevalence, Predictors, and Consequences

Richard W. Wilsnack, Sharon C. Wilsnack, Gerhard Gmel, and Richard W. Wilsnack, Ph.D., Lori Wolfgang Kantor is a professor emeritus in the Department of Psychiatry and Just as binge drinking rates differ for men and women, the predictors and conse- Behavioral Science, University of quences of binge drinking vary by gender as well. This article examines these dif- North Dakota School of Medicine ferences and how binge drinking definitions and research samples and methods and Health Sciences, Grand may influence findings. It also describes the relationship between age and binge Forks, North Dakota. drinking among men and women, and how and environment affect this relationship. It examines gender-specific trends in binge drinking, predictors of Sharon C. Wilsnack, Ph.D., is binge drinking for men and women, and binge drinking in the context of smoking. The the Chester Fritz Distinguished article reviews current findings on gender differences in the health consequences of binge drinking, including morbidity and mortality, suicidality, cancer, cardiovascular Professor in the Department disorders, liver disorders, and brain and neurocognitive implications. It also discusses of Psychiatry and Behavioral gender differences in the behavioral and social consequences of binge drinking, Science, University of North including alcohol-impaired driving, sexual assault, and intimate partner violence, and Dakota School of Medicine and includes implications for treatment and prevention. Health Sciences, Grand Forks, North Dakota. Key words: Alcohol and other drugs (AODs); AOD associated consequences; binge AOD use; gender differences; physical health; predictive factors Gerhard Gmel, Ph.D., is a pro- fessor, University of Lausanne, and is affiliated with the Alcohol Introduction disorder).5,6 In this article we review Treatment Center, University of recent research findings on gender dif- Lausanne Hospital, Lausanne, A large research literature shows ferences in the prevalence, predictors, Switzerland. He is also an invited that women consistently consume less and consequences of binge drinking, professor, University of the alcohol than men, and they experience and we note how interpretation of West of England, Bristol, United fewer social problems resulting from these findings has been limited by dif- Kingdom. drinking than men, but these gender ferences in concepts, measurements, differences vary culturally, demograph- and research methods. Lori Wolfgang Kantor, M.A., ically, and historically.1-3 This literature is a science writer at CSR, often has not given close attention to Incorporated. gender differences in binge drinking Measurement Issues and its consequences. This lack of at- tention is unfortunate, because binge There is considerable variation drinking is recognized as a major con- in the research literature as to tributor to the social and health bur- how binge drinking is measured dens of alcohol consumption.4 Binge (4+, 5+, 6+ drinks) and labeled (binge drinking has been linked specifically to drinking, heavy episodic drinking, a wide variety of adverse consequences, or risky single-occasion drinking).7-10 acute (e.g., accidents and injuries) and Furthermore, many studies use gender- chronic (e.g., liver disease), that harm specific measures of binge drinking not only the drinker but also commu- (e.g., 5+ drinks for men and 4+ drinks nities and societies as a whole (e.g., for women),11 but many other studies productivity losses, crime, and public use the same measure for men and

Gender Differences in Binge Drinking | 57 women (e.g., the Alcohol Use ways and over various periods of time, cific drinking culture and environment Disorders Identification Test uses the gender difference persists, whether where the binge drinking occurs. 6+ drinks).12-16 Other studies define or not studies use gender-specific binge drinking by estimated blood criteria for defining binges. Another alcohol concentration (BAC) level analysis of data from 15 countries Gender-Specific Trends (e.g., a BAC of at least .08%), which reached a similar conclusion.34 may be a less sensitive criterion for However, binge drinking rates and Complex age effects are one reason men than for women.17 gender differences vary greatly across why it is difficult to evaluate trends in Finally, different studies measure populations. One explanation of the women’s and men’s binge drinking. different frequencies of binge drink- difference is that recent changes in Much of the research and discussion of ing over different time periods (e.g., binge drinking have not yet erased the those trends focuses on two questions: in the past 2 weeks or past 30 days). sizable gender gap present in many 1. Is binge drinking changing (in Measuring the frequency of binge societies. A second explanation is that recent years) in ways that differ drinking in a given time period (e.g., gender differences in binge drinking by gender? once in the past 30 days) may pro- cannot be attributed only to biological 2. Are gender-differentiated changes duce greater apparent gender differ- or cultural differences but may leading to a convergence of men’s ences than measuring binge drinking result from a combination of these 3 and women’s rates of binge as any or none. Moreover, using influences. drinking? longer time periods for measurement In the mass media, the common (e.g., a year versus a month) may re- Age duce gender differences when binge answers to these questions are that drinking is measured as any or none One response to these explanations women’s binge drinking is increasing but may magnify gender differences has been concern that gender differ- faster than men’s, and, as a result, when binge drinking frequency is ences in binge drinking may be dis- men’s and women’s binge drinking measured. Because of the inconsistent appearing specifically among younger rates are converging. measurement methods used across drinkers. In the United States, binge Research to answer these questions the research, we cannot focus our drinking is most prevalent in late ado- is hard to interpret for many reasons discussion on any one criterion of lescence or early adulthood, with rates besides age effects. In addition to quantity, frequency, or time period. declining as drinkers grow older.35 the variation in how binge drinking However, for examination of the con- However, a focus on binge drinking in is measured, some analyses of binge sequences of acute and chronic binge any one age group may be an oversim- drinking rates include abstainers, drinking, the importance of measure- plification, for several reasons: whereas others do not. Some studies ment variation remains uncertain. • Women’s binge drinking has not analyze changes in binge drinking fre- caught up with men’s in any age quency, whereas others analyze chang- group in the United States or any es in rates of ever/never binge drink- Prevalence other country, judging from large, ing. Furthermore, many studies that general-population surveys. measure trends over extended periods There has been widespread alarm do not separate period effects (histori- in the mass media about the extent of • As drinkers get older, binge drink- cal trends in whole populations) from women’s binge drinking. A frequent ing (versus none) declines consis- age effects (changes that occur more theme is that, traditionally, men have tently in Europe, North America, in one age group than others) and been binge drinkers more than wom- Australia, and New Zealand, but cohort effects (changes that are greater en, but this gender difference is de- these declines do not occur consis- in groups born in one historical period clining rapidly because of a growing tently in other areas of the world.3 than others). epidemic of binge drinking among • Frequency of binge drinking by men Nevertheless, a small set of large 18,19 women. However, research evi- and women often shows compli- longitudinal studies has provided con- dence indicates that these media sto- cated nonlinear relationships with sistent answers to the two questions ries oversimplify men’s and women’s age.28,36,37 about trends. From 2000 to 2010, patterns of binge drinking. large U.S. studies found that any binge Recent survey data consistently • Gender-specific associations of drinking (measured as ever or never) age with binge drinking may vary illustrate that men in the United 38 in the preceding month increased in States and throughout the world among regions within countries. prevalence more among women than binge drink more than women Taken together, these findings suggest among men.35,39,40 This trend was (see Table 1).20-33 Although studies that how age modifies effects of gender consistent with findings from binge measure binge drinking in various on binge drinking depends on the spe- drinking studies that used different

58 | Vol. 39, No. 1 Alcohol Research: Current Reviews Table 1 Prevalence of Binge Drinking

Source Population Binge Drinking Measure Men Women

2014 National Survey on Drug Use and Health20 United States, 5+ drinks, 1 occasion, past 30 days 33% 17% ages 18 and older China Chronic Disease and Risk Factor China, 50+ grams (men), 40+ grams (women), ethanol, 32% 4% Surveillance, 200721 ages 15 to 60 1 day, past 12 months Health Survey for England, 200722 England, >2 times recommended daily maximum 35% 27% ages 16 and older (>8 units for men, >6 units for women), past week, among drinkers Kangwha Cohort Study, Korea, 198823 Kangwha County, Korea, 6+ drinks, 1 occasion, past year 21% <1% ages 55 and older Moscow Health Survey 200424 Moscow, Russia, 80+ grams (men), 60+ grams (women), ethanol, 30% 6% ages 18 and older 1+ occasion per month National Health Survey 2004, Singapore25 Singapore, 5+ drinks, 1 occasion, past month 9% 5% ages 18 to 69 National survey, Denmark, 200326 Denmark, 6+ drinks, 1 occasion, once a month or more 38% 18% ages 15 to 99 National survey, Mozambique, 200527 Mozambique, 5+ drinks (men), 4+ drinks (women), or 25% 11% ages 25 to 64 equivalent drink container, 1 day, past week National survey, Spain, 2008 to 201028 Spain, 80+ grams (men), 60+ grams (women), ethanol, 10% 4% ages 18 to 64 1 occasion, past month Nationwide survey on alcohol consumption Brazil, 5+ drinks (men), 4+ drinks (women), 1 occasion, 40% 18% patterns, Brazil, 2005 to 200629 ages 18 and older past year South African National HIV Prevalence, Incidence, South Africa, 5+ drinks (men), 4+ drinks (women), 1 occasion, 17% 4% Behaviour and Communication Survey, 200830 ages 15 and older past month Survey, Hong Kong, 200631 Hong Kong, 5+ drinks, 1 occasion, past 30 days 15% 4% ages 18 to 70 Survey of Lifestyle, Attitudes and Nutrition in Ireland, 6+ drinks, 1 occasion, past year 92% 79% Ireland, 200732 ages 18 to 29 Third National Health Examination Survey, Thailand, Thailand, Multiple beverage-specific measures 40% 7% 200433 ages 15 and older time periods (a week and a year) other age groups.40,45 Trends in men’s Predictors of Adult and with findings from other coun- and women’s binge drinking may be Binge Drinking tries (England, Finland, Russia, and modified by drinking pattern chang- 25,36,41-43 Singapore). The greater increase es in different birth cohorts. In the in prevalence among women resulted United States and Finland, evidence Childhood Experiences in partial convergence of men’s and has shown that both men and women women’s likelihood of binge drinking. in more recent birth cohorts have been Childhood experiences are possible In contrast, in the United States, increasingly likely to become binge early predictors of binge drinking. convergence of women’s and men’s However, evaluations of gender differ- drinkers, at least until the 1980s birth frequency of binge drinking more likely 35,36,44 ences in childhood influences on binge occurred because of greater declines in cohort. These patterns indicate drinking are scarce, particularly in the frequency among men than among that further convergence of women’s United States. Most studies lack data women.40,44 Furthermore, evidence of and men’s binge drinking patterns may on binge drinking, do not analyze ef- men’s and women’s convergence in the be hard to predict and cannot be at- fects of childhood experiences on men United States often has been stronger tributed entirely to women’s increased and women separately, or provide data in young adults (20s and 30s) than in binge drinking.46 for only one gender.

Gender Differences in Binge Drinking | 59 Child maltreatment. Child mal- to 41 found a direct effect on binge drinking earlier than girls, which treatment (including childhood sexual drinking in women but not in men,62 could increase male risk of later binge abuse, childhood physical abuse, and whereas a much larger study of U.S. drinking, but recent gender differences neglect) has consistently been found to naval recruits found that binge drink- in age of onset are not large and are be a robust predictor of many adverse ing was more prevalent among those not entirely consistent with data from mental health outcomes, including men and women who had experienced outside the United States.73-75 The few high-risk drinking and alcohol use childhood sexual abuse (and was also studies of gender-specific associations disorder (AUD).47-51 Typically, re- more prevalent among those men, between early onset of alcohol use search has found that women more but not women, who had experienced and later binge drinking suggest that often report childhood sexual abuse childhood physical abuse).63 The vari- gender effects may be culturally de- than men,52-54 and men more often ation in the findings does not allow pendent. Caetano and colleagues, who report childhood physical abuse than simple conclusions about how gender studied Hispanic national groups in women,55,56 but not always.57 Gender may modify connections between the United States, found that drink- differences in experienced neglect are childhood maltreatment and adult ing onset at age 14 or younger versus uncertain.58-60 binge drinking. 21 or older increased the prevalence Given these gender differences in Parental problem drinking. An- of binge drinking among women types of child maltreatment, one might other childhood experience linked to more than among men for Mexican infer that childhood sexual abuse is adult alcohol problems is exposure Americans, Puerto Ricans, and South/ more of a risk factor for women’s to problematic parental drinking.64-67 Central Americans but not for Cuban- binge drinking, and childhood phys- Gender-specific analyses by Merline Americans.76 In Korea, both men and ical abuse is more of a risk factor for and colleagues64 and White and col- women who began drinking at age 17 men’s binge drinking. Unfortunately, leagues67 found that heavy drinking by or younger were more likely to binge research has infrequently compared parents adversely affected the drinking on drinking days, and later onset of how forms of child maltreatment affect behavior of their male and female drinking reduced binge drinking (as women’s versus men’s binge drinking. adult children. Unfortunately, reports typical drinking behavior) among The few relevant studies show incon- on parental drinking generally have women more than among men.77 sistent patterns, suggesting that gender not provided data on gender-specific In a Finnish community sample of differences in maltreatment effects effects or on binge drinking, and often middle-aged men and women, binge likely depend on the groups of men they have focused only on adolescent drinking was more frequent among and women studied and the measures drinkers or parents with diagnosed those who began drinking at age 16 or of binge drinking used. alcohol disorders (e.g., studies of adult younger, but this effect did not have a Widom and colleagues studied men children of alcoholics). However, a clear gender difference.78 and women with childhood histories community study in Finland found of abuse or neglect that resulted in that heavy parental drinking was court cases and compared them 30 significantly associated with binge Psychological Characteristics years later with approximately matched drinking at age 42 for men but not for The alcohol studies field has a long controls (from a Midwest U.S. metro- women, when controlling for individ- history of research on associations be- politan area).51 The researchers found ual drinking history.68 In data from the tween personality traits and alcohol use no significant differences in frequen- Young in Norway Longitudinal Study, in clinical and nonclinical samples.79-81 cy of past-month binge drinking parental binge drinking (not gender For this article, we selected two clusters (defined as 8+ drinks) between men specific) was related to adult children’s of personality characteristics that have with and without histories of child intoxication, or 5+ drink binges at known gender differences in preva- maltreatment. However, women who age 28, but there were no significant lence and that may affect men’s and had been neglected (with or without gender differences for this parental women’s binge drinking differently: other abuse) were more frequent binge influence.69 The lack of other recent disinhibiting traits (i.e., impulsivity, drinkers in the past month than same- data means the question of how gender sensation-seeking, and risk-taking) and sex controls. In South Africa, on the modifies parental drinking effects on affective characteristics (i.e., anxiety other hand, a history of childhood binge drinking by adult children re- and depression). physical punishment nearly doubled mains unresolved. Disinhibiting traits. Research has the prevalence of binge drinking as the Early onset of alcohol use. In the shown that heavy or binge drinking in usual behavior on a drinking day, al- United States, early onset of alcohol young adulthood is associated with a though this effect did not differ signifi- use is linked to adult alcohol prob- set of related disinhibiting personality cantly between men and women.61 lems,70,71 although the strength of this traits, including impulsivity, sensation- Concerning childhood sexual abuse, relationship has been challenged.72 seeking, and risk-taking.82-84 These a Pennsylvania study of adults ages 31 Boys in the United States begin behavior traits are more prevalent in

60 | Vol. 39, No. 1 Alcohol Research: Current Reviews men than in women,85-87 although scored higher than other men on a In the United States and worldwide, the size of the gender difference varies measure of depressive symptoms.103 smoking is more common among across age groups and traits. From The 2006 BRFSS survey also reported men than among women.115-117 To the these two findings, one could infer that that women with lifetime diagnoses of extent that smoking may be part of these disinhibiting traits contribute anxiety or depressive disorders or with a lifestyle that encourages or leads to to the excess of binge drinking current depression were more likely to binge drinking, the general patterns among men compared with women. binge drink than women without anx- described here might contribute to the However, it is not so clear that iety or depression, and the severity of gender gap in which men binge drink disinhibiting traits are associated with depression increased women’s (but not more than women. However, prolon- men’s binge drinking more strongly men’s) odds of binge drinking.108 gation of smoking may have unknown than with women’s. Some studies In a national Canadian survey, for effects on women’s binge drinking, found stronger associations between both men and women, depression and evidence indicates that women disinhibiting traits and frequency of was associated with drinking larger find it more difficult than men to stop binge drinking or intoxication among quantities per drinking occasion, smoking.118-120 men than among women.88,89 Other but the association was stronger for Multiple gender-specific studies studies concluded that disinhibiting women.109 In the large U.S. National worldwide have shown that smoking traits were more clearly associated with Epidemiologic Survey on Alcohol and is strongly related to both men’s and women’s heavy drinking.90,91 The most Related Conditions (NESARC),105 women’s binge drinking, typically common finding, however, was that women’s binge drinking was showing stronger connections for disinhibiting traits were associated associated only with post-traumatic women than for men. U.S. surveys with binge drinking, intoxication, or stress disorder and panic disorder have reported that men and women problem drinking among both women (without agoraphobia). A survey who smoke have three times higher and men, with more similar than at a large public university found odds than nonsmokers of being binge dissimilar gender-specific effects.92-95 that students with general anxiety drinkers,121 and smokers have a higher It is important to be cautious about disorder were more likely than other probability than nonsmokers of heavy interpreting such associations causally, students to engage in frequent binge drinking behavior at ages 35 and old- because the extent to which a history drinking, and students with major er.122 In China in 2007, the majority of heavy or binge drinking facilitates depression were less likely than other of men and women smokers were also men’s and women’s impulsivity, students to engage in frequent binge binge drinkers, an association that was sensation-seeking, and risk-taking is drinking.110 Both of these associations much stronger in women.21 A separate unknown. were stronger among men than 2006 study in Hong Kong found that Anxiety and depression. Anxiety women. These mixed findings suggest smoking multiplied the odds of binge and depression are more prevalent that depression and anxiety do not drinking by 3.7 for men and 12.3 for among women than men,96-99 and have simple or gender-determined women.31 In Brazil, the São Paulo some patterns of anxiety and depres- associations with binge drinking. Epidemiologic Catchment Area Study sion, such as patterns defined in the Studying how drinkers’ ages and found that men and women who were Diagnostic and Statistical Manual drinking opportunities differently binge drinkers were more than twice as of Mental Disorders, Fifth Edition affect links between binge drinking likely as non–heavy drinkers to be cur- (DSM-5), are associated with some and anxiety or depression among men rent smokers, and the relationship was patterns of alcohol consumption, such versus women may be worthwhile. stronger for women.123 In a national as AUD.100-102 However, it is not clear Canadian survey, the odds of binge that depression and/or anxiety are asso- drinking were significantly greater than ciated with binge drinking, specifically. Adult Binge Drinking 1.0 for all women smokers, but only Many studies with gender-specific data and Smoking for men who smoked more than six have failed to find connections among cigarettes a day.124 The 2004 Moscow anxiety, depression, and binge drink- Typically, studies that have exam- Health Survey found that women who ing for women or men.68,103-107 There ined adult binge drinking and other were binge drinkers had higher odds are some exceptions. A 2006 U.S. substance use have focused on tobacco of daily smoking than other women, Behavioral Risk Factor Surveillance smoking, particularly cigarettes. In the but men who were binge drinkers System (BRFSS) survey found that United States, among the whole young did not have higher odds of daily men with current depression were adult population,111 college students,112 smoking than other men.125 Most of more likely to be binge drinkers than adults ages 18 to 25,113 and adults these studies were cross-sectional and nondepressed men.108 In a U.S. survey older than age 50,114 binge drinkers could not distinguish the degree that of men and women older than age 56, consistently have higher odds than smoking influenced binge drinking or heavy-drinking or binge drinking men non–binge drinkers of being smokers. vice versa. These studies also did not

Gender Differences in Binge Drinking | 61 explore the possibility that both smok- to 2010) found that among binge al behavior (including thoughts ing and binge drinking were part of a drinkers, women reported more days of suicide and suicide attempts). syndrome with shared antecedents. It of physical and mental ill health than Research has found that suicidal would be worth examining the extent men, and men and women who had behavior often is associated with to which women who both smoke and recent heavy binge drinking episodes chronic heavy drinking,132,133 which binge drink are attempting to show (7+ drinks for women and 8+ drinks may be a symptom of psychological independence from older feminine for men) were more likely to report problems or a way of coping with stereotypes that discouraged both poor health–related quality of life than such problems. For both men and behaviors. binge drinkers who drank less.127 women, completed suicide has been In contrast, a study that analyzed associated with acute alcohol intox- National Health Interview Survey ication,134 which may precipitate or Differences in Health (NHIS) data from 1997 to 2004 found enable the behavior. Consequences that episodic heavy drinking (5+ drinks How episodic binge drinking as a in 1 day) added only modestly to the behavior pattern is related to men’s Research on how gender affects mortality risk of light and moderate or women’s suicidality has been the health consequences of adult drinkers.128 And, a population-based studied much less often. Available binge drinking is scarce, for several study of nearly 27,000 men and wom- research suggests that binge drink- possible reasons. Studies of chronic en who participated in the Danish ing has stronger associations with alcohol-related health problems may National Cohort Study from 1994 women’s suicidality than with neglect binge drinking episodes be- to 2005 reported that binge drinking men’s. According to U.S. National cause researchers may assume binge (6+ drinks on an occasion) among Violent Death Reporting System drinking has acute, not chronic, ef- male and female moderate drinkers was suicide data from 2003 to 2011, fects. Gender-specific analyses may be not associated with increased all-cause the likelihood of high postmor- neglected because including enough mortality when they were compared tem blood alcohol concentrations women who binge drink (e.g., in Asian with moderate drinkers who did not (BACs) of more than .08 g/dL was countries) for reliable statistical analysis binge drink.129 The authors suggested much greater than the likelihood is often difficult. Research may focus of high BACs in general popu- that Danish customs around binge 134 on adolescent rather than adult binge drinking (which usually occurs during lation survey data. Women’s drinking because of greater concern a long evening of eating and drinking) postmortem BACs generally were about acute and long-term health may account for the results. higher than men’s, but they were consequences for young drinkers. And, A Russian survey asked respondents not statistically significantly higher. investigators may have difficulty dis- about the health of close relatives after Data from the 2008 to 2012 U.S. tinguishing between effects of binge age 30 and found that men who had National Survey on Drug Use and drinking and effects of chronic heavy engaged in any binge drinking were Health showed that among women drinking, because the two drinking more likely to have died than other and men who had not experienced patterns are correlated. Nevertheless, male drinkers, but for women, in- major depressive episodes, women’s research does suggest where binge creased mortality occurred only among binge drinking was associated with drinking has gender-related health ef- those who binge drank at least once planned and attempted suicide, but fects, and where it does not. 130 men’s binge drinking was associated a month. In Norway, women and 135 men who binge drank on 10 or more only with suicidal thoughts. These Morbidity and Mortality occasions in the past year were more data showed no association between suicidality and binge drinking in Several recent studies have found likely to report alcohol-related sickness that caused absence from work than men and women who had past ma- that binge drinking adversely affects jor depressive episodes. In a nation- those who binge drank no more than mortality and morbidity for both ally representative sample in France, 5 times, and the pattern of more fre- men and women. In a sample of U.S. binge drinking at least monthly pre- quent binge drinking was associated moderate drinkers ages 55 to 65, the dicted suicidal ideation and suicide with sickness-related absence more odds of dying in the next 20 years were 131 attempts better for women than for twice as great for moderate drinkers strongly for women than for men. men.136 And, in a survey of U.S. col- who initially reported binge drinking lege undergraduates, reported past in the preceding month than for Suicidality suicide attempts were significantly moderate drinkers who did not report associated with reported past binge such binge drinking. No significant A special case of mortality risk drinking among young women but difference between genders was among binge drinkers is the potential not among young men.137 However, found.126 National U.S. surveys (2008 effect of binge drinking on suicid- the time order of binge drinking

62 | Vol. 39, No. 1 Alcohol Research: Current Reviews and suicidality remains unclear, except levels (now debated) and acting as cancer risk for men only if they had as shown in the postmortem data re- a cumulative carcinogen (through consumed low amounts of dietary ported by Kaplan and colleagues.134 increased exposure to acetaldehyde fiber,162 were African American,163 and byproducts of the CYP2E1 or had been lifetime, rather than Cancer enzyme, likely activated by binge current, heavy drinkers.164 And, some drinking).152,153 large or meta-analytic studies found A possible life-endangering effect of Research on associations between that drinking had little or no associa- binge drinking is an increase in wom- binge drinking and breast cancer has tion with prostate cancer.165-167 en’s and men’s risks of various forms been scarce. In the Danish Nurse The picture is just as confused for of cancer. Evidence clearly shows that Cohort Study, data from 1993 to the limited research on associations heavy alcohol consumption is a risk 2001 showed that women who binge between binge drinking and prostate factor for cancers in the oral cavity, drank on weekends (Friday through cancer risk. In the 1986 to 1998 pharynx, esophagus, liver, colon and 138,139 140-142 Sunday) or on the latest weekday Health Professionals Follow-Up rectum, and pancreas. In had greater risk of breast cancer than Study of men ages 40 to 75, men general, research on these cancers has women who were light drinkers, who were binge drinkers (compared not provided information about binge even after adjusting for total volume with abstainers) had the greatest drinking and its gender-specific effects. of alcohol consumed.154 In the U.S. increase in prostate cancer risk.168 In One exception is a San Francisco Bay Nurses’ Health Study, data from this study, binge drinking was de- Area population-based case-control 1980 to 2008 showed that monthly fined as drinking 105 grams or more study, which found that the risk of binge drinking was associated with a of ethanol on 1 to 2 occasions per pancreatic cancer was higher specifi- 33% increase in risk of breast cancer, week. The older part of the Finnish cally among men who had a history but controlling for cumulative Twin Cohort study, which surveyed of binge drinking, particularly if the alcohol consumption weakened the twins (mean age of 40) from 1981 binge drinking persisted over years and association.155 A New Zealand case- 143 to 2012, found that binge drinkers involved large numbers of drinks. control study found that weekly had a greater risk of prostate cancer Another recent exception is a Korean binge drinking was associated with than non–binge drinkers.158 In con- longitudinal study of differentiated a 55% increase in risk of breast trast to these cohort-based studies, 156 thyroid cancer, which found that cancer among Maori women. A case-control data from the 2000 acute, heavy alcohol consumption case-control study in North Carolina NHIS survey,169 the U.K. Prostate (more than 151 grams of ethanol on found a positive association between Testing for Cancer and Treatment one or more lifetime occasions), when binge drinking and risk of breast (ProtecT) study,170 and the U.S. compared with no alcohol consump- cancer among women who drank Prostate Cancer Prevention Trial171 tion, doubled men’s cancer risk and an average of 91 grams or more of 144 showed no connection between binge tripled women’s cancer risk. ethanol per week, but the association drinking and prostate cancer. Our In studies of gender-specific (or was not significant after controlling conclusion from the conflicting re- nearly so) cancers, gender-specific for other variables, possibly because 157 search is that binge drinking does not effects of alcohol get closer attention. the sample size was small. have simple or unconditional effects Research on gynecological cancers Evaluating the effects of alcohol on prostate cancer. (i.e., cervical, ovarian, and endome- consumption and binge drinking on trial/uterine) has consistently found male-specific cancers has been diffi- Cardiovascular Disorders no association between women’s cult. The effects of drinking on testic- drinking and the risks of these can- ular cancer are unknown, because no Heavy drinking (variously defined) cers.145-148 In contrast, a large set of recent or major research on testicular by both men and women consistently evidence has consistently shown that cancer has evaluated the drinking has been associated with higher risks women’s risk of breast cancer increases patterns of the men studied. Also, of hypertension,172,173 atrial fibrilla- with increased alcohol consumption, although research on prostate cancer tion,174 and .175,176 Relationships even at moderate levels, resulting in has examined alcohol consumption, between chronic heavy drinking and more than 100,000 alcohol-related the findings conflict. Some studies coronary heart disease (CHD) have cases of breast cancer worldwide each found that heavier drinking was asso- been less consistent. Some studies year.149,150 (Alcohol is apparently less ciated with a greater risk of prostate found that such drinking was a risk relevant in the rarer male breast can- cancer.158,159 Some research reported factor for both women and men,177 cer.151) Hypothetically, alcohol may that drinking raised risk only for whereas other studies failed to find increase women’s breast cancer risk advanced cancer160 or only for non- such connections.178-180 through multiple processes, including advanced cancer.161 In other studies, Generally, binge drinking has increasing tumor-promoting estrogen heavier drinking raised prostate been associated with a higher risk of

Gender Differences in Binge Drinking | 63 cardiovascular disorders, but reports of conclusions about how gender impairment of the normal neuronal such associations often are not gender modifies the adverse effects of binge pruning process in binge drinking specific.181-183 Available gender-specific drinking on the liver. females.209 data have shown that men’s risks from A larger set of studies of cognitive binge drinking usually are greater than Brain and Neurocognitive functioning has identified at least three women’s risks. For example, men’s Consequences general areas in which binge drinking risk was greater than women’s for adolescent and young adult males and CHD and hypertension,184 death from Damage that some patterns of cardiovascular disease,185 and death alcohol consumption can do to the females may be impaired. from ischemic stroke.186 However, brain is both well-known and well- 1. In tasks involving working memo- findings for women were often limited studied, particularly in adolescents 200-202 ry, binge drinking females showed by small sample size, and some studies and individuals with AUD. less activation of spatial working found that women and men binge Furthermore, many studies have memory than same-sex controls, drinkers had similar risks for hyperten- specifically examined the harmful and binge drinking males showed 187 effects of binge drinking on the brain sion and for death after myocardial greater activation than controls.210 infarction.188 and neurocognition. However, it is difficult to draw general and reliable In other working memory tasks, the brains of binge drinkers appar- Liver Disorders conclusions from these studies about gender differences in binge drinking ently had to work harder to per- Research has shown conclusively effects on the brain,203 in part form at the same level as non–binge that heavy drinking increases risk of because many of these studies (e.g., drinkers, but no gender differences a variety of liver diseases and dam- those that used functional magnetic were reported for those tasks, possi- 189-191 age. From our review of this resonance imaging) examined small, bly because of small sample sizes in research, we draw three general conclu- nonrepresentative samples, which these studies.211,212 sions about gender and the effects of does not allow reliable, within- 2. In studies of response inhibition binge drinking on the liver: gender evaluations (i.e., comparing and monitoring of one’s own 1. Research on the effects of binge binge drinkers with same-sex behavior, binge drinking gener- drinking on the liver is scarce controls). Nevertheless, certain patterns have emerged that may ally impaired females more than and reveals little about gender 90,213,214 differences.192,193 guide future gender-specific research males, but at least one study and interventions. found an increase in performance 2. Research on liver damage specifi- self-monitoring among females, cally from binge drinking may be One pattern is that binge drink- ing may alter the anatomy of the who were possibly compensating scarce because research has repeat- 215 edly found that harm to the liver young brain in ways that could have for alcohol effects. No such in- results from continuous (frequent) persistent adverse effects. In adoles- crease was found among male binge drinking rather than episodic cents and college students who have drinkers. drinking (such as binges).194-196 binge drinking histories, studies have shown evidence of poorer integrity 3. In evaluations of executive func- Binges may merely increase the cu- tioning and decision-making, one mulative toxic exposure to alcohol. (as indicated by lower fractional an- isotropy) of white matter in multiple study found the worst performance 216 3. The risk of liver damage from areas of the brain,204,205 an effect that in male binge drinkers, another chronic drinking is greater for at least one study found mainly in study found males and females 190,197 women than for men, possibly males and in areas of the brain relat- were similarly impaired,217 and a because of differences in how the ed to cognitive function and atten- laboratory test of acute impairment body distributes and metabolizes 206 189,198 tional processes. Studies also have reported that males and females alcohol. A European study shown that adolescent binge drinkers performed similarly, although the reported an exception to this had reductions in white and gray females had higher BAC levels.218 gender difference, however. matter in the cerebellum (for both The study found that for men, genders)207 and changes in frontal All these performance tests are more binge drinking created a higher cortices (thicker for females, thinner descriptive than explanatory, saying risk of alcohol-related hepatic for males).208 In the latter study, the little about why gender differences steatosis (fatty liver) than it did sometimes occur and sometimes do 199 increased cortical thickness was as- for women. sociated with worse performance on not, or about the extent to which these In general, not enough research has visuospatial, inhibition, and atten- levels of impairment are reversible or been conducted to draw any firm tion assessments, possibly reflecting might affect adult life.

64 | Vol. 39, No. 1 Alcohol Research: Current Reviews Differences in Behavioral the females, had BACs of more than Nevertheless, research findings show and Social Consequences .07 g/dL.230 several clear patterns in how binge Although AID episodes are very like- drinking and sexual assaults are likely Research has repeatedly documented ly to involve binge drinkers, a majority to be connected. and decried multiple adverse of binge drinkers do not report driving Perpetration. One repeated finding behavioral and social consequences after drinking. In 2003 to 2004 U.S. is that binge drinking among male of binge drinking.219-222 This research, survey data from self-reported binge college students can make them more however, has not reported much drinkers, 13.2% of the men and 8.1% likely to engage in sexual aggression. about gender differences for many of the women reported driving after In terms of immediate consequences, of these consequences. The research drinking.231 However, tendencies to a study found that men were more has revealed even less about possible binge drink and to drive while intoxi- likely to engage in sexual aggression if gender-specific links between binge cated often occur together. The odds of they had BACs of more than .15 g/dL, drinking and behavioral or social particularly if they were otherwise AID are more than 5 times greater for 241 harm. Our focus here, therefore, is binge drinkers than for other drinkers, light drinkers. Another study de- on three major behavioral and social and the odds are more than 10 times termined that the number of drinks problems for which gender-specific greater for those who binge drink fre- men drank in the 4 hours before a sexual encounter affected their odds effects of alcohol consumption have quently or who generally drink heavily, 242 been recognized and studied: alcohol- and these odds increases may be great- of aggressive sex with new partners. impaired driving (AID), sexual assault, er for men than for women.227,232,233 And, among men who reported per- petrating past sexual violence, having and intimate partner violence (IPV). A study of daily diaries kept by college consumed a larger number of drinks at students estimated that each 0.1% the time led to greater aggression (up Alcohol-Impaired Driving increase in estimated daily blood to the point where severe intoxication alcohol level was associated with a was disabling).243 One college study In recent U.S. research on AID, 4% increase in men driving after two gender patterns are clear. Men found 1-year lagged effects of men’s drinking, and a 1% increase for binge drinking on sexual aggression,244 engage in AID more than women, 234 women. suggesting that binge drinking as a but the prevalence of both men’s and continuing pattern among men might women’s AID has been declining Sexual Assault reinforce recurrent sexual aggression, at since the 1990s, judging from self- 40 Knowledge about how binge drink- least in the college years. reports and the National Roadside Victimization. There is much Survey.223 However, from 1982 to ing is related to sexual assault has three important limitations: evidence that women’s drinking, in 2004, women’s arrests for driving general, is associated with subsequent under the influence increased (while 1. Because the great majority of re- 245 224 sexual assault. A lingering question men’s decreased), possibly reflecting ported sexual assaults involve men is whether women’s binge drinking in- changes in laws and law enforcement assaulting women, research has creases this apparent risk. Incapacitated (including lower limits for BACs) and focused on how alcohol is related to 225,226 rape, which can occur when women increases in women’s driving. these assaults.235,236 Little is known have drunk too much to be able to U.S. surveys indicate that more about the circumstances in which resist an attack, is a major adverse than 80% of AID episodes were self- men are sexually assaulted.237,238 effect of binge drinking. Among col- reported by binge drinkers.227,228 It 2. Most research has focused on as- lege women, a majority of rapes occur is unclear, however, whether binge saults among college students and when women have drunk enough to drinking immediately preceded 236,240 young adults, groups most likely to be incapacitated. Apart from inca- the episodes of drunk driving, and pacitation and rape, women who binge U.S. reports have not indicated how be both heavy drinkers and sexually active. drink are also at greater general risk many binge drinking drivers were of sexual victimization246-248 for many men and how many were women. 3. Research may reveal associations possible reasons: men’s misinterpreta- Cultural differences may affect AID between binge drinking and sexual tion of women’s drinking as a sign of gender patterns. In Sweden, men and assaults, but understanding the sexual availability, miscommunication women arrested for driving under extent that binge drinking caus- of women’s refusals, and women’s the influence drank a similar amount es or results from the assaults is underestimation of hazards from male beforehand (typically more than five difficult because of uncertainties companions.245 One study of college drinks).229 Among Australian drivers about the order of events and time women found evidence that binge killed in single-vehicle crashes, 50% lags between drinking and the as- drinkers may overestimate their ability of the males, compared with 29% of saults.239,240 to resist rape attempts.249

Gender Differences in Binge Drinking | 65 It is not clear whether experiences IPV, therefore, it is important to study are victimized cope with the distress of sexual victimization lead women binge drinking among both men and in other ways. Indeed, male victims to binge drink, possibly to help cope women as perpetrators and as victims of IPV might be more likely to use with the emotional aftereffects of of IPV. binge drinking as a stereotypically male assault. In some studies of women A large body of research links alco- method of coping, but few studies in college250 and in the general U.S. hol use in general to IPV perpetration have looked for or found evidence of population,235 experiences of sexual and victimization.258,262 One might men’s binge drinking behavior after assault did not predict subsequent expect binge drinking, in particular, IPV victimization.274,275 If binge drink- binge drinking. Other studies, to increase the likelihood of IPV per- ing is becoming more prevalent among however, did find that experiences petration through disinhibition and women (as noted earlier), there may of incapacitated rape251 or repeated increased aggression.263 Indeed, in be a greater need for interventions to victimization252 were associated with bivariate analyses of survey data, binge reduce the use of alcohol as a coping subsequent binge drinking. These drinking was associated with IPV per- mechanism. apparent contradictions suggest two petration among men and women in more complex patterns: Canada and Costa Rica and among 258 Alcohol’s Harm to Others 1. Women’s experiences of sexual women in Brazil. In bivariate anal- victimization may perpetuate (not yses of U.S. survey data, rates of IPV To date, alcohol research has fo- just initiate) binge drinking (and perpetration were doubled for male cused mostly on how drinking harms binge drinkers and nearly tripled for the drinker.276 Limited previous re- controlling for effects of prior 264,265 drinking might obscure effects female binge drinkers. However, search on harm to people other than in multivariate analyses of U.S. data, the drinker has focused mainly on of victimization on subsequent 277,278 279,280 drinking).247,250 the associations between binge drink- AID, fetal development, and ing and IPV either disappeared264,265 or IPV,281,282 largely neglecting broader 2. In the short term, such as during became too small to be meaningful.266 harm to others’ mental health, quality college or the young-adult years, Binge drinking might also increase of life, living conditions, and resources. women’s binge drinking and sex- women’s vulnerability to IPV An Australian study has suggested that ual victimization might become victimization. In surveys in Brazil, costs of such harm to others may be a vicious circle, each making the Canada, Mexico, and Peru, binge double those experienced by drinkers other more likely, increasing risk drinking women were more likely 283 245 themselves. of revictimization. to report being victims of IPV.258 A Some studies of alcohol’s harm to These more complex patterns should meta-analysis of three longitudinal others (AHTO) have examined gender be further evaluated. U.S. studies found that women’s differences in the types of harm caused binge drinking significantly increased and harm received. A common finding the odds of their subsequent IPV has been that women are considerably Intimate Partner Violence 267 victimization, but other U.S. more likely than men to experience Research on IPV has focused studies either could not confirm such marital and family harm, and men largely on male violence against a relationship265,268,269 or found only are significantly more likely than female partners and the aftereffects very weak relationships.266 These women to experience physical assault for female partners.253,254 Consistent mixed findings about perpetration from strangers and other crime vic- with this focus, 2005 U.S. survey and victimization, particularly from timization.284-286 However, with a few data have shown that women were multivariate analyses, suggest that exceptions,287,288 AHTO research has roughly twice as likely as men to binge drinking (as distinct from focused on harmful effects of others’ report being victims of IPV over other drinking patterns) may not be drinking or heavy drinking without their lifetimes and in the past year.255 a direct cause of IPV, but it may be exploring possible associations between However, this focus neglects women’s an indicator of other personality and specific drinking patterns (e.g., heavy violence against male partners, which behavior patterns that may lead to IPV episodic or binge drinking) and spe- may be more prevalent at times in (e.g., antisocial traits).270,271 cific types of harm. Such associations some groups, particularly outside the Research shows, somewhat more might include relationships between United States.256-259 It also neglects consistently, that a history of IPV binge drinking and AID, crashes, and the degree that IPV is an interactive victimization increases the likeli- fatalities, or relationships between process in which violence can be hood that women will engage in binge drinking and increased risk reactive and defensive as well as pro- binge drinking after varying time of fetal alcohol effects. The harm to active, with both partners as victims lags.267,272,273 However, this relationship others paradigm is a relatively new de- and attackers.260,261 To understand is not always evident or strong,268,269 velopment in alcohol epidemiology.289 how binge drinking may be related to possibly because many women who As this perspective matures, we hope

66 | Vol. 39, No. 1 Alcohol Research: Current Reviews that greater attention will be given to Integrated Interventions for Binge stigmatized by their alcohol use or associations between specific drink- Drinking and Smoking misuse.303 ing patterns, such as binge drinking, Given the strong associations be- Considerable anecdotal evi- dence,304-306 supported by qualitative and specific types of harm, as well as tween binge drinking and smoking studies in several countries,307-310 possible gender differences in those described in this article, there may be suggests that one motivation for binge associations. promise in combined interventions drinking among women—younger that target both smoking cessation and women in particular—may be that Possible Implications binge drinking. Indeed, preliminary “drinking like a man” produces data presented by Ames and colleagues feelings of power, status, and gender suggest the potential value of inte- equality. To date, in all countries Treatment grated smoking cessation and binge studied, men drank more alcohol than drinking interventions, particularly Our research literature search 299 women, and men engaged in extreme for young adults. Environmental in- forms of drinking, such as high- on gender differences in alcohol terventions that disengage alcohol use treatment outcomes found very little volume drinking and heavy episodic and tobacco use (e.g., smoking bans in or binge drinking, more than women. information specifically relevant to bars) may also help to reduce hazard- binge drinking. Nonetheless, research In many traditional societies, heavy ous drinking behavior. Evidence from alcohol consumption symbolizes and on gender-specific alcohol treatment several countries indicates that female is helpful when considering strategies enhances men’s greater power relative smokers find it more difficult than to women, serving as an emblem of to reduce binge drinking. Before the male smokers to stop smoking,118-120 early 1990s, most alcohol and drug male superiority and a privilege that so combined interventions to reduce men have often denied to women.311 treatment programs were developed both smoking and binge drinking for and served primarily men.290 Indeed, in contemporary higher- could prove especially helpful to income countries, numerous studies of However, more recent research on women who both smoke and binge young men have reported associations gender-sensitive treatment has focused drink. among endorsement of traditional on treatment strategies that may be masculine norms, heavy and binge particularly appropriate and effective Prevention drinking, and adverse drinking for women. Much of this evolution consequences.312,313 With changing of gender-sensitive treatment has In our search for prevention gender roles in many societies, and been informed by empirical evidence programs that specifically target binge increasing opportunities for women, of gender differences in treatment drinking, we found an article that increased access to and consumption needs. This evidence includes research described gender-specific prevention of alcohol understandably may seem demonstrating higher prevalence strategies focused specifically on binge like an expression of liberation and among women of (1) comorbidity drinking college women.300 Aimed empowerment for many young of substance use disorders and other primarily at nurse practitioners, women. psychiatric disorders (e.g., mood, this article argued that for women To our knowledge, prevention anxiety, and eating disorders), (2) college students, several common scientists have not tried to reduce trauma exposure and associated consequences of binge drinking (e.g., binge drinking in young women by physical and mental health needs, and sexually transmitted infections, sexual changing the significance of heavy (3) the central role of relationships assault, and other physical injury) alcohol consumption as a symbol of (with children, intimate partners, and bring them into contact with health gender equality. A critical question others) in women’s addiction and care providers, offering opportunities is how best to persuade women that recovery.291-293 A number of studies for intervention. The author suggested alcohol is a poor way to demonstrate have reported a general tendency several intervention strategies that gender equality—clearly not through for women to respond somewhat may be particularly effective for simple educational approaches314 or better to a variety of psychosocial female binge drinkers, including by trying to frighten or shame them, interventions294-296 and to show a brief motivational interventions.294,301 such as with warning labels.315 One less consistent or harder-to-detect She speculated that Web-based modest policy step might be to restrict response to some pharmacological interventions may be particularly advertising that links drinking to treatments.297,298 There is general effective for women, perhaps due to liberation from traditional feminine agreement on the need for more well- women’s greater involvement with roles and stereotypes.316 It is possible, controlled randomized clinical trials electronic programs302 and the greater also, that mass media and marketing that examine the effects of gender- feeling of anonymity online programs methods could be used to sell the specific treatment. may provide for women who feel positive advantages of abstention or

Gender Differences in Binge Drinking | 67 low-risk alcohol consumption. A sequences of binge drinking for men’s predict binge drinking versus being powerful message might be that and women’s behavior and health. consequences of binge drinking or women do not gain status or express Second, although a majority of outcomes of some third factor that liberation by emphasizing their prevalence studies have disaggregated also predicts binge drinking sameness with men or by trying to binge drinking rates by gender, many outdrink them, but by setting their studies of predictors and consequences • Temporal and causal linkages own standards—in their drinking of binge drinking have not. In some (including possible bidirectional decisions and in other areas of their cases, studies have focused only on relationships) between smoking lives.305,317 Such messaging may be men or only on women, whereas and binge drinking, binge most effective if it provides gender- other studies sampled both males drinking and suicide attempts, specific information about drinking and females but did not conduct binge drinking and sexual assault, norms318 and is reinforced by or report gender-specific analyses. and binge drinking and intimate multiple community sources.319 In the United States in the 1990s, partner violence Parallel prevention strategies actions by the National Institutes Fourth, we were unable to find could be targeted to men, especially of Health led to increases in female recent binge drinking literature, other younger men, to weaken associations research participants in both human320 321 than studies addressing age differ- among traditional constructions of and animal studies. Despite ences, that examined interactions of masculinity, heavy episodic drink- these increases, many researchers, gender with other major demograph- from diverse scientific fields, fail to ing, and other risk-taking behavior. ic variables, such as race/ethnicity, Specific strategies might include consider the role of (biological) sex sexual orientation, or socioeconomic media literacy training to recognize and (culturally defined) gender when status. Future research should give and resist media images that link designing, analyzing, and reporting masculinity and excessive alcohol research. In addition to continued increased attention to such variables’ use, and interventions designed to pressure on funding agencies to associations with binge drinking prev- change expectancies about alcohol’s require sampling of both genders alence, predictors, and consequences. effects on sexuality, aggression, and when appropriate for the research Finally, very little research has other dimensions of traditional question being studied, editors and tested strategies specifically designed masculinity.313 reviewers for scientific journals can to reduce or prevent binge drinking. play an important role in requiring There are major conceptual and Future Research Needs adequate analyses and reporting methodological challenges to de- of sex and gender differences in signing and evaluating intervention When attempting to review gender research publications.322 A greater strategies that specifically address differences in the prevalence, pre- understanding of gender-differentiated binge drinking, as compared with dictors, and consequences of binge aspects of binge drinking is one of more general interventions to reduce drinking—and gender-sensitive many benefits that could result from or prevent chronic heavy drinking strategies to reduce binge drinking— development of new, and greater or AUDs. Nonetheless, our review we became aware of many gaps that enforcement of existing, guidelines for suggests that there may be promise future research could fill. Some of attention to sex and gender in scientific (and possibly gender differences in ef- the major gaps and challenges in this research. fectiveness) in intervention strategies area are listed and discussed briefly in Third, the majority of studies that specifically target the combina- this section. reviewed in this article were cross- tion of binge drinking and smoking, First, the use of differentdefini - sectional, limiting inferences that tions and measures of binge drinking as well as in strategies that attempt can be drawn about time order and to weaken perceptions, expectancies, poses a serious challenge to research causality. Some of the many questions on many aspects of binge drinking. and norms that link men’s binge that well-designed longitudinal drinking with ideals of traditional For researchers interested in gender research could begin to answer are: similarities and differences, the use masculinity or women’s binge drink- of more consistent definitions and • The persistence or nonpersistence ing with feelings of status, power, measures would permit much firmer into adulthood of effects of and gender equality. In addition, conclusions about gender-related adolescent and young-adult binge the emerging perspective of AHTO patterns in binge drinking prevalence drinking on brain structure and may eventually suggest approaches (across types of populations sampled function for preventing or reducing binge and in various cultural contexts), as • The extent that psychological drinking linked to gender-related well as about gender-linked predic- characteristics such as impulsivity, harm, such as IPV and adverse fetal tors of binge drinking and the con- anxiety, and depression precede and alcohol effects.

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Garbutt JC, Kranzler HR, O’Malley SS, et al. identities and women’s changing social positions. normative feedback: The use of gender-specific Efficacy and tolerability of long-acting injectable Sex Roles. 2008;59:694-712. referents. J Stud Alcohol Drugs. 2007;68(2):228- naltrexone for alcohol dependence: A randomized 237. PMID: 17286341. controlled trial. JAMA. 2005;293(13):1617-1625. 309. Watts R, Linke S, Murray E, et al. Calling the shots: PMID: 15811981. Young professional women’s relationship with 319. Holder HD, Gruenewald PJ, Ponicki WR, et al. Effect alcohol. Fem Psychol. 2015;25(2):219-234. of community-based interventions on high-risk 298. Baros AM, Latham PK, Anton RF. Naltrexone and drinking and alcohol-related injuries. JAMA. 310. Young AM, Morales M, McCabe SE, et al. Drinking cognitive behavioral therapy for the treatment of 2000;284(18):2341-2347. PMID: 11066184. alcohol dependence: Do sex differences exist? like a guy: Frequent binge drinking among Alcohol Clin Exp Res. 2008;32(5):771-776. undergraduate women. Subst Use Misuse. 320. National Institutes of Health, Office of Extramural PMID: 18336635. 2005;40:241-267. PMID: 15770887. Research. Inclusion of women and minorities as participants in research involving human subjects— 311. Wilsnack RW, Wilsnack SC, Obot IS. Why study 299. Ames SC, Werch CE, Ames GE, et al. Integrated policy implementation page. http://grants.nih.gov/ gender, alcohol and culture? In: Obot IS, Room smoking cessation and binge drinking intervention grants/funding/women_min/women_min.htm. R, eds. Alcohol, Gender and Drinking Problems: for young adults: A pilot investigation. Ann Behav Accessed August 7, 2017. Med. 2010;40:343-349. PMID: 20730517. Perspectives from Low and Middle Income Countries. Geneva, Switzerland: World Health 321. Clayton JA, Collins FS. Policy: NIH to balance sex in 300. 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76 | Vol. 39, No. 1 Alcohol Research: Current Reviews ALCOHOL RESEARCH: Current Reviews

Binge Drinking’s Effects on the Developing Brain— Animal Models

Susanne Hiller-Sturmhöfel and Linda Patia Spear Susanne Hiller-Sturmhöfel, Ph.D., is a science writer and editor Adolescence typically is a time of experimentation, including alcohol use and, partic- affiliated with CSR Inc., Arlington, ularly, binge drinking. Because the brain is still developing during adolescence, such Virginia. exposure could have long-lasting effects. Animal models and adolescent intermit- tent ethanol exposure (AIE) paradigms have been used to help elucidate the conse- Linda Patia Spear, Ph.D., is quences of adolescent binge drinking. These studies have identified cognitive deficits, a distinguished professor, particularly in challenging cognitive tasks, and behavioral alterations such as greater risk preferences, impulsivity, and disinhibition. AIE also is associated with changes Department of Psychology, State in affect when the animals reach adulthood, including increased social anxiety and, University of New York, and the sometimes, general anxiety. Animal models have demonstrated that AIE can result in director of the Developmental retention of certain alcohol-related adolescent phenotypes (i.e., reduced sensitivity to Exposure Alcohol Research alcohol’s aversive effects and increased sensitivity to alcohol’s rewarding effects) into Center, Binghamton University, adulthood, which may motivate continued elevated alcohol use. The detrimental ef- Binghamton, New York. fects of adolescent alcohol exposure extend to a diversity of lasting alterations in the brain, including reduced , increased proinflammatory responses, chang- es in gene expression through epigenetic mechanisms, and alterations in the activi- ties of various neurotransmitter systems. Further exploration of these mechanisms in animal models and humans may lead to improved prevention and intervention efforts.

Key words: Adolescence; alcohol exposure; alcohol use disorder; animal studies; binge drinking; brain development

Adolescence typically is a time of Moreover, in human adolescents it is human behaviors such as alcohol use experimentation and emulation of difficult to discern whether observed and addiction. Certain factors that adult behaviors, and many adolescents correlations between alcohol use and influence adolescent neurobehavioral initiate alcohol and other drug (AOD) the behavioral or neuropsychological function and AOD misuse are not use during this developmental period. measures under investigation reflect amenable to analysis using animal Brain development continues during causes or consequences of alcohol use models, including variables such as ver- adolescence, which could render the or are purely coincidental. Finally, bal ability and language, and influenc- adolescent brain particularly vulnera- despite significant progress in noninva- es such as self-esteem, culture, media, ble to alcohol’s effects. Consequently, sive imaging technologies, the complex- or even parenting styles. Despite these adolescent alcohol exposure could ity of the human brain and technical limitations, much of what is currently result in long-lasting changes in neuro- limitations of brain analyses hamper known about the intricacies of brain psychological function and increased researchers’ abilities to fully investigate development, neural substrates of risk of developing alcohol use disorder how alcohol influences adolescent brain AOD use and misuse, and adolescent (AUD). To better understand and structure and function. responses to AODs has been obtained minimize these risks, it is crucial to Animal models using laboratory using animal models. This article sum- comprehensively study alcohol’s animals such as mice and rats can help marizes some of the characteristics of impact on the adolescent brain. Such circumvent some of these problems. animal models for studying alcohol’s studies in humans face a number of However, their use also is associated effects on the adolescent brain and challenges, however. For example, eth- with certain limitations. Most impor- reviews the findings of studies using ical constraints prevent the administra- tantly, no currently available animal those models that have shed light on tion of alcohol to underage youth. model can fully represent complex functional and structural alterations

Binge Drinking’s Effects on the Developing Brain—Animal Models | 77 associated with adolescent alcohol use, adolescents and rodent models of ado- gion that comprises a notably greater the alcohol-induced persistence of lescence when comparable assessment proportion of the total brain matter in adolescent phenotypes into adulthood, measures of alcohol sensitivity and humans and other primates than in ro- and the impact of adolescent alcohol consequences were used.2 dents. In humans, the PFC is thought use on later alcohol consumption. to play a central role in executive Animal Models of Alcohol Use and functions, such as working memory, Its Consequences temporal processing, planning, flex- Characteristics of ibility, and decision-making, which Animal Models One of the main factors for using influence behaviors such as drug rodent animal models for alcohol re- self-administration and dependence. The potential usefulness and validity search is that these animals voluntarily Comparative studies have indicated of animal models, especially for com- self-administer AODs when given free that rats also engage in these behaviors, plex behaviors such as alcohol misuse access. For example, rodents often oral- and that the PFC is critical for mediat- and its consequences, depend primarily ly self-administer substantial amounts ing these processes in rodents, nonhu- on the specific research questions being of alcohol, particularly if they are man primates, and humans.5,6 In rats asked. The validity of such models can offered beer or sweetened beverages. and humans, the PFC can be divided be assessed on three levels:1 Laboratory animals and humans exhib- into subregions that are associated it similar behavioral and cognitive re- with similar cognitive functions across • Face validity assesses whether the sponses to acute AOD administration. species.5 Experimental animal models phenomenon under study in the Laboratory animals effectively model a have been used successfully to repro- model resembles the targeted human broad diversity of alcohol effects seen duce features of neuropathological and behavior in terms of its behavioral, in humans, ranging from and neurochemical changes observed in cognitive, and physiological features. social stimulation at low alcohol levels humans who had neurodegenerative However, it is important to realize to intoxication, motor impairment, and psychiatric disorders that affected that even if certain behaviors or sedation, and memory impairment at their cognitive function.7 other effects appear similar across higher doses.3 In addition, animals that Extensive studies also have estab- species, they may not share the same are chronically exposed to AODs can lished the relevance of animal models underlying mechanisms. develop physical dependence, charac- for investigating drug use behaviors • The measure of construct validity terized by dysphoria and physical signs and the consequences. For instance, focuses on the relevance of the phe- of withdrawal (e.g., tremor, anxiety, brain reward systems using the neu- nomenon under investigation in the insomnia, and even seizures) when rotransmitter dopamine, including do- animal model to the concept being access is terminated.4 Such physical pamine projection regions of the nu- modeled. Investigators seek to deter- dependence can be accompanied by cleus accumbens (NAc), amygdala, and mine how similar the animal model a tendency for relapse, particularly PFC, are critically involved in drug is to the biological foundation and after re-exposure to the drug or expo- self-administration and dependence neural underpinnings of the human sure to stressors or drug-related cues. in humans and animal models.8-10 In behavior being modeled. This con- Experiments that used a conditioned addition, in humans and laboratory cept also considers the impact of place preference approach demonstrat- animals, specific brain structures and moderators, such as previous experi- ed that laboratory animals, even with- neurochemical systems are critical for ences or the environment. out physical dependence, can develop different aspects of alcohol use and a preference for contextual cues associ- misuse (e.g., producing dependence or • The concept of predictive validity ated with drug use. mediating craving and relapse).11 reflects how effectively the animal Not only are the behavioral conse- However, differences exist between model predicts experimental findings quences of alcohol exposure often sim- the rodent and the human and non- or treatment outcomes in humans. ilar in humans and in animal models, human primate brains that should be Assessment of the validity of animal but the neural substrates underlying considered when translating findings models of adolescent alcohol con- these effects also exhibit across-species from animal studies to the neurological sumption and its consequences is an similarities. Numerous studies have substrates and consequences of alcohol ongoing, iterative process, as research identified sufficient similarities in use in humans. For example, electro- in these areas escalates in both human brain structure and function between physiological studies have suggested adolescents and laboratory animals. rodents and humans to support the that the medial PFC in the rat brain The current research supports cautious validity of animal models in assessing combines elements (i.e., the anterior optimism in the use of such models. the consequences of alcohol use on cingulate cortex and the dorsolateral For example, findings have shown the brain. For instance, consider the PFC) that are separated in the primate signs of consilience between human prefrontal cortex (PFC), a brain re- brain.12

78 | Vol. 39, No. 1 Alcohol Research: Current Reviews Animal Models of Adolescence Despite such similarities, there to later alcohol consumption. These are, of course, marked differences Adolescence—that is, the transition studies typically use alcohol exposure between humans and rodents in the levels that produce blood ethanol from dependence on parents to the duration of this developmental peri- concentrations of .08% or more—the independence of adulthood—is not od. Adolescence is relatively brief in level required to meet the definition unique to humans and is, to some rodents and in other mammals with for binge drinking specified by the extent, experienced by all mammals. a short life span. Adolescence in rats National Institute on Alcohol Abuse Similar biological changes, includ- has been estimated to last only about and Alcoholism23 (see Drinking ing alterations in the brain, are seen a month (i.e., postnatal day [P] 25 to Patterns and Their Definitions in across a variety of mammalian species P55), with early to mid-adolescence 13-15 this issue). Blood ethanol concentra- during adolescence. Adolescence- ending at about P42, and late adoles- tions in these studies often average 22 associated neural alterations include cence occurring from P43 to P55. .15% to .20%, which is well within regionally specific reductions in the The experimental designs used to study the binge-drinking range observed in number of synaptic connections be- adolescent alcohol use and its conse- field studies of human adolescents.24 tween and declines in the quences, such as analyses involving Usually, each alcohol exposure during relative volume of certain cortical and operant self-administration, must be 14 a rat’s adolescence is followed by a subcortical areas. Speed of informa- adapted to this relatively short time short period of abstinence before the tion flow across distant brain regions period. 14 next exposure period, a design some- increases, as does the reactivity of To ensure the face validity of mod- times called adolescent intermittent some subcortical brain regions, includ- els, experimental designs for modeling ethanol exposure (AIE). ing the NAc and amygdala.13,15 human alcohol use and its consequenc- Adolescence-associated changes in es in animals must consider human dopamine-terminal regions, such as drinking patterns. For example, alco- Cognitive and Behavioral Alterations the amygdala and NAc, are particularly hol misuse among human adolescents typically takes the form of binge Animal studies have helped identify important in the context of adolescent a variety of cognitive deficits resulting AOD use, because these regions are drinking on weekends rather than dai- ly drinking. This human adolescent be- from repeated adolescent alcohol expo- critically involved in processing and sure, particularly deficits in tasks that responding to rewarding, aversive, and havior can be modeled by intermittent alcohol exposure. However, alcohol are thought to require hippocampal emotionally arousing stimuli, 25 misuse among adults often involves functioning. Other identified deficits including social stimuli. In adolescents, reflect aspects of executive functioning, when compared with adults, these more regular drinking patterns, which may be better represented by more where prefrontal cortical brain regions brain regions often react in an continuous exposure models. are thought to play a particularly exaggerated way to motivational important role.16 Interestingly, the 13,15 Despite these constraints, judicious stimuli. In contrast, maturation use of animal models can complement observed effects are highly specific. of cognitive control regions in the studies in human adolescents and Learning of some less cognitively chal- PFC and other frontal regions occurs lenging tasks, such as passive avoid- 16 address questions that are ethically or gradually during adolescence. This technically not amenable to study in ance or simple operant conditioning maturational dissociation is thought to humans. Studies using animal models tasks, does not seem to be affected contribute to adolescent-characteristic have identified numerous functional by adolescent alcohol exposure.26,27 behaviors, such as increased risk-taking alterations associated with adolescent Alcohol-exposed animals sometimes 17 and exploratory drug use. alcohol use, as well as a variety of neu- exhibit deficits on more challenging Such developmental alterations ral alterations. tasks, such as conditional discrimina- have been observed in humans and in tion and object recognition tasks.28 animal models and have been matched For adolescent animals exposed to eth- by analogous behavioral changes in Functional Alterations anol, tasks that demand some degree various species. Adolescent rats, for Associated With Adolescent of cognitive flexibility or self-control instance, show more peer-directed Alcohol Exposure seem to be particularly vulnerable to interactions, novelty-seeking or performance impairment. These tasks risk-taking behaviors, and consumma- Studies of the lasting consequences include reversal learning,29 extinction, tory behavior; find social stimuli, novel of repeated alcohol exposure during and set-shifting tasks.30 Adolescent stimuli, and pleasant tastes particularly adolescence in animal models have alcohol exposure also is associated with reinforcing; and voluntarily consume identified numerous functional alter- a greater vulnerability to disruptions two to three times more alcohol than ations across domains, ranging from in spatial memory that are induced by adult rats.18-21 cognition and behavior, to affect, and ethanol challenge in adulthood.25

Binge Drinking’s Effects on the Developing Brain—Animal Models | 79 Other studies have assessed the studies, suggesting greater disinhibi- are often more sensitive to certain effects of AIE on risk-taking behav- tion, but to decrease open-arm time in desired effects of alcohol, such as its re- ior, impulsivity, and disinhibition, others, a pattern of findings consistent warding and social facilitating effects.47 all behavioral propensities that could with a profile of increased anxiety. It Adolescents are also usually sensitive to promote experimentation with AODs. is possible that adolescent alcohol ex- the disruptive effects of acute alcohol Such studies have demonstrated that posure can be characterized by profiles intoxication on learning and memo- animals with adolescent alcohol expo- of both increased anxiety and disin- ry.25 Collectively, adolescent-associated sure exhibited greater risk preferences hibition. Competition between these attenuated sensitivity to aversive effects on a probability-discounting task.31,32 propensities—depending, for example, and increased sensitivity to desirable AIE has been associated with increased on the perceived stressfulness of the effects of alcohol could contribute to impulsivity and greater disinhibition, as situation or the animals’ previous han- enhanced susceptibility to the initi- indicated by an increase in time spent dling—may explain these reliable but ation and escalation of alcohol use in open or lighted test areas.30,32-34 opposing outcomes.43 during adolescence,47 with intoxication having pronounced disruptive effects on learning and memory.25 Changes in Affect Retention of Adolescent Animals given repeated alcohol ex- Phenotypes Into Adulthood posure during adolescence often retain Animal studies also have demon- adolescent-typical phenotypes into strated changes in measures of affect in One surprising long-lasting con- adulthood.50 This persistence can be adult animals that were exposed to al- sequence of adolescent alcohol use observed through baseline behavioral, cohol as adolescents. For example, AIE observed repeatedly in AIE studies is cognitive, electrophysiological, and animals exhibited depression-like signs, the retention of adolescent phenotypes neuroanatomical assessments, as well such as reduced consumption of a sug- into adulthood. In rodent studies, as in the animals’ responses to alcohol ar solution or increased immobility in 51 35-37 adolescents have been shown to differ challenges in adulthood. For exam- a swim test. Similarly, alcohol ex- from adults in a variety of alcohol- ple, animals exposed to alcohol during posure during early to mid-adolescence related phenotypes. In instances where adolescence maintained an enhanced was associated with reliable increases researchers could assess similar effects sensitivity to alcohol’s rewarding 38,39 in social anxiety in adulthood. in human adolescents, the analyses and stimulatory effects into adult- Interestingly, this effect seems to be uncovered comparable age-related dif- hood.38,52-54 This persistent sensitivity sex-specific and is only observed in ferences.2 For example, like their hu- could promote alcohol consumption males. Other studies in male rats after man counterparts, adolescent animals in adulthood. In other studies, animals AIE have detected increases in general often voluntarily consume significantly that experienced AIE retained their anxiety, as indicated by decreased time more alcohol per drinking occasion adolescent-typical insensitivities to al- on the open arms (relative to time on than adults.18,44,45 This elevated alcohol cohol’s sedative, motor-impairing, and the closed arms) of an elevated plus intake is particularly notable in male aversive effects, which could permit the maze.37,40,41 However, increases in animals and mirrors intake by human maintenance of elevated alcohol drink- general anxiety have not always been adolescents.46 ing during adulthood.53,55-58 Also, the observed.36,42 Adolescents often differ from adults decline in sensitivity to alcohol-induced It is challenging to distinguish disin- in their sensitivity to alcohol’s effects, deficits in spatial working memory that hibition and anxiety in animal studies. with the direction of these differenc- normally occurs between adolescence For example, although the elevated es dependent on the effect studied. and adulthood did not occur in animals plus maze test was developed and val- Adolescents are less sensitive to many exposed to alcohol in adolescence.59 As idated as a test of anxiety, results from of alcohol’s undesired effects, such as a result, adult animals exposed to AIE it are sometimes interpreted in terms alcohol-induced motor impairment, retain adolescent-like vulnerability to of disinhibition. Increased time spent sedation, aversion, and social impair- alcohol-induced memory impairments in an environment that animals per- ment, which normally serve as cues and show more memory disruption ceive as more risky (i.e., the open arm to limit intake.47 Adolescents are also under the influence of alcohol than of an elevated maze) could indicate less sensitive to acute withdrawal (i.e., adults without a history of adolescent either greater disinhibition, decreased hangover effects) after moderate to alcohol exposure. anxiety, or some interaction of the high alcohol consumption. In animal Generally, retention of these adoles- two, with increases in disinhibition models, this effect has been reflected in cent phenotypes into adulthood is as- perhaps contributing to a suppression reduced levels of withdrawal-associated sociated with alcohol exposure during in anxiety.30,34 In studies of adolescent anxiety.48,49 In contrast to the attenuat- adolescence; equivalent alcohol alcohol exposure, AIE has been found ed sensitivity of adolescents to many of exposure during adulthood does not to increase open-arm time in some alcohol’s undesired effects, adolescents induce similar effects.55,58 Moreover,

80 | Vol. 39, No. 1 Alcohol Research: Current Reviews adolescent phenotypes are more that may reflect the persistence of (i.e., the strain of rats or mice used), pronounced if adolescent alcohol adolescent phenotypes is elevated al- amount and mode of adolescent alco- exposure is episodic, rather than cohol consumption during adulthood. hol exposure, and assessment method continuous, reflecting typical adolescent Findings are mixed as to whether of adult alcohol intake.43 Also, when binge-drinking consumption patterns.55 adolescent alcohol exposure increas- adolescent rats were given either a An episodic exposure pattern can es adult alcohol consumption. The sweetened alcohol solution or the result in withdrawal episodes following hypothesis is supported by findings sweetened solution without alcohol, each exposure, which could result in es- that alcohol-preferring rats given free both groups later increased intake only calating withdrawal signs (e.g., increased access to ethanol in their home cages of the solution they were exposed to anxiety-like behavior, lower seizure throughout adolescence acquired an during adolescence, not the alternate threshold, and more severe seizures), operant self-administration task for solution.70 This suggests that increased particularly in adolescents.60,61 alcohol in adulthood more quickly alcohol intake during adulthood after Researchers are trying to uncover than animals that did not have access consuming alcohol during adolescence the neurobiological mechanisms that to alcohol during adolescence.64,65 may reflect increased acceptability underlie the retention of adolescent Moreover, these animals exhibited of a familiar solution, rather than phenotypes after adolescent alcohol greater resistance to extinction of the alcohol-specific effects. Although the exposure. One line of investigation operant task, more spontaneous recov- existing data suggest that in some cases has explored whether animals exposed ery of self-administration, and elevated adolescent alcohol exposure can lead to to AIE retain into adulthood an response levels during reacquisition increased consumption during adult- immature balance of enhanced ex- of the operant task compared with hood, researchers still need to further citation to inhibition in the brain. animals with no history of alcohol ex- clarify the circumstances in which Some analyses have assessed the role of posure. Similar findings were obtained these intake-enhancing effects emerge. gamma-aminobutyric acid (GABA), in mice. Animals that had voluntary the major inhibitory neurotransmitter access to alcohol throughout adoles- in the brain. Studies found that in the cence consumed more alcohol as adults Neural Alterations , inhibitory effects of than mice whose access to alcohol was GABA responsible for baseline levels of delayed until adulthood.66 Rats ex- Alcohol exposure during adoles- tonic inhibition normally are attenuat- posed to alcohol through intermittent cence has detrimental and potentially ed in adolescents; however, after AIE, intraperitoneal administration in early long-lasting effects not only on cog- this attenuation is maintained into to mid-adolescence later exhibited in- nition, affect, and behavior, including adulthood.50,62 Ethanol potentiation of creased alcohol consumption, an effect future alcohol consumption, but also this tonic inhibition is more marked that was not apparent when alcohol on the structure and function of the in adolescents than adults—an effect exposure was delayed until late adoles- brain. Particularly pronounced effects that is maintained into adulthood after cence.41,67 include reductions in the formation AIE.50,62,63 These adolescent-typical The findings of increased adult con- of new brain cells (i.e., neurogene- neurophysiological characteristics and sumption levels following adolescent sis), long-lasting neuroinflammation, their persistence into adulthood may exposure are not universal, however. In changes in gene expression through contribute to alcohol’s enhanced some studies, adolescent rats exposed epigenetic mechanisms, and alterations memory-impairing effects in ado- to alcohol vapor, and mice or rats giv- in the activities of neurotransmitter lescents and to long-lasting memory en free access to alcohol in their home systems in several vulnerable brain impairment seen in adulthood after cages did not exhibit increased alcohol regions. AIE.51 More work is needed to identify consumption during adulthood.44,68,69 the overall prevalence of persistent Other researchers found that animals Neurogenesis and Cell Death adolescent-typical immaturities after ad- given free access during adolescence olescent alcohol exposure under various to alcohol through an operant task Adolescence is associated with a baseline and challenge conditions, and demonstrated no increased operant variety of neuroanatomical changes, to further characterize the mechanisms response during adulthood, although including enhanced neurogenesis in underlying these persisting effects. they did show increases in some some brain regions (e.g., the hippo- alcohol-related responses.30,42 campus).71 Reductions in the numbers Several variables may influence of neurons and in the connections Effects on Later Ethanol whether adolescent alcohol exposure between neurons (a process known as Consumption increases adult alcohol consumption, pruning) may occur in other regions of which may explain the diverse find- the brain (e.g., the PFC).72 One of the Another potential long-term conse- ings. These variables include the sex most consistent neurological findings quence of adolescent alcohol exposure of the animals, genetic background associated with adolescent alcohol ex-

Binge Drinking’s Effects on the Developing Brain—Animal Models | 81 posure is a reduction in neurogenesis roimmune genes that encode proin- Adolescent animals exposed to alcohol and a region-specific increase in cell flammatory signaling molecules.77 show alterations in histone acetylation, death and cell damage in the brain. Adolescent exposure also has been which, in turn, influences DNA meth- The regions most commonly affected shown to activate Toll-like receptor 4 ylation and the level of gene expres- include the frontal cortex, hippocam- (TLR4), a receptor in the innate im- sion.41,78,79 Such epigenetic alterations pus, amygdala, NAc, and cerebel- mune system that plays a central role have been identified in the amygdala, lum—regions that also undergo signif- in initiating innate immune responses NAc, and PFC, which are brain struc- icant developmental changes during throughout the body.77 Ethanol- tures involved in memory processing, adolescence.71,73-75 The adolescent induced TLR4 activation triggers the decision-making, and emotional reac- brain seems to be particularly vulner- expression of various transcription fac- tions. For example, rats with AIE ex- able to the effects of alcohol exposure tors that, in turn, promote the expres- hibited persistent increases in histone because similar disruptions were not sion of proinflammatory cytokines and deacetylation and reductions in histone observed after equivalent exposure in other mediators of inflammation. In acetylation in the amygdala,41 resulting adulthood.73 The effects of binge-like the short term, such proinflammatory in reduced expression of certain genes exposure during adulthood occurred in responses may be adaptive. However, (e.g., brain-derived neurotrophic factor different regions of the brain and were when these responses are maintained [BDNF]). When the alcohol-induced less pronounced than the effects of ex- over longer periods, the result is deacetylation was prevented by treat- posure during adolescence.74 long-lasting neuroinflammation. ment with a histone deacetylase inhib- Adolescent alcohol exposure affects In the brain, ethanol-induced ac- itor, histone acetylation levels in the not only the overall number of brain tivation of TLR4 and its subsequent amygdala normalized, and the tran- cells in specific brain regions but also actions can contribute to brain damage scription of BDNF was restored.41 The their connections with each other. associated with excessive alcohol expo- effects of AIE on histone acetylation Recent studies investigated the effects sure.77 For example, in animal studies, levels also may contribute to observed of AIE on the structure and function activation of TLR4 using a bacterial behavioral and neural effects of AIE. of synapses in the hippocampus, a compound (i.e., lipopolysaccharide) Treatment with the deacetylase inhib- brain region associated with learning induced a long-lasting reduction in itor attenuated anxiety-like behaviors, and memory.76 The analyses found that neurogenesis similar to that observed reversed the increase in alcohol intake AIE resulted in a greater proportion of after AIE.71 In mice that did not pro- during adulthood, and normalized the immature relative to mature dendritic duce TLR4, adolescent alcohol expo- decline in neurogenesis usually exhibit- 41,80 spines (specialized sites on neurons sure did not result in the characteristic ed by AIE animals. that receive and amplify input from inflammatory, cognitive, and behavior- signal-emitting neurons) in the brains al consequences usually associated with Neurotransmitter Systems of AIE animals compared with those this exposure.40,77 of nonexposed adult animals. Animals The role of TLR4 and neuroinflam- Alcohol exerts its dose-dependent with AIE also manifested more robust mation in the functional and neural and region-specific effects largely long-term potentiation as adults when consequences of adolescent alcohol through direct or indirect interactions they were compared with nonexposed exposure is supported by findings that with the major neurotransmitter and animals, a pattern of neurophysiolog- treatment with an anti-inflammatory neuromodulatory systems in the brain, ical activation similar to the pattern compound (i.e., indomethacin) including the GABA system discussed normally seen in adolescents. Long- prevented the typical cell death and earlier, as well as the dopamine, sero- tonin, glutamate, acetylcholine, and term potentiation is the strengthening behavioral deficits seen after AIE.28 endocannabinoid systems.81 However, of synaptic connections when the These observations suggest that there is specificity in these effects, and synapses are repeatedly activated. anti-inflammatory agents may repre- not all systems and brain regions are Although this process is necessary sent a new class of pharmacotherapeu- equally vulnerable. Many of these for learning, greater than normal tic interventions for preventing, ame- alcohol-sensitive neurotransmitter and long-term potentiation has been liorating, or even reversing some of the neuromodulatory systems and affected linked to memory deficits and other long-term consequences of adolescent 76 brain regions undergo developmental learning-related behavioral changes. alcohol exposure. transformations during adolescence, and they may be especially vulnera- Neuroinflammation Epigenetic Mechanisms ble to alcohol-induced perturbations during development. Indeed, AIE Adolescent alcohol exposure has Adolescent alcohol exposure also has been shown to be associated with been shown to induce long-term influences gene expression by modify- alterations in several of these systems, increases in expression of several neu- ing epigenetic regulatory mechanisms. including:

82 | Vol. 39, No. 1 Alcohol Research: Current Reviews • Changes in the activity of the that adolescent alcohol exposure ative and aversive effects) that likely dopamine system in the NAc. impairs the normal cholinergic neu- serve as cues to terminate intake. Several studies have reported rotransmission in the basal forebrain Animal studies have shown that re- enhanced dopamine function that is crucial for ensuring cortical peated exposure to alcohol during ad- in neurons projecting to the plasticity and learning. Hence, AIE- olescence, especially AIE that mirrors NAc, a pivotal component of the induced deficits in the cholinergic binge-drinking patterns observed in brain’s reward system, following system may contribute to future human adolescents, induces specific AIE. These neurons exhibited cognitive deficits. patterns of sustained neurobehavioral increased dopamine-mediated Repeated alcohol use during ado- alterations that may promote further neurotransmission under normal lescence induces specific alterations in drinking. Particularly worrisome conditions and after an alcohol a variety of neural systems that play are reports that adolescent alcohol challenge.78,82,83 The neurons also critical roles in neural, cognitive, and exposure may lead to the retention exhibited higher basal extracellular behavioral function. It is possible that of adolescent phenotypes—includ- dopamine levels.78,84 Given the some of these neural alterations reflect ing adolescent-typical responses to critical role that dopamine plays positive adaptations to AIE to mitigate alcohol—into adulthood. Other in facilitating reward-related cognitive, behavioral, and affective motivation and behaviors, these long-term consequences of the alcohol exposure. Yet, these potential compen- consequences have been reported findings suggest that AIE may after AIE, including impaired per- enhance the rewarding experiences sations do not appear to be sufficient, given the growing list of long-term formance of executive functions, associated with alcohol, which could memory impairment, reduced cogni- promote further alcohol ingestion. consequences of AIE on later neuro- cognitive and behavioral function. tive flexibility, greater risk preference • Changes in the activity of the and disinhibition, and elevated social glutamate system. Glutamate is the (and sometimes general) anxiety. In primary excitatory neurotransmit- Conclusions and many cases these effects are specific to ter in the brain and acts via several Future Directions adolescent alcohol exposure and are types of receptors, including the not evident after equivalent alcohol N-methyl-D-aspartate (NMDA) Adolescence is characterized by so- exposure during adulthood. receptor. AIE has been reported to cial and emotional development and Animal studies also have identified increase NMDA receptor binding often is accompanied by experimenta- lasting neural alterations induced by in the frontal cortex, as well as the tion with AODs. Brain development AIE that may contribute to behav- expression of one subunit of this continues during adolescence, and, in- ioral and cognitive changes. These receptor (i.e., the NR2B subunit).85 creasingly, adolescence is being viewed changes include reduced neurogen- Other research has reported a as a period of enhanced brain plasticity esis, increased neuroinflammation, decrease in the subunit’s phosphor- and experience-related brain sculpting. epigenetic alterations, and alterations 78 ylation. Altered NMDA function- Many adolescent experiences (e.g., in numerous neurotransmitter sys- ing in the PFC has been suggested education, sports, and positive social tems, including glutamate, GABA, to disrupt functioning of that brain interactions) provide beneficial long- the balance between these excitatory region and to contribute to the term sculpting. Other influences, such and inhibitory systems, dopamine, impulsive behavior and the lack of as repeated exposure to alcohol, can and the basal forebrain cholinergic control over drinking that is charac- system. When different age groups 78 be detrimental and have long-term ef- teristic of individuals with AUD. fects on neural functioning, cognition, were compared, the consequences • Changes in the acetylcholine and behavior, including enhanced typically were more pronounced system in the basal forebrain. AOD consumption, that persist into after adolescent alcohol exposure One reliable consequence of AIE adulthood. than after equivalent adult exposure. observed in rodent studies is a Studies conducted primarily using Likely anatomical targets for these long-lasting decrease in the basal rodent models of adolescence have long-term effects include the hippo- forebrain of the number of neu- shown that propensity for the initi- campus, amygdala, NAc, and PFC. rons that exhibit activity of the ation and escalation of alcohol use These neural systems underlie the choline acetyltransferase enzyme, during adolescence may be promoted developmental shifts in sensitivity to which is required for synthesis of by adolescents’ greater sensitivity to drug rewards and drug aversion that the neurotransmitter acetylcholine. the socially facilitating and rewarding normally occur during adolescence This effect is seen following adoles- effects of alcohol, combined with a re- and adulthood. These systems are cent, but not adult, alcohol expo- duced sensitivity to other effects (e.g., also involved in neurodevelopmental sure.29,31,36,86 These findings suggest social and motor impairment, and sed- processes related to socioemotional

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86 | Vol. 39, No. 1 Alcohol Research: Current Reviews ALCOHOL RESEARCH: Current Reviews Effects of Binge Drinking on the Developing Brain

Studies in Humans

Scott A. Jones, Jordan M. Lueras, and Bonnie J. Nagel Scott A. Jones and Jordan M. Lueras are graduate students in Binge drinking is a pattern of alcohol drinking that raises a person’s blood alcohol the Department of Behavioral concentration to at least .08%, which amounts to consuming five alcoholic drinks for Neuroscience, Oregon Health men and four alcoholic drinks for women in about 2 hours. It is the most common & Science University, Portland, form of alcohol misuse in adolescents and young adults. Heavy drinking includes the same criterion as binge drinking, but with higher frequency (i.e., 5 or more days in the Oregon. past 30 days). Although binge drinking or heavy drinking alone is insufficient to meet the criteria for an alcohol use disorder (AUD) diagnosis, there are neurobiological Bonnie J. Nagel, Ph.D., is an changes, as well as an increased risk of developing an AUD later in life, associated associate professor in the with this form of alcohol misuse. This review describes the recent neuroimaging find- Departments of Behavioral ings in binge drinking and heavy-drinking adolescents and young adults, a develop- Neuroscience and Psychiatry, mental period during which significant neuromaturation occurs. Oregon Health & Science University, Portland, Oregon. Key words: Alcohol misuse; binge drinking; college drinking; neurodevelopment; neuroimaging; young adults

It has been well established that the involved in reward and emotional pro- in the United States reported binge brain undergoes significant matura- cessing.6,10,11 The asynchronous devel- drinking.21 Heavy drinking includes tion during adolescence that continues opment of the prefrontal cortex and the same criterion as binge drinking, into young adulthood.1 Studies using emotional and reward circuitry has but with higher frequency (i.e., 5 or structural magnetic resonance imaging been hypothesized to result in more days in the past 30 days).21 In have described linear and nonlinear increased risk-taking behavior during the National Survey on Drug Use and changes in cortical gray-matter volume adolescence, such as alcohol use.12-15 Health, 257,000 adolescents (1%) and thickness2-5 and increases in This is especially of concern because and 3.8 million young adults (10.8%) white-matter volume and integrity2,6-9 ongoing neurodevelopment may ren- reported heavy drinking.21 Although occurring during development. Gray- der the adolescent brain particularly binge or heavy drinking alone is insuf- matter volume peaks earlier in females vulnerable to the neurotoxic effects of ficient to meet criteria for an alcohol (i.e., around age 11) than in males alcohol, as has been shown repeatedly use disorder (AUD) diagnosis, there (i.e., around age 12) and declines in animal models.16-19 are neurobiological changes, as well during adolescence due to pruning of Binge drinking is a pattern of al- as an increased risk of developing an unused synaptic connections in order cohol drinking that raises a person’s AUD later in life, associated with this to promote efficient communication blood alcohol concentration to at least form of alcohol misuse.22 This article between neurons.6 Furthermore, gray .08%, which amounts to consuming reviews neuroimaging studies assessing matter has been shown to reach earlier five alcoholic drinks for men and four the effects of binge and heavy drink- maturation in the sensorimotor corti- alcoholic drinks for women in about ing on brain structure and function ces, whereas the frontal and temporal 2 hours.20 It is the most common in adolescents. Studies in which par- cortices mature later in development.4 pattern of alcohol consumption in ticipants met criteria for AUD were The prefrontal cortex, which is central adolescents and young adults. As of not included. Further, the age range to executive control, matures later 2014, 1.5 million adolescents ages included studies in adolescents and compared with earlier developing lim- 12 to 17 (6.1%) and 13.2 million young adults, which extends up to a bic structures thought to be more young adults ages 18 to 25 (37.7%) mean age of 25, because brain matu-

Effects of Binge Drinking on the Developing Brain | 87 ration continues to occur well into the ume, and that these changes often are resonance imaging scan when the late 20s.2 associated with alcohol drinking char- subjects were alcohol naïve and a acteristics. follow-up scan approximately 3 years Contrary to findings of smaller later, after binge drinking. At baseline, Effects on Brain brain volumes, Howell and colleagues adolescents who later transitioned Structure—Gray Matter reported greater ventral striatal, tha- into heavy drinking had smaller ACC, lamic, and lingual-gyrus volumes in posterior cingulate cortex, and inferior college-age binge drinkers compared frontal gyrus (IFG) gray-matter vol- 24 27 Volume with control subjects. A study on umes. Furthermore, heavy-drinking binge drinking, college-age participants adolescents showed accelerated reduc- Cross-sectional studies in binge also found increased frontal, occipital, tions in the thalamus/hypothalamus, drinking adolescents and college-age anterior cingulate cortex (ACC), and inferior temporal gyrus, middle tempo- individuals have demonstrated regions posterior cingulate cortex volumes ral gyrus (miTG), caudate, and brain of both more and less gray-matter compared with nondrinking control stem, with greater lifetime alcohol use volume compared with nondrinking subjects.26 In this study, larger dor- associated with a greater reduction in peers, with volumes often related to solateral prefrontal cortex (DLPFC) gray-matter volume in the left caudate frequency and quantity of alcohol volumes were positively associated and brainstem.27 consumption. For example, a recent with speed and quantity of alcohol A follow-up to this study that in- study found that adolescents and consumption and negatively associated vestigated gray-matter volumes in young adults who consumed mod- with age of onset of alcohol use.26 It heavy-drinking adolescents at base- erate to high levels of alcohol had is worth noting that these individuals line and during multiple follow-ups smaller total-brain, frontal-lobe, and reported binge drinking for a mini- found that heavy drinkers exhibited temporal-lobe volumes than their mum of 3 years prior to neuroimaging greater reductions in overall neocortex nondrinking peers; however, they also sessions, suggesting that volumetric volume, as well as in frontal, lateral found that a greater number of lifetime increases in regional gray matter may frontal, and temporal cortex volumes.28 drinks was positively associated with be associated with long-term binge Finally, Whelan and colleagues used greater temporal-lobe volume.9 In sup- drinking. machine-learning techniques to classify port of the notion that binge drinking In addition to these disparate adolescents before and after initiation is associated with lower gray-matter findings in gray-matter volume, sex- of binge drinking.29 They reported that volume, a study of college-age binge specific effects also have been observed before alcohol use, binge drinking ado- drinkers found that higher Alcohol in college-age binge drinkers. Kvamme lescents had lower gray-matter volume Use Disorders Identification Test and colleagues noted a significant in the superior frontal gyri (SFG) and (AUDIT) scores, indicative of greater sex-by-drinking status interaction greater volume in the premotor cortex reported frequency and quantity of al- in numerous prefrontal, parietal, compared to nondrinking control sub- cohol consumption and alcohol-related temporal, and striatal regions, such jects. After alcohol initiation, however, problems, were associated with smaller that binge drinking males had smaller smaller ventral medial prefrontal cortex frontal-lobe volumes.23 An associa- volumes than alcohol-naïve males, (PFC) and IFG volumes were observed tion between alcohol use and smaller whereas binge drinking females had compared with nondrinking controls.29 gray-matter volume also was supported larger volumes than alcohol-naïve Taken together, these findings suggest by another study that identified small- females.23 Although these sex-specific that binge drinking during develop- er precuneus volumes in a group of effects partially may explain the ment may result in accelerated decreas- college-age binge drinkers compared bidirectional effects seen in previous es in gray-matter volume, above and with alcohol-naïve controls.24 Further, studies, there are likely many other beyond what is seen in typical matu- greater AUDIT scores again were factors that could contribute to these ration, likely caused by the neurotoxic associated with smaller gray-matter disparate findings, including the effect of alcohol. It also is possible, volumes in the amygdala and hippo- inability of cross-sectional designs based on evidence from cross-sectional campus.24 Additionally, among binge to capture alterations in nonlinear studies in college-age individuals (de- drinking adolescents, greater peak developmental trajectories.2-5 scribed above), that a longer duration number of drinks in the past 3 months To better address volume-related of alcohol use into young adulthood was associated with decreased cerebel- changes associated with drinking, lon- may result in greater gray-matter lar gray-matter volume.25 Together, gitudinal studies have begun to inves- volumes in young adults who binge these findings suggest that binge drink- tigate gray-matter volume both before drink, potentially because of impaired ing during development is associated and after binge drinking. The first of synaptic pruning. Additional longitu- with various regions of lower cortical, such studies examined heavy-drinking dinal studies with multiple time points subcortical, and cerebellar brain vol- adolescents with a baseline magnetic will be necessary to elucidate alcohol’s

88 | Vol. 39, No. 1 Alcohol Research: Current Reviews effects on the full developmental tra- sex differences in the rate and timing the equivocal findings in gray-matter jectory across adolescence and young of synaptic pruning in adolescents.6 volume described above. In fact, in the adulthood. In a longitudinal investigation of longitudinal study by Squeglia and col- the effects of binge drinking on corti- leagues, although a greater number of Cortical Thickness cal thickness, Luciana and colleagues lifetime alcohol-use occasions was asso- found that adolescents who initiated ciated with greater reductions in cau- Generally, studies investigating alcohol use showed a significantly date and brainstem volume, a greater cortical thickness in binge drinking greater decrease in middle frontal gyrus number of lifetime marijuana uses was adolescents have supported findings (miFG) cortical thickness between associated with increases in caudate of decreases in gray matter. Similar baseline and revisit compared with volume.27 This provides further evi- to their gray-matter volume findings adolescents who remained alcohol dence that although gray-matter vol- noted above, Pfefferbaum and col- naïve,32 suggesting that alcohol has a ume and thickness typically decrease in leagues noted that alcohol-consuming neurotoxic effect on devel- binge drinking adolescents and young adolescents had thinner total, frontal, opment. However, this study found no adults, concomitant marijuana use temporal, and cingulate cortices than differences in cortical thickness prior may result in observed increased vol- nondrinkers; moreover, the number of to initiation of alcohol use, contrary ume and thickness. binge drinking episodes in the past year to a subsequent study observing differ- was negatively associated with frontal ences in baseline gray-matter volume.27 9 and parietal cortex thickness. This Other studies have investigated the Effects on Brain Structure— finding is in agreement with another effects of binge drinking on cortical White Matter cross-sectional study of young adults, thickness in a longitudinal manner, which determined that binge drinkers but without an alcohol-naïve baseline. had thinner cortical measures in the Jacobus and colleagues examined cor- ACC and posterior cingulate cortex tical thickness over 3 years and found Volume compared with light drinkers (i.e., con- that concomitantly binge drinking and As opposed to the varied findings suming one or two drinks per week, marijuana using adolescents had thick- 30 in gray-matter volume, results in but no binge episodes). Further, er cortices across time in five frontal, white-matter volume have been more ACC cortical thickness was negatively eight parietal, one temporal, and parsimonious. Cross-sectional studies correlated with the number of drinking one occipital region compared with have shown that a greater number of occasions and number of drinks per oc- alcohol- and marijuana-naïve control lifetime drinks was associated with casion in the past 3 months, indicating subjects.33 Moreover, in three frontal smaller central white-matter volume,9 that greater frequency and quantity of regions, control subjects showed a de- and peak number of drinks during a 30 use is associated with thinner cortices. crease in cortical thickness across time, binge episode in the past 3 months Similar to the volumetric study pre- whereas concomitantly binge drink- was associated with smaller cerebellar viously cited, sex-specific effects also ing and marijuana using adolescents volumes.25 Longitudinal studies tell a have become apparent when investigat- did not. A prior study had suggested similar story, with binge drinking ado- ing cortical thickness in binge drink- that these effects persisted following lescents showing reduced white-matter ing adolescents.23 A cross-sectional abstinence, because concomitantly volumes both before27 and follow- study in binge drinkers identified binge drinking and marijuana using ing initiation of binge drinking.28,32 sex-by-drinking status interactions for adolescents showed greater thickness Squeglia and colleagues found that cortical-thickness measures in four in the ACC, medial temporal gyrus, heavy-drinking adolescents had lower frontal regions (i.e., frontal pole, pars lingual gyrus, and occipital cortex both baseline cerebellar white-matter vol- orbitalis, medial orbital frontal, and before and after 28 days of monitored umes compared with control subjects, rostral anterior cingulate). Thus, binge abstinence.34 but the investigators identified no drinking males had thinner cortices Taken together, these studies suggest regions where white-matter volume than alcohol-naïve control subjects, that, when combined with marijua- changed differentially across time.27 whereas binge drinking females had na use, binge drinking may result in However, in a follow-up study, thicker cortices than alcohol-naïve increases, as opposed to decreases, in heavy-drinking adolescents exhibited control subjects.31 The directionality of cortical thickness, that these increases significantly attenuated white-matter these findings is consistent with those are cumulative with prolonged use, growth in the pons and corpus callo- of Kvamme and colleagues.23 The find- and that they persist even following sum between baseline and follow-up ings suggest that during this particular a month of abstinence. Furthermore, scans, compared with controls.28 window of development, alcohol may although these studies contradict Luciana and colleagues reported sim- have differential effects for boys and some literature,9,30,32 they may help ilar findings, such that alcohol-naïve girls, likely resulting from underlying provide an alternative explanation for controls showed an increase in vol-

Effects of Binge Drinking on the Developing Brain | 89 ume in white-matter regions of the stance using adolescents found that control subjects.39 Moreover, lower precentral gyrus, miTG, SFG, and binge drinking adolescents, again, FA in the fornix and SCR at baseline lingual gyrus between baseline and had lower FA than control subjects in in concomitant binge drinking and follow-up, whereas binge drinking eight different regions, including the substance using adolescents predict- adolescents did not.32 Taken together, superior corona radiata (SCR), infe- ed greater subsequent use at the first these observations suggest that reduced rior longitudinal fasciculus, superior follow-up, above and beyond baseline white-matter volume may precede al- longitudinal fasciculus (SLF), inferior substance use.40 It is important to note cohol use, and that alcohol use during fronto-occipital fasciculus (IFOF), that in these two studies,39 adolescent adolescence attenuates the typical and cerebellar peduncle.37 Those with binge drinkers and substance users maturational increase in white-matter concomitant substance use, in con- were not drug and alcohol naïve at volume observed in adolescence in a trast, only had significantly lower FA baseline; rather, they were drinking dose-related fashion.2,6-8 (compared with control subjects) in and using marijuana throughout the three regions, including the SCR and entirety of the study. Lastly, Jacobus SLF, and they had significantly higher and colleagues identified 20 regions in Microstructure FA than binge drinking adolescents the brain where there was a significant in four regions (i.e., the SCR, SLF, group-by-time interaction, such that Varied differences in white-matter IFOF, and cerebellar peduncle). In this microstructure have been observed be- adolescents who used both alcohol and study, greater marijuana use frequency marijuana concomitantly showed a tween binge drinking adolescents (with was associated with greater FA in the and without concomitant marijuana sharper decline in FA between baseline SCR and SLF, whereas a greater num- and 3-year follow-up than those who use) and non–alcohol using controls. ber of lifetime drinks was associated 41 First, a cross-sectional diffusion tensor only binge drank. In combination, with greater FA in the SLF. Together, these findings suggest that whereas imaging study investigating fractional these findings suggest that binge drink- anisotropy (FA)—a measure thought binge drinking during adolescence and ing during adolescence is associated young adulthood appears to be associ- to reflect white-matter myelination with reduced FA, but that concomi- and axonal integrity and coherence— ated with reduced FA, results tend to tant marijuana use may interact with be less clear when adolescents concom- found that binge drinking adolescents the effects of alcohol, resulting in an itantly use marijuana. Whereas Jacobus had lower FA than control subjects in alteration of this effect. and colleagues found that binge seven frontal, three parietal, two tem- These cross-sectional findings have drinkers with concomitant marijuana poral, four subcortical, and two cere- been corroborated by numerous longi- use initially had had greater FA than bellar regions. Furthermore, in six of tudinal studies. Luciana and colleagues those who only binge drank,37 a longer these regions, lower FA was associated reported that compared with control history of concomitant marijuana use, with significantly greater lifetime hang- subjects, adolescent binge drinkers extending into young adulthood, may over symptoms and higher estimated showed significantly diminished nor- eventually result in a steeper decline in peak blood alcohol concentrations.35 mative increases in FA in the dorsal FA across development.41 In a second cross-sectional study, caudate and IFOF between baseline concomitant binge drinking and sub- and follow-up visit.32 Another study stance using adolescents had lower FA found that concomitant binge drink- Effects on Brain Function than control subjects in 10 separate ing and substance using adolescents frontal, parietal, temporal, and subcor- had reduced FA in the corpus callo- tical regions, and reduced FA in these sum, prefrontal thalamic fibers, and Verbal Encoding regions was associated with greater posterior corona radiata at follow-up, lifetime alcohol use.36 Interestingly, the compared with control subjects, with Learning and memory abilities are investigators also noted three regions no differences reported at baseline.38 crucial for an adolescent’s success, and (i.e., the superior longitudinal fascic- A series of studies examined FA in a development of those abilities may be ulus, internal capsule, and occipital group of binge drinking and concom- altered or attenuated by alcohol use. lobe) where FA was greater in con- itant binge drinking and substance Verbal encoding/learning, using a comitant binge drinking and substance using adolescents and young adults at verbal paired-association task, has been using adolescents than in control baseline and follow-up.39-41 First, they used to investigate the impact of alco- subjects, and they found that greater found that binge drinking adolescents hol on learning and memory in binge FA in these regions was associated with both with and without concomitant drinking adolescents with and without greater lifetime alcohol use. substance use showed a significant, comorbid marijuana use. A prelimi- Finally, a third cross-sectional study widespread decline in FA across the nary study found that binge drinking of binge drinking adolescents and three visits, resulting in lower FA adolescents had greater activation concomitant binge drinking and sub- after 3 years of use compared with in the SFG, superior parietal lobule,

90 | Vol. 39, No. 1 Alcohol Research: Current Reviews inferior parietal lobule (IPL), and the subsequent study showed that binge males showed greater activation cingulate, as well as lower activation in drinking adolescents had greater than control subjects in the SFG, one cluster encompassing the cuneus, activation in the medial frontal gyrus IFG, ACC, miFG, miTG, superior precuneus, lingual gyrus, and parahip- (meFG), SFG, IPL, and supramarginal temporal gyrus, and cerebellum. pocampal gyrus (PHG) during novel gyrus, as well as less activation in These findings suggest that, in general, word encoding.42 the middle occipital gyrus, when adolescents show alcohol-related In a follow-up investigation, compared with control subjects.45 increases in activation, particularly Schweinsburg and colleagues found Furthermore, in longitudinal analyses, in fronto-parietal networks during that binge drinking and concomitant binge drinking adolescents actually had working memory; however, at least binge drinking and substance using lower activation in the IPL and meFG for spatial working memory, these adolescents, when compared with at baseline (i.e., prior to drinking), but findings may be sex specific. Further marijuana-only users and control sub- when compared with control subjects, work is necessary to tease out the jects, showed greater encoding-related they showed a greater increase across different elements (e.g., spatial versus activation in the postcentral gyrus, time. These greater increases in brain verbal) of working memory and the IPL, and SFG, and less activation in activation were associated with a effects of alcohol on their associated the fusiform gyrus, PHG, cuneus, greater peak number of drinks in the neural responses. precuneus, IPL, IFG, precentral gyrus, past year, more past-month drinking and cingulate.43 They also identified days, and greater withdrawal/hangover Risk Taking and Reward Response regions of the brain (i.e., the IFG, symptoms at follow-up.45 Further, less miFG, SFG, and cuneus) where users premorbid activation in the meFG Because adolescence is a time of of either alcohol or marijuana showed and IPL predicted a higher peak increased risk taking, including exper- greater brain response than nonusers number of drinks and drinking days imentation with alcohol, it may come during novel word encoding, whereas in the year preceding follow-up.45 This as no surprise that binge drinking ad- users of both substances resembled suggests that binge drinking not only olescents show altered brain response nonusers. Because performance on affects neural response during working during various phases of risk taking. the task was the same between binge memory, but that baseline differences Whereas some investigators have drinkers and control subjects,42,43 in brain activation during working attempted to elucidate binge drink- memory may be useful in identifying ing’s effects on a particular aspect of these findings suggest that alcohol 48-50 use during adolescence may cause adolescents who may go on to drink. risk-taking behavior, others have These findings also are supported investigated risk taking more broad- adolescents to adopt a different neural 51 strategy (e.g., heavier prefrontal-cortex by cross-sectional work using other ly. In a study looking at risk-taking recruitment) to achieve the same suc- working memory tasks. One study behavior using the Iowa Gambling cessful verbal encoding. Because of the found that during verbal working Task, binge drinking adolescents had cross-sectional design, it is unknown memory, binge drinking young greater risk-related activation in the whether these differences were present adults had greater activation in the amygdala and insula compared with parietal cortex (pre–supplementary control subjects, and they had more prior to or developed as a consequence 46 of alcohol consumption. motor area) than control subjects. reported drinking problems related Moreover, more drinks per drinking to less activation in the orbitofrontal occasion were associated with greater cortex (OFC) and more activation in 51 Working Memory dorsal medial PFC activation, the insula. Two recent studies sepa- whereas more drinking occasions per rately investigated the effects of binge Brain response during working week were associated with greater drinking during adolescence during memory also has been shown to be cerebellar, thalamic, and insular decision making and reward receipt. In altered in binge drinking adolescents activation. In contrast, Squeglia and the first study, binge drinking adoles- and young adults. In a preliminary colleagues reported that binge drinking cents, compared with control subjects, study, Tapert and colleagues found adolescents had lower activation in showed reduced cerebellar response that brain response during a visual the SFG and IFG compared with during reward receipt following initi- working memory task was negatively control subjects.47 However, this study ation of binge drinking, a finding that associated with subjective response differed in two ways from the previous remained significant when controlling to alcohol, such that adolescents studies. Squeglia and colleagues for premorbid activation, and which who reported that a greater quantity used a spatial working memory task was associated with more drinks per of alcohol was needed to feel an and also reported significant sex drinking day in the past 90 days.48 effect showed greater activation in differences, such that binge drinking A longitudinal investigation found the SFG, cingulate, cerebellum, and females showed less activation than that binge drinking adolescents, com- PHG during memory retrieval.44 A control subjects, and binge drinking pared with control subjects, had lower

Effects of Binge Drinking on the Developing Brain | 91 activation in the IFG, IPL, miTG, with alcohol-related alterations in baseline and follow-up were associated and superior temporal gyrus across brain response during decision making with more lifetime drinks. The same time, suggesting a different pattern and reward/consequence notifica- group of researchers also found that of brain activation that occurs prior tion. Further, group differences in these patterns of activation differed in to binge drinking and persists after fronto-parietal brain response during adolescents who experienced alcohol- alcohol initiation.49 There also was a risky decision making and reward induced blackouts. Prior to initiation significant group-by-time interaction receipt that occur prior to drinking of heavy drinking, adolescents in the dorsal caudate, such that binge may serve as a risk factor for future who did and did not experience drinking adolescents showed similar drinking.29,49 alcohol-induced blackouts showed risky decision-making–related brain less activation in the IPL compared responses as controls at baseline, but with control subjects.55 However, they showed a reduced response fol- Inhibition adolescents who went on to experience lowing binge drinking. This reduction Several longitudinal studies have alcohol-induced blackouts showed was associated with a greater number used a standard go/no-go procedure greater activation during inhibition of drinking days and heavy drinking to investigate the effects of binge in the miFG, miTG, cerebellum, and days in the previous 3 months. drinking on brain response during parietal cortex (pre–supplementary Further, Worbe and colleagues used inhibition. One study found that, at motor area) compared with those a novel risk-taking gambling task in baseline, adolescents who went on to who did not experience blackouts. binge drinking young adults to in- engage in heavy drinking had reduced These findings suggest that adolescents vestigate brain responses during the brain response during successful in- who later experience alcohol-induced decision-making and feedback phases hibition in the DLPFC, miFG, SFG, blackouts show patterns of brain of both reward and loss gambles.50 IFG, meFG, paracentral lobules, activation during inhibition, which During decision making in conditions cingulate, putamen, miTG, IPL, and may render them more vulnerable with both a low and high potential pons, compared with adolescents who to the memory-impairing effects for a loss, the study found that binge remained alcohol naïve.52 In another of alcohol. drinkers had greater activation in the study, less activation during success- Lastly, a recent study in binge drink- OFC, superior parietal cortex, and ful inhibition in the ventral medial ing young adults found that those who DLPFC compared with control sub- PFC predicted more alcohol depen- escalated drinking over a 12-month jects. This finding was accompanied by dence symptoms in heavy-drinking period had greater fronto-parietal ac- more risky decisions during high-loss adolescents at 18-month follow-up.53 tivation during inhibition compared selections. Furthermore, although giv- Meanwhile, in a study investigating with young adults who maintained ing feedback during the task reduced the failure to inhibit responding, great- stable drinking levels.56 Taken togeth- the amount of risky decisions in binge er activation in the premotor cortex er, it appears that hypoactivation of drinking young adults, it also was asso- served as a risk factor for adolescents the fronto-parietal network during ciated with greater activity in the IFG who later went on to engage in binge inhibition may serve as a risk factor for and IPL, when compared with control drinking.29 Together, these studies alcohol use initiation; however, after subjects. suggest that lower engagement of nu- alcohol use initiation, hyperactivation In addition to studies looking at merous regions, particularly within the of the fronto-parietal network during adolescent risk-taking behavior, a fronto-parietal network, during suc- inhibition may serve as a risk factor for study by Whelan and colleagues inves- cessful inhibition, as well as greater en- escalation of drinking. tigated brain responses during reward gagement of premotor regions during anticipation and receipt outside of the unsuccessful inhibition, may precede Cue Reactivity context of risk, using the monetary in- the onset of binge drinking. centive delay task.29 The study demon- Furthermore, compared with Two recent studies have looked at strated that, compared with control alcohol-naïve control subjects, heavy- brain activation elicited by an alcohol subjects, adolescent binge drinkers had drinking adolescents were shown to cue (i.e., cue reactivity), using an al- greater activation during reward re- have significantly lower levels of brain cohol pictures task, in binge drinking ceipt in the SFG prior to initiation of activation during inhibition in the adolescents and young adults. Dager binge drinking, but they had reduced miFG, IPL, putamen, and cerebellum and colleagues found that young adults activation during reward anticipation at baseline.54 They also showed greater who transitioned from moderate to and receipt in the ventral medial PFC increases in inhibition-related brain heavy drinking over a 1-year follow-up and IFG after binge drinking. Taken responses, compared to controls, had greater activation at baseline in together, these findings suggest that following initiation of heavy drinking. the caudate, ACC, medial prefrontal binge drinking during adolescence Greater increases in brain response cortex, precentral gyrus, insula, IFG, and young adulthood is associated during response inhibition between and OFC, compared with those who

92 | Vol. 39, No. 1 Alcohol Research: Current Reviews remained moderate drinkers or heavy and white matter, resulting in poorer greater impulsivity in adolescent binge drinkers throughout the study.57 sustained attention. drinkers has been shown to be associ- Furthermore, brain activation in this Furthermore, binge drinking ated with smaller DLPFC and IPL vol- network of regions predicted future adolescents and young adults have umes and greater dorsal cingulate and drinking and alcohol-related problems, demonstrated impaired performance precuneus volumes,70 whereas reduced above and beyond baseline drinking on a variety of learning and memory FA in the fornix of concomitant binge characteristics. This suggests that tasks.59,61,62,64,65 These findings also drinking and substance using adoles- changes in how the brain responds to have been associated with changes in cents has been shown to predict greater alcohol cues may help predict which brain structure in binge drinking ado- amounts of risky behavior a year and individuals may transition from light lescents in regions of the brain where a half later.40 Functionally, riskier be- to heavy drinking and may be more these adolescents differ from control havior on the Iowa Gambling Task in informative than simply comparing subjects. Binge drinking–related binge drinking adolescents has been heavy drinkers with control subjects. deficits in working memory also have accompanied by greater activation in In another study, heavy-drinking been demonstrated,61,63 with one study the insula and amygdala, when com- adolescents had greater cue-elicited showing that after 3 years of binge pared with control subjects.51 Also, as brain response in the dorsal striatum, drinking, greater gray-matter volume described above, greater activation in cerebellum, PHG, and thalamus than in the DLPFC was positively associ- the OFC, superior parietal cortex, and control subjects prior to abstinence; ated with working-memory errors.26 DLPFC, when compared with con- however, the group differences in Further, decreased FA in the inferior trols, has been associated with more the cerebellum and ACC no longer longitudinal fasciculus in binge drink- risky decisions when there was a high remained significant after 28 days ing and substance using adolescents potential for loss.50 Taken together, of abstinence.58 This suggests that has been shown to be associated with these findings suggest that the under- although cue-elicited brain response poorer working-memory perfor- development of control regions (e.g., may be a predictor of future drinking, mance.67 In addition, although an smaller DLPFC and IPL volumes) if adolescents manage to maintain initial study found that the number of and hyperactivation of reward-salience abstinence, they may be able to reduce drinking days in the past year predict- regions (e.g., amygdala), both of which that cue-elicited response. This finding ed greater reductions in performance are hallmarks of adolescent neuro- has important implications for future on a visuospatial task,60 a follow-up development, may be exacerbated intervention strategies. study showed that thicker frontal cor- in adolescents who binge drink and tices corresponded with poorer visuo- may underlie the observed increase in spatial performance in binge drinking risk-taking behavior in binge drinking Effects on Behavior females.31 These findings suggest that adolescents. and Cognition delayed cortical maturation may un- derlie the effects of binge drinking on Many of the structural and function- visuospatial performance. Conclusions al differences observed in adolescent Binge drinking adolescents also binge drinkers also are associated with demonstrate impaired, or riskier, de- Although evidence is still emerging changes in cognition and behavior. cision making,68 likely resulting from on how binge drinking during adoles- Several studies have examined neu- impairments in impulsivity69 and inhi- cence and young adulthood affects the rocognitive changes related to binge bition.64 One study found that young brain, many general conclusions can drinking and reported poorer perfor- adults who showed stable, high levels be drawn from current literature (for mance in many domains, including of binge drinking made riskier choices a summary of all replicated findings in attention,59,60 learning and memo- on the Iowa Gambling Task compared binge drinking adolescents and young ry,59,61-66 and visuospatial functioning.60 with adolescents who engaged in adults, see Figure 1). First, binge Neuroimaging studies have found stable, low levels of binge drinking.68 drinking during adolescence appears to that the poorer sustained attention Other studies have reported that result in a decrease in both gray-matter observed in binge drinking adolescents heavy-drinking adolescents show great- volume and cortical gray-matter thick- is associated with thicker PFCs31 and er impulsivity than light drinkers69 and ness,9,30 with longitudinal studies sug- lower FA in the inferior longitudinal that binge drinking adolescents show gesting that some of these differences fasciculus67—regions where thickness impaired inhibition compared with may be present prior to binge drinking and FA differed significantly between control subjects.64 and continue to worsen as adolescents binge drinking adolescents and con- Neuroimaging studies have helped initiate alcohol consumption.27,28,32 trol subjects. This suggests that binge shed some light on the mechanisms Although it must be noted that some drinking during adolescence may cause underlying this impaired decision mak- studies show increased gray-matter a delay in the maturation of both gray ing and impulse control. Structurally, volume or thickness in binge drinking

Effects of Binge Drinking on the Developing Brain | 93 Cingulate: Frontal lobe: ↓ cortical thickness ↓ gray-matter volume ↓ cortical thickness Parietal lobe: ↓ fractional anisotropy ↓ fractional anisotropy ↓ task activation: risk taking/reward response ↑ task activation: working memory ↑ task activation: working memory ↓↑ task activation: verbal encoding ↓↑ task activation: inhibition and inhibition

Occipital lobe: ↑ gray-matter volume Striatum: ↓ fractional anisotropy ↓ fractional anisotropy ↓ task activation: inhibition ↑ task activation: cue reactivity Cerebellum: ↓ gray-matter volume ↓ white-matter volume Temporal Iobe: ↓ fractional anisotropy ↓ gray-matter volume ↑ task activation: working memory ↓ fractional anisotropy ↓ task activation: verbal encoding ↑ task activation: working memory ↓ decreased/smaller and cue reactivity ↑ increased/greater

Figure 1 Replicated findings in binge drinking adolescents and young adults. Figure 1 Replicated findings in binge drinking adolescents and young adults. adolescents, it is plausible that these concomitant users to those using only activation in task-relevant regions at contradictory findings either are caused alcohol or marijuana likely are neces- baseline, followed by an exacerbat- by the influence of concomitant mari- sary to completely disentangle these ed increase in activation, above and juana use33,34 or are the result of exam- effects. beyond that seen in control subjects, ining the effects of binge drinking on a Functionally, binge drinking during after initiation of binge drinking. A nonlinear developmental pattern2-5 in a adolescence appears to affect brain failure to recruit task-relevant regions cross-sectional manner.24,26 responses in numerous regions, across at baseline in future binge drinkers Second, multiple studies consistently a variety of tasks. Cross-sectional work could lead to poorer task performance, have shown that the developmental has identified both increased and de- while hyperactivation following alco- increases in white-matter volume, of- creased brain activation in multiple hol use suggests that binge drinking ten observed in adolescents,2,6-8 appear task domains (e.g., verbal learning, adolescents require more recruitment to be attenuated in adolescents who working memory, risk taking, cue of task-relevant networks to achieve binge drink,27,28,32 and that this atten- reactivity, and inhibition) and demon- desired cognitive outcomes. uation is associated with the degree strates the necessity of longitudinal Meanwhile, similar or lower levels of substance use.9,25 However, studies studies to determine which effects of brain activation during risk-taking demonstrating altered white-matter are a result of alcohol consumption behavior (i.e., risky decision making microstructure in binge drinking ad- and which reflect an underlying risk and reward response) also have been olescents have yielded mixed results, phenotype for those who will go on observed in binge drinking adoles- showing both increases and decreases to binge drink. Longitudinal work, cents.48,49 However, unlike during in FA. Again, it appears that this may specifically in working memory45 and working memory and response inhibi- partially be explained by the presence response inhibition,52,54 suggests that tion, binge drinking adolescents have of concomitant marijuana use in ado- binge drinking adolescents demon- lower levels of brain response over lescence.36,38-41 More studies comparing strate similar or lower levels of brain time during risky decision making and

94 | Vol. 39, No. 1 Alcohol Research: Current Reviews reward response. This may suggest not 3. Paus T. Mapping brain maturation and cognitive 19. Vetreno RP, Crews FT. Binge ethanol exposure development during adolescence. Trends Cogn Sci. during adolescence leads to a persistent loss only a pattern of activation during 2005;9(2):60-68. PMID: 15668098. of neurogenesis in the dorsal and ventral risky decision making that may serve hippocampus that is associated with impaired adult 4. Shaw P, Kabani NJ, Lerch JP, et al. Neurodevelopmental 49 cognitive functioning. Front Neurosci. 2015;9:35. as a risk factor for future drinking, trajectories of the human cerebral cortex. J Neurosci. PMID: 25729346. but also a diminished brain response 2008;28(14):3586-3594. PMID: 18385317. 20. National Institute on Alcohol Abuse and Alcoholism to risky stimuli and rewards following 5. Tamnes CK, Ostby Y, Fjell AM, et al. Brain maturation 48,49 binge drinking. This decreased in adolescence and young adulthood: Regional (NIAAA). NIAAA council approves definition of brain response may be what causes age-related changes in cortical thickness and white binge drinking. NIAAA Newsletter. Winter 2004;(3). matter volume and microstructure. Cereb Cortex. https://pubs.niaaa.nih.gov/publications/Newsletter/ binge drinking adolescents to show 2010;20(3):534-548. PMID: 19520764. winter2004/Newsletter_Number3.pdf. Accessed greater risky behavior and may en- December 14, 2016. 6. Giedd JN, Blumenthal J, Jeffries NO, et al. Brain hance reward seeking. development during childhood and adolescence: 21. Substance Abuse and Mental Health Services Understanding these altered neuro- A longitudinal MRI study. Nat Neurosci. Administration (SAMHSA). Behavioral Health Trends biological features in binge drinking 1999;2(10):861-863. PMID: 10491603. in the United States: Results From the 2014 National Survey on Drug Use and Health. Rockville, MD: adolescents is extremely relevant, be- 7. Lebel C, Beaulieu C. Longitudinal development of SAMHSA; 2015. cause changes in both brain structure human brain wiring continues from childhood into and function have been related to adulthood. J Neurosci. 2011;31(30):10937-10947. 22. DeWit DJ, Adlaf EM, Offord DR, et al. Age at first PMID: 21795544. alcohol use: A risk factor for the development of changes in cognition in binge drinking alcohol disorders. Am J Psychiatry. 2000;157(5):745- adolescents.26,31,40,50,51,60,67,70 Moreover, 8. Paus T, Zijdenbos A, Worsley K, et al. Structural 750. PMID: 10784467. maturation of neural pathways in children not only do differences in task acti- and adolescents: In vivo study. Science. 23. Kvamme TL, Schmidt C, Strelchuk D, et al. Sexually vation serve as risk factors for future 1999;283(5409):1908-1911. PMID: 10082463. dimorphic brain volume interaction in college-aged 45,49,52,54 binge drinkers. Neuroimage Clin. 2016;10:310-317. drinking, but neurobiological 9. Pfefferbaum A, Rohlfing T, Pohl KM, et al. Adolescent PMID: 26900571. features, such as fronto-parietal hyper- development of cortical and white matter structure activation during inhibition and atyp- in the NCANDA sample: Role of sex, ethnicity, 24. Howell NA, Worbe Y, Lange I, et al. Increased ventral puberty, and alcohol drinking. Cereb Cortex. striatal volume in college-aged binge drinkers. PLoS ical white-matter microstructure, may 2016;26(10):4101-4121. PMID: 26408800. One. 2013;8(9):e74164. PMID: 24086317. serve as risk factors for escalated drink- 10. Blakemore SJ, Choudhury S. Development of the 25. Lisdahl KM, Thayer R, Squeglia LM, et al. Recent ing and risk-taking behavior in ado- adolescent brain: Implications for executive function binge drinking predicts smaller cerebellar volumes 40,56 lescents who are already drinking. and social cognition. J Child Psychol Psychiatry. in adolescents. Psychiatry Res. 2013;211(1):17-23. Adolescent onset of alcohol use has 2006;47(3-4):296-312. PMID: 16492261. PMID: 23154095. been associated with an increased risk 11. Spear LP. Adolescents and alcohol. Curr Dir Psychol 26. Doallo S, Cadaveira F, Corral M, et al. Larger mid- for developing an AUD later in life;22 Sci. 2013;22(2):152-157. PMID: 25309054. dorsolateral prefrontal gray matter volume in young binge drinkers revealed by voxel-based morphometry. thus, understanding neurobiological 12. Casey BJ, Jones RM, Hare TA. The adolescent PLoS One. 2014;9(5):e96380. PMID: 24789323. markers that are associated with both brain. Ann N Y Acad Sci. 2008;1124(1):111-126. initiation and escalation of alcohol use PMID: 18400927. 27. Squeglia LM, Rinker DA, Bartsch H, et al. Brain volume 13. Crews FT, He J, Hodge C. Adolescent cortical reductions in adolescent heavy drinkers. Dev Cogn is important for advancing future pre- Neurosci. 2014;9:117-125. PMID: 24632141. vention and intervention strategies in development: A critical period of vulnerability for addiction. Pharmacol Biochem Behav. 28. Squeglia LM, Tapert SF, Sullivan EV, et al. Brain an effort to reduce the rates of AUD. 2007;86(2):189-199. PMID: 17222895. development in heavy-drinking adolescents. 14. Spear LP. The adolescent brain and age-related Am J Psychiatry. 2015;172(6):531-542. behavioral manifestations. Neurosci Biobehav Rev. PMID: 25982660. Financial Disclosure 2000;24(4):417-463. PMID: 10817843. 29. Whelan R, Watts R, Orr CA, et al. Neuropsychosocial 15. Steinberg L. Risk taking in adolescence: New profiles of current and future adolescent alcohol The authors declare that they have perspectives from brain and behavioral science. Curr misusers. Nature. 2014;512(7513):185-189. no competing financial interests. Dir Psychol Sci. 2007;16(2):55-59. PMID: 25043041. 16. Crews FT, Braun CJ, Hoplight B, et al. Binge ethanol 30. 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96 | Vol. 39, No. 1 Alcohol Research: Current Reviews NIH’s Adolescent Brain Cognitive Development (ABCD) Study

Alcohol Research: Current Reviews Editorial Staff

Adolescence is the stage of life during which most people begin using alcohol, and it is also a time of considerable social, psychological, and physiological change. The brain, particularly the frontal cortex, con- tinues to develop throughout adoles- cence and does not fully mature until early adulthood. Adolescent alcohol exposure can impair brain development, compromise short- baseline standards for typical brain will be done every other year, and and long-term cognitive function- development (similar to those that the remaining assessments will be ing, and increase the likelihood of currently exist for height, weight, conducted semiannually or annually. developing alcohol-related problems and other physical characteristics). One important goal of the ABCD during adolescence and later in life. These data are expected to illuminate Study is to create a unique data Furthering our understanding of the how brain development is affected resource for the entire scientific developing brain—as well as how by substance use and other child- community by embracing an open differences in brain structure and hood experiences, such as patterns science model. Curated, anonymized function that exist prior to alcohol of sleep, use of social media, and data will be released annually to the and other substance use contribute engagement in sports and with video research community, along with the to substance use disorders—is a high games. It may also reveal neurobi- computational workflows used to priority for the National Institutes ological, cognitive, and behavioral produce the data, beginning 1 year of Health (NIH). precursors of substance misuse and after data collection begins. In September 2015, NIH other risk behaviors, and ultimately ABCD is supported by the launched the Adolescent Brain inform preventive and treatment National Institute on Alcohol Cognitive Development (ABCD) interventions. Abuse and Alcoholism, the National Study, the largest long-term study The ABCD Consortium consists Institute on Drug Abuse, the of brain development and child of a Coordinating Center, a Data National Cancer Institute, the and adolescent health in the United Analysis and Informatics Center, Eunice Kennedy Shriver National States. The ABCD Study will recruit and 21 research sites across the Institute of Child Health and more than 11,000 9- to 10-year-olds country. Recruitment, which began Human Development, the National to capture data before children begin in September 2016, is expected to Institute of Mental Health, the using alcohol or other addictive sub- span 2 years. ABCD workgroups National Institute on Minority stances. It will integrate structural have established standardized and Health and Health Disparities, the and functional brain imaging; genet- harmonized assessments of neu- National Institute of Neurological ic testing; and neuropsychological, rocognition, physical and mental Disorders and Stroke, the NIH behavioral, and other health assess- health, social and emotional func- Office of Behavioral and Social ments of study participants conduct- tions, and culture and environment. Sciences Research, and the Division ed over a 10-year period, yielding a They also have established multi- of Adolescent and School Health at substantial amount of information modal structural and functional the Centers for Disease Control and about healthy adolescent brain de- brain imaging and bioassays. Brain Prevention. velopment. Data gathered from par- imaging and biospecimen collection For more information, visit ticipants will allow the creation of for genetic and epigenetic analyses http://abcdstudy.org/index.html.

NIH’s Adolescent Brain Cognitive Development (ABCD) Study | 97 In any given year, about 15 million adults in the United States meet the diagnostic criteria for alcohol use disorder (AUD), but less than 10 percent of them receive treatment. Often, finding quality AUD care can be complicated, and many people aren’t aware of available treatment options.

In response, NIAAA developed the online tool, Alcohol Treatment NavigatorSM, which makes this complicated process easier by telling people what they need to know, what to do, and how to recognize quality care. This landmark resource is comprehensive but also easy-to-use. We hope you will explore the site and then share it widely.

Visit https://AlcoholTreatment.niaaa.nih.gov ALCOHOL RESEARCH: Current Reviews

Binge Drinking’s Effects on the Body

Patricia E. Molina and Steve Nelson Patricia E. Molina, M.D., Ph.D., is the Richard Ashman, Studies have focused on the effects of chronic alcohol consumption and the mecha- Ph.D., Professor; head of the nisms of tissue injury underlying and cirrhosis, with less focus on Department of Physiology; and the pathophysiological consequences of binge alcohol consumption. Alcohol binge drinking prevalence continues to rise, particularly among individuals ages 18 to 24. director of the Comprehensive However, it is also frequent in individuals ages 65 and older. High blood alcohol levels Alcohol–HIV/AIDS Research achieved with this pattern of alcohol consumption are of particular concern, as alco- Center and the Alcohol and Drug hol can permeate to virtually all tissues in the body, resulting in significant alterations Abuse Center of Excellence, in organ function, which leads to multisystemic pathophysiological consequences. In Louisiana State University Health addition to the pattern, amount, and frequency of alcohol consumption, additional Sciences Center, New Orleans, factors, including the type of alcoholic beverage, may contribute differentially to the Louisiana. risk for alcohol-induced tissue injury. Preclinical and translational research strategies are needed to enhance our understanding of the effects of binge alcohol drinking, Steve Nelson, M.D., is the particularly for individuals with a history of chronic alcohol consumption. Identifica- John H. Seabury Professor of tion of underlying pathophysiological processes responsible for tissue and organ Medicine and the dean of the injury can lead to development of preventive or therapeutic interventions to reduce School of Medicine, Louisiana the health care burden associated with binge alcohol drinking. State University Health Sciences Key words: Alcohol and other drug (AOD) intoxication; alcoholic hepatitis; Center, New Orleans, Louisiana. alcoholic liver cirrhosis; alcohol-induced disorders; binge drinking;

Introduction the individual, has been well-estab- equivalents in tissue has been consis- lished.3,4 The resulting tissue injury tently demonstrated to be an overall Alcohol misuse is the fifth-leading has increasingly been recognized and mechanism of the tissue injury that risk factor for premature death and dis- examined as a contributing factor to results from chronic alcohol misuse. ability worldwide,1 and, adjusting for alcohol-related comorbidities and Dose-dependent relationships between age, alcohol is the leading risk factor mortality. Several pathophysiological alcohol consumption and incidence for mortality and the overall burden mechanisms have been identified of diabetes mellitus, hypertension, of disease in the 15 to 59 age group.2 as causative factors of tissue and ischemic heart disease, dysrhythmias, According to the World Health organ injuries that resulted from stroke, pneumonia, and fetal alco- Organization, in 2004, 4.5% of the excessive alcohol consumption, hol syndrome have been reported.4 global burden of disease and injury was including acetaldehyde generation, However, recognition of alcohol as an attributable to alcohol: 7.4% for men adduct formation, mitochondrial underlying causal factor in comorbid and 1.4% for women.2 injury, cell membrane perturba- conditions remains a challenge in the Alcohol can permeate to virtually tions, immune modulation, and clinical setting. all tissues in the body, resulting in oxidative stress (Figure 1). Some Several factors associated with significant alterations in organ func- of these mechanisms are the result alcohol consumption, including pat- tion, which leads to multisystemic of direct alcohol-induced cell per- tern, amount, and frequency, and pathophysiological consequences. turbations, whereas others are the the type of alcoholic beverage, may The effect of alcohol misuse on mul- consequence of tissue alcohol me- contribute differentially to the risk tiple organ systems outside the liver, tabolism (Figure 2). The oxidative for alcohol-induced tissue injury. The mediated through direct and indirect stress caused by excess production question of whether all types of alcohol effects beyond those associated with of reactive oxygen species (ROS) or produce similar pathophysiological alterations in the nutritional state of a reduction in reducing antioxidant consequences remains to be answered.

Binge Drinking’s Effects on the Body | 99 However, the particularly detrimental effects of binge drinking have increas- ingly gained attention. Binge drinking, as defined by the National Institute on Alcohol Abuse and Alcoholism (NIAAA), is a pattern of alcohol con- sumption that brings blood alcohol concentration to .08 g/dL, which typically occurs following the intake of five or more standard alcohol drinks by men and four or more by women over a period of approximately 2 hours.5 Results from the 2015 National Survey on Drug Use and Health show overall prevalence of binge drinking (during the past 30 days) of 26.9% among U.S. adults ages 18 and older.6 Those data show that binge drinking preva- lence and intensity are highest among those ages 18 to 24 but also occur in high frequency among older individ- uals (ages 65 and older). Thus, binge drinking prevails in two vulnerable segments of the population, raising their risks for greater severity of injury and frequency of comorbidities.

Understanding the Biomedical Consequences of Binge Drinking A limitation to our understanding of the consequences of binge alcohol con- sumption on organ injury is the lack of information on the time period, duration, and number of binge oc- currences that describe the long-term practice of binge drinking. Preclinical studies conducted under controlled conditions provide opportunities to examine quantity and frequency vari- ables in the investigation of the effects of alcohol consumption on organ Figure 1 Mechanisms of alcohol-induced tissue injury. Alcohol contributes to tissue injury injuries. However, interpreting, com- directly and indirectly through mechanisms including oxidative stress, inflammation, paring, and integrating the patterns of acetaldehyde adduct formation, barrier integrity disruption, decreased anabolic alcohol consumption described in clin- signaling, enhanced catabolic processes (particularly through the ubiquitin ical reports is difficult because of the proteasome pathway), profibrotic changes, mitochondrial dysfunction and injury, different types of data collected across and cell membrane perturbations. Note: mTORC1, mammalian target of rapamycin studies. This difficulty underscores the complex 1; mTORC2, mammalian target of rapamycin complex 2; ROS, reactive need for researchers to perform more oxygen species. Source: Molina PE, Gardner JD, Souza-Smith FM, et al. Alcohol rigorous comprehensive and systematic abuse: Critical pathophysiological processes and contribution to disease burden. data collection on alcohol use patterns. Physiology. 2014;29(3)203-215. The Timeline Followback (TLFB) tool, for example, uses a calendar and

100 | Vol. 39, No. 1 Alcohol Research: Current Reviews Figure 2 Tissue alcohol metabolism contributes to tissue and organ injury through altered redox potential, generation of ROS, and generation of metabolites, such as acetaldehyde, that form DNA and protein adducts. Alcohol (ethanol) is metabolized to acetaldehyde primarily by ADH in the cytosol and CYP2E1 in the endoplasmic reticulum. Acetaldehyde is converted to acetate in the mitochondria by the enzyme ALDH. Acetaldehyde can form adducts with DNA and proteins that can produce injury through activation of immune responses. During the oxidative process, both ADH and ALDH reactions reduce NAD+ to NADH, shifting the cellular redox ratio. In addition, the cytochrome P450 enzymes, particularly CYP2E1, contribute to the oxidation of alcohol to acetaldehyde, particularly at increasing alcohol concentrations, as well as following their induction by chronic alcohol misuse. The pathway of alcohol oxidation results in the production of large amounts of ROS,

including H2O2, and is thought to be an important mechanism contributing to alcoholic liver injury. ROS are eliminated by antioxidants like GSH under normal conditions. Alcohol depletes cellular GSH stores, thereby exacerbating ROS-mediated injury. ROS can interact with lipids, producing lipid peroxidation, which leads to formation of reactive molecules such as MDA and HNE, which can then form protein adducts. Note: Acetyl-CoA, acetyl coenzyme A; ADH, alcohol dehydrogenase; ALDH, acetaldehyde dehydrogenase type 2; CYP2E1, cytochrome

P450 2E1; GSH, glutathione; H2O, water; H2O2, hydrogen peroxide; HNE, 4-hydroxy-2-nonenal; MDA, malondialdehyde; NAD+, nicotinamide adenine dinucleotide (oxidized); NADH, nicotinamide adenine dinucleotide (reduced); NADP, nicotinamide adenine dinucleotide phosphate

(oxidized); NADPH, nicotinamide adenine dinucleotide phosphate (reduced); O2, oxygen; ROS, reactive oxygen species. Source: Molina PE, Gardner JD, Souza-Smith FM, et al. Alcohol abuse: Critical pathophysiological processes and contribution to disease burden. Physiology. 2014;29(3)203-215.

a structured interview to collect ret- should be taken into consideration the health consequences associated rospective information on the types for future development of alcohol use with binge drinking. Epidemiological and frequency of alcohol use over a screening tools, because binge drinking studies that compared the preva- given time period.7,8 Nevertheless, has been suggested to result in greater lence of coronary heart disease in accounting for a lifetime pattern of alcohol-related harm.9 “wine-drinking countries” and beer- or binge alcohol consumption remains Different types of alcoholic bev- liquor-drinking countries have pro- challenging when conducting clinical erages consumed in binge drinking posed that red wine, but not beer or studies. Alcohol consumption patterns episodes could also differentially affect spirits, consumed with a meal may

Binge Drinking’s Effects on the Body | 101 confer cardiovascular protection.10 binge drinking is more likely to con- cidated. However, it is reasonable to The proposed protective effects of red tribute to organ injury than paced, speculate that greater bacterial burden wine include decreased blood clot moderate alcohol drinking that is asso- and altered bacterial profiles, together formation, vascular relaxation, and ciated with a meal. with increased permeability of the gut attenuation of low-density lipoprotein The gut mucosa is particularly sus- mucosa, would lead to continuous en- (LDL, or bad cholesterol) oxidation, ceptible to alcohol-induced injury, try of bacterial toxins into the systemic an early event preceding formation of and alcohol consumption can result circulation. These changes could pro- cholesterol-filled plaque. These effects in a loss of intestinal barrier integrity. duce chronic and sustained activation are attributed to polyphenols, espe- Several direct and indirect mechanisms of immune responses that, in turn, cially resveratrol, and their antioxidant have been identified that disrupt the could lead to immune exhaustion and properties. structural and functional components dysfunction. Preclinical studies show However, not all reports support the involved in maintaining the integrity that binge-on-chronic alcohol feeding link between consuming a specific bev- of the gut mucosal barrier. Alcohol alters the gut microflora at multiple erage type (i.e., wine vs. beer or spirits) and its breakdown products directly taxonomic levels, influencing hepatic and health benefits. Some reports damage epithelial cells through gener- inflammation, neutrophil infiltration, suggest that beverage amount is more ation of ROS and through disruption and liver steatosis,23 which highlights directly linked to health outcomes.11,12 of tight junction protein expression the need for clinical investigation into The differential contribution of alco- and signaling.14 This process disrupts the relationship between gut micro- holic beverages to beneficial or detri- the integrity of the intestinal barrier, flora and hepatic liver disease. mental health outcomes remains to be allowing bacteria and toxins to reach examined in both preclinical and clini- the bloodstream. Acute alcohol binge cal studies. In binge drinking episodes, drinking in healthy human volunteers Local and Systemic the form of alcohol consumed most can produce a significant increase in Consequences of Gut Injury frequently is beer (67.1%), followed serum endotoxin levels and bacterial by liquor (21.9%) and wine (10.9%).13 16S ribosomal DNA, suggesting the Toxins and bacterial products leaked Moreover, beer accounts for most of gastrointestinal microbial origin of from the gastrointestinal tract can be the alcohol consumed by drinkers endotoxin.15-17 transported through the lymphatic who are at the highest risk of causing More recently, attention has system. This route of dissemination, or incurring alcohol-related harm, focused on the changes in intestinal which escapes hepatic clearance, may including drinkers ages 18 to 20, those microbiome that contribute to alcohol- prove critical in the enhanced systemic with more frequent binge episodes per associated intestinal inflammation delivery of toxins. Preclinical studies month, and those drinking 8 or more and permeability. Alcohol promotes have shown that repeated binge-like drinks per binge episode. Therefore, both dysbiosis (decreased diversity alcohol intoxication increases lym- dissecting how pattern of drinking and or an imbalance in the types of phatic permeability and inflammation type of alcoholic beverage contribute microbes) and bacterial overgrowth in the adipose tissue that immediately to overall outcomes is challenging. in the gastrointestinal system.18-21 surrounds the mesenteric lymphatics. Alcohol alters the balance between Inflammatory response in mesenteric bacterial strains, decreasing the perilymphatic adipose tissue is associ- The Gastrointestinal Tract, presence of beneficial bacteria, such as ated with altered adipose tissue insulin Liver, and Pancreas Lactobacillus and Bifidobacterium, and signaling and circulating adipokine increasing that of Proteobacteria and profiles, which suggests a link between Of all tissues affected by binge-like Bacilli.19 This imbalance adds to the lymphatic leak, adipose tissue inflam- alcohol consumption, the gastrointes- possibility that bacterial overgrowth mation, and metabolic dysregulation.24 tinal tract bears the greatest burden may contribute to local mucosal Whether chronic alcohol consump- due to its direct exposure to high tissue inflammation through bacterial tion not in a binge pattern produces concentrations of alcohol following metabolism of alcohol and enhanced similar alterations in lymphatic per- ingestion (Figure 3). Binge drinking local production of metabolites such meability and mesenteric adipose often occurs apart from meals, which as acetaldehyde.22 Moreover, increased inflammation remains to be deter- may also contribute to its deleterious bacterial load, together with shifts in mined. However, localized alterations effects on organs. Food consumed at intestinal bacterial strains, brings about in mesenteric adipose tissue metabolic the time of alcohol consumption influ- diverse profiles of bacterial-derived regulation, including insulin signal- ences not only the alcohol absorption metabolites. ing, may prove to be relevant to the rate and blood alcohol concentration, How these shifts in bacterial strains, enhanced risk for metabolic syndrome but also the direct effect of alcohol on load, and metabolites contribute to that is associated with binge alcohol the gastrointestinal mucosa. Hence, organ injury remains to be fully elu- consumption.25 After burn injury

102 | Vol. 39, No. 1 Alcohol Research: Current Reviews Gastrointestinal Cardiovascular Pulmonary system Musculoskeletal Nervous system tract, liver, and system • Oxidative stress system • Impaired behavioral pancreas • Cardiomyocyte and diminished • Decreased growth and cognitive • Esophageal and mitochondrial lung host defense factor signaling function, impaired gastric dysmotility and sarcoplasmic mechanisms and responsiveness, impulse control and • Liver oxidative stress, reticulum damage, increased ubiquitin motor skills, and steatosis, hepatitis, altered calcium proteasome blackouts and fibrosis dynamics, and pathway activation, • Structural changes in • and cardiac fibrosis upregulation of prefrontal and parietal mucosal atrophy • Myocardial negative regulators regions, and gender- • Impaired intestinal oxidative of skeletal muscle specific differences nutrient absorption, stress, impaired growth, and in frontal, temporal, disruption of cardiomyocyte disruption of bone and cerebellar brain intestinal barrier and contraction, remodeling activation during lymphatic function, hypertension, and working memory tasks and increased potentiation of the • Enlargement of lateral bacterial toxin renin-angiotensin- ventricles and cisterns, translocation aldosterone system and degradations in • Increased pancreas neural white matter inflammation • Reduced neurogenesis • Increased neuroimmune gene expression

Figure 3 The systemic effects of chronic binge alcohol consumption and the principal organ systems affected.

and a binge-like pattern of alcohol metabolism of alcohol and the result- aminotransferase), hepatic steatosis, intoxication, rodents showed similar ing ROS generation; acetaldehyde and inflammatory cytokine expression exacerbation of adipose tissue inflam- formation and the resulting adducts; compared to rodents subjected only to mation.26 This suggests that a possible immune response activation, partic- chronic or to acute alcohol exposure.32 synergism between binge-like alcohol ularly in Kupffer and stellate cells; These results demonstrate that binge- intoxication and injury promotes a and alterations in cell signaling are all on-chronic alcohol exposure results in dysregulated adipose environment proposed as mechanisms that underlie greater insult than either chronic or conducive to insulin resistance, and liver injury associated with binge-like acute alcohol exposure alone. Clinical potentially metabolic syndrome, if alcohol consumption. For people with studies have provided evidence of these alterations are sustained beyond chronic alcoholism, binge drinking associations among alcohol binge the immediate period following binge augments liver injury27,28 and is a ma- drinking patterns, immune activation drinking or burn injury.3 jor trigger for the progression from (high CD69 and low TLR4, CXCR4, Second to the gastrointestinal tract, steatosis to steatohepatitis.29-31 In one and CCR2 expression), and decreased the liver has the most exposure to high study, rodents that received binge-on- chemotactic responses to SDF-1 and alcohol concentrations during periods chronic alcohol exposure had accentu- MCP-1.33 These associations reflect an of binge drinking. Hepatocellular ated elevation in liver enzymes (alanine altered immune profile that may be as-

Binge Drinking’s Effects on the Body | 103 sociated with liver injury and increased levels of alpha-amylase, glucose, and Binge drinking has been associated susceptibility to infection. More re- insulin, strongly suggesting a detri- with increased risk of cardiovascular cently, attention has been drawn to mental effect of acute binge alcohol comorbidities, including hypertension, the potential greater liver injury in exposure on the pancreas. Specifically, stroke, , and individuals with metabolic syndrome. preclinical studies have proposed that, sudden death, and this risk may extend A population-based study showed a alone, chronic and binge alcohol expo- to the younger population as well.47-51 direct association between binge drink- sure caused minimal pancreatic injury, Acute elevations in blood alcohol levels ing frequency and liver disease risk, but chronic plus binge alcohol expo- resulting from binge alcohol consump- after adjusting for average daily alcohol sure resulted in significant apoptotic tion are associated with an increased intake and age.34 In this study, binge cell death; alterations in alpha-amylase, risk of new-onset atrial fibrillation, a drinking and metabolic syndrome glucose, and insulin; pancreatic in- most common arrhythmia strongly produced supra-additive increases flammation; and protein oxidation and associated with adverse cardiovascular in the risk of decompensated liver lipid peroxidation, which are indicative events and sudden death.52 A higher disease. Because of increasing rates of of oxidative stress.37 The pathogene- risk for myocardial infarction has obesity and metabolic syndrome, re- sis of alcoholic pancreatitis involves been reported after 1 day of heavy search on the effects of alcohol misuse acinar cell alcohol metabolism. The alcohol consumption (which could and the biomedical consequences is direct toxic effects of alcohol and its reflect a binge-like pattern of alcohol needed for this particular segment of metabolites on acinar cells, in the pres- consumption).53 the population. ence of an appropriate trigger factor, Few preclinical studies have exam- Located strategically between the may predispose the gland to injury. ined the effect of binge drinking on liver and the gastrointestinal tract, In addition, pancreatic stellate cells cardiac function. In one study, over the pancreas also has high susceptibil- are implicated in alcoholic pancreatic a 5-week period, rodents received ity to alcohol-induced tissue injury. fibrosis.38 Thus, experimental and repeated episodes of alcohol adminis- Heavy, chronic alcohol consumption clinical data suggest that alcohol con- tration that modeled a binge drinking is a recognized contributing factor sumption alone does not initiate pan- pattern.54 These rodents did not show in the development of pancreatitis. creatitis, but it sensitizes the pancreas changes in cardiac structure, but this However, how dose and pattern of to disease from other insults, including drinking pattern resulted in increased alcohol consumption affect pancreatic smoking, exposure to bacterial toxins, phosphorylation of myocardial p38 function and structure is not known. viral infections, and binge alcohol mitogen-activated protein kinase and Studies show that alcohol consump- consumption.39 transient increases in blood pressure, tion of more than 40 g per day is which became progressively higher increasingly detrimental for any type with repeated episodes of binge of pancreatitis.35 Retrospective clinical Cardiovascular Consequences drinking. These effects were partly studies have shown that binge alcohol mediated by adrenergic mechanisms. drinking is associated with aggravation The effect of alcohol consumption More recently, the combined binge- of first-attack severe acute pancreatitis, on cardiovascular function has been on-chronic pattern of alcohol feeding which is reflected in higher admission the subject of much debate. The rela- to rodents has been shown to result levels of serum triglycerides, Balthazar tionship between alcohol consumption in alcohol-induced cardiomyopathy, computed tomographic score, and and cardiovascular health is not linear characterized by increased myocardial Acute Physiology and Chronic and is thought to follow a J-shaped oxidative/nitrative stress, impaired mi- Health Evaluation II score, as well curve, with low amounts of alcohol tochondrial function and biogenesis, as higher mortality and incidence of consumption frequently reported as and enhanced cardiac steatosis.55,56 The 40 complications.36 cardioprotective. However, data sug- role of oxidative stress has been con- Insight into the mechanisms in- gest that binge drinking is associated firmed by other preclinical studies.57 volved in pancreatic injury is derived with transient increases in systolic and from preclinical studies that show diastolic blood pressure (Figure 3).41-43 detrimental effects of binge alcohol The prevalence of hypertension has Pulmonary Consequences exposure on the pancreas. These effects been reported to be higher in indi- include tissue edema, inflammation, viduals who consume more than six Preclinical studies have identified acinar atrophy and moderate fibrosis, drinks per day. However, the pattern impairments in multiple aspects of endoplasmic reticulum stress, oxidative of alcohol consumption was not con- lung function after chronic and binge- stress, and apoptotic and necrotic cell sidered in these studies.44 The effect of like alcohol administration, including death. These structural changes are as- even a modest rise in blood pressure is altered epithelial barrier function, sup- sociated with pancreatic dysfunctional considerable, as it is a recognized risk pressed immunity, impaired bacterial changes, which are reflected by altered factor for cardiovascular mortality.45,46 clearance, depleted glutathione (GSH),

104 | Vol. 39, No. 1 Alcohol Research: Current Reviews and impaired pulmonary epithelial cil- Preclinical studies suggest that, after trol, impairments in motor skills (e.g., iary function (Figure 3).58,59 Moreover, binge-like alcohol administration, balance and hand-eye coordination), alcohol binge drinking increases the physical exercise may ameliorate cog- blackouts, and loss of consciousness risk for sustaining traumatic injuries nitive impairment and suppressed neu- (Figure 3).80 All of these effects have and aggravates outcomes from trau- rogenesis.73 The effect of binge alcohol serious health consequences ranging matic injuries,60 such as burns,26,58,61-63 consumption on exercise performance from falls and injuries to death.81 In bone fractures,64 and hemorrhagic and recovery remains to be systemat- particular, adolescents are vulnerable shock.65 For alcohol-intoxicated hosts, ically investigated. One clinical study to the cognitive manifestations and similar detrimental effects have been reported no change in isokinetic and memory loss associated with binge reported on bacterial pneumonia out- isometric muscle performance, central drinking. National estimates suggest comes, a frequent comorbid condition activation, or creatine kinase release that significant numbers of people associated with traumatic injury.66 during or after acute moderate alcohol who binge drink report at least one Binge-like alcohol administration intoxication.74 Short-term reductions incident of blacking out in the pre- impairs innate and adaptive immune in lower-extremity performance were vious year.82,83 Blackouts, defined as responses in the lungs, thereby increas- reported in a study that investigated short periods of amnesia during which ing infection susceptibility, morbidity, athletes after an alcohol drinking a person actively engages in behaviors and mortality.61,62 It is possible that, episode and the associated reduced (e.g., walking or talking) without in hosts previously exposed to chronic sleep hours.75 Another study found creating memories for them, often alcohol consumption, binge drink- that alcohol consumption following occur at blood alcohol concentrations ing detrimentally affects pulmonary a simulated rugby game decreased exceeding .25 g/dL.84,85 Blackouts are outcomes from traumatic injury by lower-body power output but did not common among college students who priming host defense mechanisms. affect performance of tasks requiring drink alcohol. Estimates suggest that This combined effect may prevent clear repeated maximal muscular effort.76 up to 50% of students that engaged in isolation of binge alcohol consumption However, the same researchers found drinking reported a blackout episode effects from chronic alcohol consump- that alcohol consumption following during the past year.86,87 The pattern tion effects. eccentric exercise accentuated the of rapid consumption of large doses losses in dynamic and static strength of alcohol, frequently on an empty in males.77 stomach, is characteristic of the adoles- Musculoskeletal Consequences In contrast, alcohol consumption cent period.88 following muscle-damaging resistance The consequences of binge drinking The incidence of skeletal muscle exercise did not alter inflammatory are not short-lived or limited to the pe- dysfunction (i.e., myopathy) resulting capacity or muscular performance re- riod of intoxication. Imaging studies of from chronic alcohol misuse surpasses covery in resistance-trained women,78 binge drinking adolescents document that of cirrhosis.67 This progressive suggesting possible gender differences long-lasting changes. Reports indicate loss of mass is multifactorial and in alcohol’s modulation of exercise per- structural changes in the prefrontal involves metabolic, inflammatory, and formance and recovery. These studies and parietal regions, as well as in re- extracellular matrix alterations, which were conducted using healthy volun- gions known to mediate reward, and promote muscle proteolysis and de- teers and athletes. Other studies that these changes are thought to reflect creased protein synthesis (Figure 3).68 investigated patients with alcoholic long-lasting effects of alcohol bingeing An additional severe complication of liver disease showed lower muscular on critical neurodevelopmental pro- binge drinking is the development of endurance, maximal voluntary isomet- cesses.89 Functional imaging studies acute muscle injury, rhabdomyolysis. ric muscle strength, and total work of of the brains of binge drinking and Binge drinking that precedes coma or knee extensors.79 Controlled studies nondrinking adolescents found that immobility can lead to rhabdomyolysis are needed, particularly in light of the binge drinking adolescents showed and, consequently, to renal injury, popularity of binge drinking events greater responses in frontal and parietal as documented in case reports in the frequently associated with collegiate regions, no hippocampal activation to literature.69-71 The mechanisms are not and professional sports. novel word pairs, and modest decreases well-understood, but they may involve in word-pair recall, which could in- acute hypokalemia.72 This phenom- dicate disadvantaged processing of enon may warrant further study, as Neuropathological novel verbal information and a slower environmental factors such as high Consequences learning slope.90 In another study, ambient temperature and individual adolescent binge drinking resulted in drug-drug interactions can obscure The behavioral and cognitive effects gender-specific differences in frontal, presentation and hinder management of binge drinking include difficulties temporal, and cerebellar brain activa- of alcohol-induced rhabdomyolysis. in decision-making and impulse con- tion during a special working memory

Binge Drinking’s Effects on the Body | 105 task, reflecting differential effects of administration to rodents produced hepatitis and cirrhosis have received binge drinking on neuropsychologi- increases in cerebrospinal fluid volume much attention, less attention has been cal performance and possibly greater in the lateral ventricles and cisterns, focused on the pathophysiological vulnerability in female adolescents.91 decreased levels of N-acetylaspartate consequences of binge alcohol con- Other researchers have reported that and total creatine, and increased sumption. The differential duration degradations in neural white matter choline-containing compounds, of the intoxication period, excessive were linked with impaired cogni- glutamate, and glutamine, all of concentrations of alcohol at the tissue tive functioning in adolescents who which recovered during abstinence.94 92 level, accelerated alcohol metabolism binge drank. Moreover, preclinical data suggested and generation of ROS and alcohol Adolescent rodent intermittent eth- that adolescent binge drinking sensi- metabolites, and acute disruption of anol exposure that modeled human tized the neurocircuitry of addiction, adolescent binge drinking produced a antioxidant mechanisms are some of possibly inducing abnormal plasticity the salient differences between chronic range of pathophysiological and neuro- in reward-related learning processes, and binge-like alcohol-mediated tissue behavioral sequelae, including altered which could contribute to adolescent adult synapses, cognition, and sleep; vulnerability to addiction.95 injury. Because of the differences in reduced adult neurogenesis; increased male and female alcohol metabolism neuroimmune gene expression; and rates, it is possible that greater tissue increased adult alcohol drinking associ- Summary injury is produced in females who con- ated with disinhibition and social anx- sume alcohol in binge-like patterns. iety.93 Preclinical studies indicated that Although the effects of chronic alco- Furthermore, in an aging population binge drinking could produce brain hol consumption and the mechanisms already riddled with polypharmacy, structural abnormalities. Binge alcohol of tissue injury underlying alcoholic there is heightened potential for toxic- ity during an alcohol binge (Figure 4). Also, pre-existing comorbid conditions such as cardiovascular disease, renal failure, or steatohepatitis may pre- dispose binge drinkers to accelerated tissue injury. Additional research is needed to bet-

in ter recognize the differential effects of binge, chronic, and binge-on-chronic patterns of alcohol consumption. Animal models that reflect these pat- nvironment iat iet terns of alcohol exposure are needed. In addition, greater effort toward documenting a history of alcohol con-

ine lcool sumption, including the frequency, quantity, and quality of alcoholic beverages consumed, should help us Polyparmacy Comoridities better understand the effects of binge drinking on biological systems.

Genetics Acknowledgments Figure 4 Factors that contribute to disease processes associated with binge alcohol The authors are grateful for edito- drinking. For individuals who drink alcohol, factors such as type of alcohol, pattern rial support from Rebecca Gonzales of consumption, duration of alcohol misuse, and the age and diet of the drinker contribute to the incidence and severity of tissue injury. Another factor, polypharmacy, and grant support from the National particularly affects the older adult population, as multiple medications increase Institute on Alcohol Abuse and the potential for toxicity during an alcohol binge. Similarly, pre-existing comorbid Alcoholism (NIAAA) of the National conditions may predispose binge drinkers to accelerated tissue injury. Finally, genetic Institutes of Health (NIH) un- predisposition and environmental toxins are likely to be determining factors that affect der award number P60AA009803 the incidence and severity of tissue and organ injury. (LSUHSC-NO Comprehensive Alcohol–HIV/AIDS Research Center).

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