Chapter 36 - Heavy Episodic Drinking or Binge Drinking: A Booming

Chapter 36
Heavy Episodic Drinking
or Binge Drinking: A Booming
Consumption Pattern
Ana Adan1,2, Irina Benaiges1, Diego A. Forero3
1Department
of Psychiatry and Clinical Psychobiology, University of Barcelona, Barcelona, Spain; 2Institute for Brain, Cognition and Behavior
(IR3C), Barcelona, Spain; 3Laboratory of NeuroPsychiatric Genetics, Biomedical Sciences Research Group, School of Medicine, Universidad Antonio
Nariño, Bogotá, Colombia
Abbreviations
AUD Alcohol use disorder
AUDIT Alcohol Use Disorders Identification Test
BAC Blood alcohol concentration
BD Binge drinking
BDNF Brain-derived neurotrophic factor
BMI Brief motivational intervention
CNS Central nervous system
ERP Event-related potentials
ESPAD European School Survey Project on Alcohol and Other Drugs
fMRI Functional magnetic resonance imaging
NIAAA National Institute on Alcohol Abuse and Alcoholism
PFC Prefrontal cortex
PM Prospective memory
INTRODUCTION
In recent decades, a new pattern of intermittent alcohol consumption has emerged involving binge intake, which happens in sessions lasting just a few hours, usually during weekend evenings
and carried on by groups of peers. This pattern, known as heavy
episodic drinking or binge drinking (BD), is found especially
among adolescents and young adults in Western cultures.
BD involves the consumption of alcoholic beverages with
the primary intention of reaching a marked intoxication, with
low perception of risk and a tendency to equal intake in men and
women (Parada et al., 2011a). Intoxication is characterized by a
blood alcohol concentration (BAC) of at least 0.08 g/l. The practice of BD is increasing and expanding worldwide, and it has been
recently labeled as a new culture of intoxication.
Epidemiological research has provided very variable data on
the prevalence of BD according to the country and the sample
studied. In the United States, where it has been most researched,
BD is responsible for more than half of the deaths due to excessive
alcohol intake, and it is the most prevalent alcohol use disorder
(AUD). The data show that more than half of 12- to 17-year-olds
consume alcohol with a BD pattern. Approximately 90% of the
ethanol consumed under age 21 is as BD, and 70% of BD episodes
involve adults aged 26 and older (Thiele, 2012).
A study conducted among 15- to 16-year-old adolescents in
35 European countries, the European School Survey Project on
Alcohol and Other Drugs (ESPAD), showed that BD is found not
only in Scandinavian countries, England, and Ireland—which are
typically characterized as having BD problems (Pedersen & von
Soest, 2013)—but in Mediterranean countries as well. The BD
phenomenon has extended and appears to be on the rise in Mediterranean countries (Portugal, France, Italy, Spain), which had
been traditionally characterized by a pattern of higher per capita
consumption, most of which derived from daily consumption
of wine during meals. On average, 43% of the ESPAD students
reported heavy episodic drinking during the previous 30 days
(Hibell et al., 2009).
In this chapter, we revise the concept of BD, which is still
ambiguous nowadays, together with the risk and/or protection factors associated with the rise and maintenance of this pattern of
alcohol intake. We highlight some consequences on health and its
impact on neuropsychological functioning, in addition to possible
early markers or endophenotypes for future use.
DEFINITION OF BINGE DRINKING
The Monitoring Future Study, carried on in the 1970s, proposed
considering the pattern of BD as the consumption of five or more
alcoholic drinks in one event, whether in men or women (Bachman,
Johnston, & O’Malley, 1981). This has been and still is the criterion
used in many studies on this topic.
The Harvard School of Public Health’s College Alcohol Study,
in the 1990s, proposed using different criteria according to sex.
The concept of BD was established as the consumption of ≥5 alcoholic drinks for men and ≥4 drinks for women, in one single event
and at least once in the previous 2 weeks (Wechsler, Davenport,
Dowdall, Moeykens, & Castillo, 1994). This change of threshold
Neuropathology of Drug Addictions and Substance Misuse, Volume 1. http://dx.doi.org/10.1016/B978-0-12-800213-1.00036-5
Copyright © 2016 Elsevier Inc. All rights reserved.
389
390 PART | III Alcohol
in women was justified because women generally have a smaller
stature and physiologic differences in the absorption and distribution of alcohol. In 2004, the National Institute on Alcohol Abuse
and Alcoholism (NIAAA) Advisor Council endorsed the sex consideration in the definition of BD. The consumption of ≥5 drinks
for men and ≥4 drinks for women in approximately 2 h produces
a BAC of 0.08 g/l or greater, taking into account that in the USA a
standard drink has 14 g of alcohol. The new gender-specific definition increased the prevalence of women with BD pattern, due
to the change in the criteria and not to actual changes in drinking
behavior (Chavez, Nelson, Naimi, & Brewer, 2011).
There are significant differences in the amount of pure ethanol
grams in a standard drink in different countries of the world, as
published by the International Center for Alcohol Policies (2010).
As Table 1 shows, the NIAAA criteria may be valid in Portugal,
whereas in England the pattern of BD must be defined as the intake
of ≥8 drinks for men and ≥6 drinks for women. In the countries
where a standard drink contains 10 g of ethanol, the cutoff may be
set to ≥6 drinks for men and ≥5 drinks for women (Parada et al.,
2011a).
However, because teenagers may drink much larger amounts
than those considered in the general definition, it has been proposed to consider several degrees of BD. Thus, the concept of
extreme BD has emerged, with two subcategories: ≥10 drinks and
≥15 drinks (Patrick et al., 2013). In the USA, from the total percentage of high school seniors with BD, 10.5% were assigned to
the first extreme category (≥10 drinks) and 5.6% to the second
(≥15 drinks).
Regarding the timeframe to determine the presence of BD,
there is also little agreement. Most of the studies set the frequency unit as 2 weeks, while others set it as 1 week and still
others use time frames of 1–3 months or even 1 year. The timeframe of 1 or 2 weeks may be underestimating the prevalence
of BD, while a long interval may overestimate it. The preferred
TABLE 1 Grams of Pure Ethanol in a Standard Drink
According to Country
Country
England
Ethanol (g)
8
Australia, Austria, France, Hungary,
Ireland, Netherlands, New Zealand,
Poland, Spain
10
Finland
11
Denmark, Italy, South Africa
12
Canada
13.6
Portugal (unofficial), United States
14
Japan
19.75
The definition of binge drinking based on standard drinks consumed is
troublesome, because there is no international agreement on how many
grams of pure ethanol there should be in a standard drink. Measures of
standard units currently used in research can range from 8 g (England) to
19.75 g (Japan) of ethanol, making comparisons across studies difficult.
Data were revised from the International Center for Alcohol Policies
(2010), based on official government definitions.
and recommended criterion seems to be the occurrence of one
episode of BD every 2–4 weeks.
The Alcohol Use Disorders Identification Test (AUDIT;
Saunders, Aasland, Amundsen, & Grant, 1993) is the self-­
administered instrument most frequently used to detect a pattern
of BD. Using its third question (How frequently do you drink six
or more alcoholic beverages in one single event?), a cutoff line
can be established different from that proposed by the NIAAA.
However, no distinction between sexes is made, nor does it allow
quantification of extreme intakes.
Another element to be taken into account is the BD trajectory
in teenagers, from these possible four: accelerating (early onset
and increased frequency), steep increase (delayed onset and rapid
escalation), slow growth (delayed onset and gradual increase), and
stable low (abstinence). High levels of alcohol intake and more
physical health problems characterize the accelerating trajectory
(Modecki, Barber, & Eccles, 2014).
CONSEQUENCES ON HEALTH
AND POSSIBLE EARLY MARKERS
BD in the United States, Europe, and most developed countries
is regarded as a major health and social concern that is associated
with significant social and personal costs. BD elevates mortality
risk (Plunk, Syed-Mohammed, Cavazos-Rehg, Bierut, & Grucza,
2014) and is related to physical injury, motor vehicle accidents,
sexually transmitted diseases, unintended pregnancy, and medical
complications, as pointed out by the NIAAA (2000). Table 2 summarizes the main effects on health that BD may cause.
The number of drinks and the BAC are good predictors of
negative alcohol-related consequences (blackouts, physical fights,
and getting physically sick) in first-year college students (Barnet
et al., 2014). The BD adolescents show more risky sexual behavior (with the exception of non-condom use) and violent behavior
(Stickley, Koyanagi, Koposov, Razvodovsky, & Ruchkin, 2013;
Townshend, Kambouropoulos, Griffin, Hunt, & Milani, 2014;
Xing, Ji, & Zhang, 2006), with there being a strong association
with the number of BD days.
In healthy young binge drinkers, alterations have been found
in macro- and microcirculation; these may represent early clinical
manifestations of cardiovascular risk that should be considered in
preventive actions (Goslawski et al., 2013). A study on rats shows
that BD directly causes insulin resistance, which is a major risk factor to develop metabolic syndrome and type 2 diabetes (Lindtner
et al., 2013). Alcohol appears to disrupt insulin-receptor signaling
by causing inflammation in the hypothalamus, a nucleus of the
central nervous system (CNS), which also participates in coronary
artery disease and stroke.
Many studies have shown a link between psychological distress, such as anxiety and depression, and alcohol abuse (Balogun,
Koyanagi, Stickley, Gilmour, & Shibuya, 2014; Cheng & Furnham,
2013; Wellman, Contreras, Dugas, O’Loughlin, & O’Loughlin,
2014). Alcohol BD is more severe among individuals with mental
health problems and excessive alcohol consumption, which can in
turn increase psychological distress. Suicide ideation and attempted
suicide are also more prevalent in BD adolescents (Xing et al., 2006).
Young BD adults had several sleep problems (trouble falling sleep,
trouble staying asleep, and snoring/sleep apnea), independent of
Heavy Episodic Drinking or Binge Drinking Chapter | 36 391
psychiatric conditions, in a dose–response relationship (Popovici &
French, 2013). While insomnia seems to be significantly associated
in both sexes, the snoring/sleep apnea is related to BD only in males.
Ethanol also increases neuroinflammation in the CNS, and
research has also observed persistent neuroimmune activation in
BD, which could contribute to neurocognitive dysfunction in the
prefrontal cortex (PFC) (Vetreno & Crews, 2012), as well as in
myelination and white matter integrity (Jacobus, Squeglia, Bava,
& Tapert, 2013). Brain-derived neurotrophic factor (BDNF) is a
molecule identified as a major regulator of structural changes and
inflammation processes in the brain related to alcohol use. The
chronic BD pattern produces a decrease of BDNF, which correlates with lower survival and neuronal differentiation of cells in
the hippocampus and the development of a depressive phenotype
during the withdrawal period (Briones & Woods, 2013).
Moreover, a critical role of the corticotropin-releasing factor type 1 receptor in excessive ethanol intake has been observed
related to stress response, in both models of BD and alcohol dependence (Kaur, Li, Stenzel-Poore, & Ryabynin, 2012). There is also
evidence that BD upregulates the group 1 metabotropic glutamate
receptor signaling throughout the amygdala (Cozzoli et al., 2014).
TABLE 2 Main Negative Consequences on Health and
Neuropsychological Performance of Binge Drinking
Acute negative
consequences
Cardiovascular and
metabolic diseases
Psychological distress
and mental disorders
Death by ethylic intoxication
Physical injury
Motor vehicle accidents
Physical fights
Unplanned sex
Unintended pregnancy
Violent behavior
Coronary artery disease
Stroke
Insulin resistance
Metabolic syndrome
Type 2 diabetes
Anxiety
Depression
Alcohol dependence
Suicide (ideation and attempts)
Insomnia (trouble falling sleep and
staying asleep)
Snoring/sleep apnea (only men)
Neurological diseases
Neuroinflammation
Persistent neuroimmune activation
Dysfunctions in myelination
Alterations in the white matter integrity
Maladaptive response to stress
Neuropsychological
deficits
Sustained attention
Memory (declarative, semantic,
prospective and working)
Associative learning
Inhibitory control
Decision making
The consequences are those evidenced by the research on adolescents,
young adult, and adult participants with a consumption pattern of
binge drinking.
Both mechanisms may be keys in the neurobiological mechanisms
that underlie the transition from BD to ethanol dependence.
RISK AND PROTECTION FACTORS
ASSOCIATED WITH BD
Drawing an explicative model of BD behavior is a highly complex
task because there is a wide variety of interrelated factors in different domains, which in turn depend on the country, the sample, and
the factors to be studied. Tables 3 and 4 show the main risk and
protection factors associated with BD, respectively.
Most works have found a higher prevalence of BD and more
drink intake in one single episode in males (Chavez et al., 2011;
Hibell et al., 2009; Pedersen & von Soest, 2013). Moreover, there
are differences between men and women in BD relating to their
expectations towards drinking and to positive alcohol metacognitions. Women’s expectations are related to improving their
sociability and sexual ability, while men’s are geared to reducing
stress (Balodis, Potenza, & Olmstead, 2009). The positive alcohol metacognitions about cognitive self-regulation are a significant predictor of weekly levels of alcohol use in BD males (Clark
et al., 2012). It is highly relevant to take into account the specific
features associated with sex in the study of BD and the design of
possible interventions.
Regarding age, the range and cutoff points used in different studies condition the data available. However alcohol intake
TABLE 3 Risk Factors Associated to Binge Drinking (BD)
Behavior in Adolescents and Young People
Individual
characteristics
Sex (men)
Adolescents and young
Early pubertal timing
Evening-type
Social and
educational
Easy alcohol access
Cheap alcohol
Low socioeconomic status
Adverse socioeconomic conditions
Family, parents,
and peers
Parental alcohol consumption
Parental BD
Friends alcohol use
Other drug
consumption
Smoking
Marijuana use
Activities, beliefs,
cognitions
Unaware of the risk of BD
Unauthorized absence from the school
(truancy)
Sport involvement
Use of products to enhance physique
muscular
Personality traits
High impulsivity
High novelty seeking
High extraversion
Low agreeableness
Low conscientiousness
The factors are those obtained in the studies revised, related to the practice
of binge drinking and/or which are predictors of sustained BD behavior.
392 PART | III Alcohol
TABLE 4 Protective Factors Associated to Binge Drinking
(BD) Behavior in Adolescents and Young People
Individual
characteristics
High intelligence
morning-type
Social and
educational
Educational achievement
Higher school grades
Occupational levels
Stronger policy environment
Family, parents,
and peers
Parental monitoring (control and
supervision)
Parental support
Family oriented leisure
Higher parental education (only
for extreme BD)
Activities, beliefs,
cognitions
School attachment
Participation in school and nonschool activities
Religious involvement
Belief that alcohol produces
cognitive self-regulation (only men)
Belief that alcohol enhances
sociability and sexuality (only women)
Personality traits
Low impulsivity
Low novelty seeking
High conscientiousness
The factors are those obtained in the studies revised, related to the practice
of non-binge drinking and/or not maintaining that behavior over time.
with BD behavior is a huge concern in all countries where there
are statistics on the topic. In the United States and England, the
prevalence among college students ranges from 43% to 58.5% in
men and 32% to 54% in women (Howell et al., 2013). In Spain, a
survey on this type of alcohol intake among teenagers and young
adults (Spanish Observatory on Drugs, 2013) reported an increase
of BD, which taking into account the previous 30 days was 35% in
men and 20% in women aged 20–24.
The study of predictors of sustained BD in young adults shows
similar determinants, being higher in males with no college/
university studies (Pedersen & von Soest, 2013; Wellman et al.,
2014). BD is related to parents and peers who also drink alcohol (Weitzman, Nelson, & Wechsler, 2003; Pedersen & von Soest,
2013; Strickly et al., 2013). Higher parental education is a protective factor for extreme BD, but it is a risk factor when considering
BD for ≥5 drinks (Patrick et al., 2013).
College students more exposed to “wet” environments—
defined as social, residential, and market surroundings where
drinking is prevalent and alcohol is cheap and easily accessed—
are more likely to engage in BD (Strickly et al., 2013; Weitzman
et al., 2003). Moreover, girls and boys who practice BD are more
prone to engage in all forms of substance use, with frequent polyconsumption. Tobacco and marijuana consumption are the most
frequent (Stickley et al., 2013) and are predictors of the intensity
of BD (Patrick et al., 2013). BD is a risk factor in the development
of alcohol dependence (Balodis et al., 2009; White et al., 2011).
Moreover, binge drinkers tend to be unaware of the risks of BD
(Strickley et al., 2013).
It is very important to perform longitudinal studies to assess
the correlates of adult BD. In this sense, we want to highlight a
study by Cheng and Furnham (2013), who investigated the association of several variables as predictors of BD in 50-year-old adults
from England. The results showed that individuals who come from
lower parental social class with adverse socioeconomic conditions
tend to develop more alcohol abuse behavior; in addition, childhood intelligence, educational achievement, and occupational levels were negatively associated with hazardous adult BD. Another
variable related to BD in adolescents is school attachment, with
truancy (unauthorized absence from the school) being a risk factor (Stickley et al., 2013). Frequent BD precedes long-term unemployment, but only in women; this result has little support for
the social causation hypothesis because it appears after controlling for many potential confounder factors (Backhans, Lundin, &
Hemmingsson, 2012). Social exclusion is also another consequence related to BD in the long term (Viner & Taylor, 2007).
A longitudinal study by Pedersen and von Soest (2013) in
Norway found that the frequency of alcohol consumption and BD
in parents predicted BD in their offspring at age 28, independently
of sex. This study also observed that parental monitoring (control
and supervision) and support with alcohol measures is of particular importance as a protective factor in adolescence.
In adolescents with accelerating BD trajectory, there is
an early pubertal timing, low socioeconomic status, and more
sport involvement compared to those classified as “stable low”
(Modecki et al., 2014). However, participation in organized school
or nonschool activities for early maturers protects against development of a “steep increase” trajectory. In addition, there is a higher
probability for starting BD behavior in males who are highly concerned about muscularity and use supplements and other products
to enhance their physique (Field et al., 2013).
Finally, it is important to highlight that a large majority of
adolescents and young adults continue the BD behavior despite
their knowledge of health risk (Zwaluw, Kleinjan, Lemmers,
Spijkerman, & Engels, 2013). This may be explained by the theory
of cognitive dissonance, which means that the drinkers’ existing
attitudes and cognitions will be modified to match the BD behavior. This suggests that, although knowledge and attitudes are
treated in prevention, these may be inefficient on BD behavior.
PERSONALITY TRAITS, CIRCADIAN
TYPOLOGY, AND BD
The study of personality traits associated with BD has confirmed
consistently the presence of higher impulsivity (White et al., 2011;
Townshend et al., 2014) and novelty seeking (Wellman et al.,
2014) in youths, with both features being predictors of maintenance in the BD pattern. Both personality dimensions are also
related to several nonadaptive behaviors and mental disorders,
mainly substance use disorders (Marquez-Arrico & Adan, 2013).
Most personality questionnaires include an impulsivity dimension, although there are also specific instruments to measure it.
The Dickman Impulsivity Inventory (DII, Dickman, 1990) may be
highlighted because it proposes the existence of functional impulsivity as the tendency to make quick decisions when required
by the situation to favor the person, in contrast to dysfunctional
impulsivity, which is related to quick but irreflexive decisions that
lead to negative consequences. Youths with BD, especially men,
Heavy Episodic Drinking or Binge Drinking Chapter | 36 393
Dysfunctional impulsivity
Sex
Women
Men
50
40
performance in the early part of the day. In contrast, evening-type
subjects go to bed and wake up late, and perform at their best
toward the end of the day and evening hours. The evening-type,
especially teenagers and young adults, show a personality pattern
of higher impulsivity, novelty seeking, extraversion, and activity,
and lower conscientiousness and harm avoidance. All the existing
data also suggest that circadian typology is related to the consumption of all types of drugs and BD, with morning-type being a protective factor and evening-type a risk factor (Prat & Adan, 2011).
NEUROPSYCHOLOGICAL IMPACT OF BD
30
20
10
Control
Binge drinking
Alcohol consumption
FIGURE 1 Dysfunctional impulsivity scores of binge drinking (BD)
and control groups according to sex. The scores on dysfunctional impulsivity are higher in the BD group than in the control group. Men obtain
higher scores in impulsivity, especially in the BD group. Dysfunctional
impulsivity was measured using the Dickman Impulsivity Inventory
(1990), with scores ranging from 12 to 60. Data from Adan (2012), with
permission from the publishers.
obtain higher scores only in dysfunctional impulsivity compared
to controls (Adan, 2012), as Figure 1 shows.
Impulsivity is the most consistent personality trait related to
early use of drugs, repetition of intake, and progression to addiction,
and it is a condition promoted with consumption that also favors
relapse (Perry & Carroll, 2008). The data available on novelty seeking, defined as the need for adventure and excitement, preference
for risk and strong emotions, boredom susceptibility, and disinhibition, point in the same direction (Castellanos-Ryan, Rubia, &
Conrod, 2011). The disinhibition dimension is the best BAC predictor in both sexes (Legrand, Gomà-i-Freixanet, Kaltenbach, & Joli,
2007). Impulsivity and novelty seeking may explain the poor performance in executive tasks seen in teenagers (Castellanos-Ryan et al.,
2011) and in addiction disorders (Dolan, Bechara, & Nathan, 2009).
Using the “Big Five” model of personality traits (extraversion,
emotionality/neuroticism, conscientiousness, agreeableness, and
intellect/openness) in a longitudinal birth cohort study, Cheng and
Furnham (2013) observed that high extraversion and low agreeableness were significant predictors of BD. In other research, low conscientiousness also appears as a predictor of weekly levels of alcohol
in BD university students (Clark et al., 2012). Perhaps not only one
but the combination of several personality traits may configure in
the future an endophenotype for the onset and maintenance of BD.
Circadian typology (morning-type, neither-type, and eveningtype) is an individual difference that affects our biological and
psychological functioning—not only in health, but also in disease
(Adan et al., 2012 for a review). Morning-type subjects go to bed
early and wake up early, and achieve their peak mental and physical
The study of the possible cognitive impact of BD is recent and
the existing studies are difficult to compare due to methodological
aspects that may influence the results (small samples, several definitions and duration of BD, use of different tasks, variable ages,
etc.). The lack of control of the educational level, the consumption
of other substances, the presence of psychopathological traits, and
personality traits may greatly affect the results. The available data
suggest that there are deficits in the cognitive performance in sustained attention tasks and memory and PFC activity tasks similar
to those found in long-term alcohol abuse subjects, although to a
lesser extent and with more mixed results.
In considering the neuropsychological impact of BD, we
should distinguish between the effects of a single episode (next
day) and those that may come from a sustained BD behavior over
time (see Table 2). In both cases, the assessments are carried out
with a zero BAC.
Effects of a Single Episode of BD
Neurocognitive impairment are found in subjective alertness,
memory retrieval processes (delayed recall), and reaction time,
while performance in attention tasks is not significantly impaired
(McKinney, Coyle, & Verster, 2012; Verster, van Duin, Volkerts,
Schreuder, & Verbaten, 2003). The pattern of impulsive acting,
objectively assessed with inhibition tasks, also increases independently from individual differences in the impulsivity trait
(McCarthy, Niculete, Treloar, Morris, & Bartholow, 2012).
Effects of BD on Learning and Memory Tasks
Studies have focused on retrospective memory in which learning,
retention, and retrieval are evaluated. The existence of memory
deficits under chronic alcohol consumption is well established,
linked to alterations in the hippocampus and PFC. BD students
perform worse in declarative memory tasks, both in immediate
and delayed recall (Parada et al., 2011b). BD young adults present
behavioral impairments in sustained attention, working memory,
and associative learning (Parada et al., 2012; Scaife & Duka, 2009;
Stephens and Duka, 2008).
For working memory, at an early age in young binge drinkers
without AUD or mental comorbidity, the performance at a behavioral level is adequate. However, hypoactivation of the right anterior PFC was obtained using combined event-related potentials
(ERP) and exact low-resolution brain electromagnetic tomography (Crego et al., 2010). Using functional magnetic resonance
imaging (fMRI), higher bilateral activity in the supplementary
premotor area was observed in a BD condition, as well as a
394 PART | III Alcohol
positive correlation between the number of drinks consumed per
event and the activity in the dorsomedial PFC and the cerebellar-­
thalamic-insular regions (Campanella et al., 2013).
The assessment of prospective memory (PM), conceptualized
as the cognitive ability to remember to carry out some activity at
some future point in time, is a crucial aspect of everyday cognitive
function, and it is sensible to exhibit neuropsychological sequels
associated with BD. Adolescents and young adults with BD showed
impairments in a task of PM with fewer location–action combinations to recall (Heffernann, Clark, Bartholomew, Ling, & Stephens,
2010) and reduced function on time-based tasks (Heffernann &
O’Neill, 2012) when compared with non-binge drinkers.
Effects of BD on Executive Functions
In BD university students, deficits in behavioral inhibition tasks
have been observed, reflecting impulsivity and poorer decision
making (Field, Schoenmakers, & Wiers, 2008; Scaife & Duka,
2009). This is more evident in high BD than in low BD subjects
(Townshend et al., 2014), in men, and in those who engage in
heavy BD at an early age (Goudriaan, Grekin, & Sher, 2011).
The assessment of decision-making using the Iowa Gambling
Task has found a pattern of “short-sightedness” for future consequences in BD, similar to that in addiction patients, and
which implies impulsive behavior with lower inhibitory control
(Johnson et al., 2008).
Heavy binge drinkers performed worse on a battery of
tasks of executive functions compared with light social drinkers (Montgomery, Fisk, Murphy, Ryland, & Hilton, 2012). They
generated significantly fewer words in a word fluency task
(access to semantic memory), had worse random letter generation (inhibitory control), and had greater switch cost on a random
letter task (switching), as shown in Figure 2.
In the revision by Stephens & Duka’s (2008), BD deficits in
executive functions were found to underlie functional hyperactivity impairments in the PFC and the amygdala, which may cause
neurotoxicity with time. Because the PFC and other brain areas
involved are subject to development and maturation during adolescence and emerging adulthood, BD until the age of 24 poses
a bigger harm to executive functioning than in later stages of life
(Hermens et al., 2013).
The appearance of alterations in brain functions when effects
in behavioral neurocognitive performance are not yet observable
points at early cerebral disturbances, which should be studied in
the future to check whether they persist when the BD habit ceases,
as well as the possibility that they may be considered endophenotypes of the progression from BD to AUD. In this direction, the
longitudinal study by Dager et al. (2013) using fMRI has identified that an amplified cue-elicited brain response was the most significant predictor of the emergence of BD and subsequent AUD.
The overactivated regions were linked to habit formation, decision
making, motivation, and attention.
FUTURE RESEARCH ON PREVENTION
AND/OR TREATMENT ON BD
Countries affected by BD should set it as a priority to promote
actions to reduce the number of persons practicing BD and the
intensity of the associated intoxications. Some strategies that have
FIGURE 2 Executive functioning performance (standardized scores)
in light and heavy alcohol social drinkers. Participants were 18–25 years
old, had never used illicit substances, and had never been diagnosed with
a substance use disorder or been advised to reduce their drinking. Heavy
social drinkers generated significantly fewer words in a word fluency task
(access to semantic memory), had worse random letter generation (RLG;
inhibitory control), and greater switch cost on a random letter task (switching).
Data re-elaborated from Montgomery et al. (2012).
proven effective in reducing alcohol consumption involve limiting
the availability of alcohol, raising its price, promoting substance
and alcohol-free environments (Naimi et al., 2014), and blocking
legal access to alcohol to a later age. Although we might acknowledge that alcohol consumption may continue and that it is not
realistic to advocate abstinence, promoting less harmful drinking
patterns and their frequency is an advisable harm reduction strategy
(Plunk et al., 2014).
Preventive and therapeutic approaches should take into
account circadian rhythmicity. Involving chronobiology in prevention implies not only promoting healthy leisure activities or
“what to do,” but also placing such activities in appropriate daytime temporal moments or “when to do” them (Adan et al., 2012).
Chronobiological therapeutic strategies such as to establish regular time patterns of sleep-wake, meals, and daily activity with a
tendency towards a morning-type functioning, and exposition to
light therapy and melatonin administration, may also be effective.
Few works have assessed the efficacy of interventions aimed
at reducing dependence or intensity of BD in the population. The
brief motivational intervention (BMI) is one of the few effective
strategies for diminishing alcohol consumption. A single face-­
to-face session of BMI in a BD group was found to reduce alcohol
use among subjects who experienced one or more alcohol-related
adverse consequences (19% less drinking), whereas no preventive effect was obtained in control subjects (Daeppen et al., 2011).
More research is needed in this area in the near future.
To conclude, research on pharmaceutical targets to avoid the
health consequences of BD and the progression to AUD will hopefully offer knowledge to be applied in the clinic in the future, based
on the promising findings from behavioral genetic approaches,
such as the reduction of the BDNF or the upregulation of glutamate
receptors in BD.
Heavy Episodic Drinking or Binge Drinking Chapter | 36 395
APPLICATIONS TO OTHER ADDICTIONS
AND SUBSTANCE MISUSE
KEY FACTS OF NEUROPSYCHOLOGY
IN BINGE DRINKERS
As we have seen in this chapter, the pattern of alcohol BD involves
significant risks to both the immediate and short-term health outcomes of those who practice it. BD is more dangerous in the case
of adolescents because the toxic amounts of alcohol in their bodies under maturation process aggravate the risks. The possible
changes in gene expression and in a wide variety of neurotransmission systems should be noted, among which stands out the
reinforcement dopaminergic pathway. These changes significantly
increase biological vulnerability to progress towards the development of a substance use disorder, not just for alcohol or other
substances with depressant pharmacological profile but in general.
Similarly, these effects on the CNS can participate in the development of other mental disorders, such as depression and anxiety
with and without comorbidity to the addictive disorder. The need
to improve the knowledge about evidence-based treatments should
be emphasized. However, efforts should prioritize developing
preventive strategies starting in childhood in order to enhance the
protective factors of BD practice.
lAssessing
DEFINITION OF TERMS
Attention Attention is a complex concept that represents a cohesive
set of processes, which include sensory, motor, and cognitive
processing.
Binge drinking Binge drinking is an intermittent pattern of heavy alcohol consumption of ≥5 drinks for men and ≥4 drinks for women, in
one single event and at least once in the past two weeks.
Circadian typology This individual difference (morning-, neither- and
evening-type) affects our biological and psychological functioning
in health and in disease. Morning-types go to bed early and wake
up early, and achieve their mental and physical peak performance in
the early part of the day, in contrast to the evening-types.
Endophenotype This is an internal, inheritable, and measurable trait
marker of vulnerability to develop a particular disease.
Executive functioning This set of cognitive skills is mainly linked
to the functioning of the brain frontal lobe, which includes mental flexibility, planning and abstract reasoning abilities, selfregulation, and task monitoring, which determine goal-directed
behavior.
Functional impulsivity Functional impulsivity is a tendency to make
quick decisions to one’s benefit when required by the situation.
Inhibition This mechanism prevents the entrance of nonpertinent
information into working memory and suppresses information that
has become irrelevant for a current task.
Impulsivity or dysfunctional impulsivity This personality trait is
defined as the tendency to act with lack of prevision, making quick
and irreflexive decisions that lead to negative consequences.
Novelty seeking This personality trait is characterized by a need for
adventure and excitement, preference for risk, and strong emotions by the mere fact of living them, boredom susceptibility, and
disinhibition.
Prospective memory This is the cognitive ability to remember to carry
out some activity at some future point in time.
Working memory Working memory is the ability to hold and manipulate information in the mind over short periods of time—a mental
workspace that is used to store important information in the course
of our everyday lives.
cognitive performance is more difficult than assessing biological aspects, because even in simple cognitive tasks
there are several skills involved in their resolution (attention,
motor control, etc.).
l
BD behavior increases neuroinflammation in the CNS,
which may contribute to dysfunction in PFC, myelination,
and white matter integrity related to neuropsychological
deficits.
lIn healthy young binge drinkers, deficits have been found in
sustained attention, learning, memory (declarative, semantic,
prospective and working), and executive functions (inhibition
control and decision making).
l
Early cerebral disturbances measured by ERPs or fMRI in
brain activity may be detected when effects on behavioral performance are not yet observable.
l
Until the age of 24, BD behavior poses a larger harm than
in later stages of life, because the brain areas implicated in
the observed cognitive impairments (PFC, hippocampus and
amygdala) are subject to development and maturation during
adolescence and emerging adulthood.
l
Future research should control factors that have a notorious
influence on cognitive performance and that have been related
to BD (level of education, consumption of other substances,
personality traits, etc.) in order to reach more robust conclusions in this area.
SUMMARY POINTS
l
This
chapter focuses on the findings, mainly during the last
decade, on the impact of BD.
l
BD in the United States, Europe, and most developed countries is a major health and social concern, with significant
social and personal costs.
lMortality risk and comorbidity with physical (cardiovascular
diseases, diabetes, metabolic syndrome, neurodegeneration)
and mental (anxiety, depression, suicide, sleep disorders)
pathologies are more prevalent in binge drinkers.
l
Adolescents and young binge drinkers show neurocognitive
impairments similar to those found in long-term alcohol abuse,
although to a lesser extent and with more mixed results.
lThe presence of high impulsivity and novelty seeking in young
people are the best personality traits to predict the appearance
and maintenance of the BD pattern.
l
Circadian typology is a remarkable individual difference in
BD and all addictive behaviors, with the morning-type being a
protective factor and the evening-type being a risk factor.
l
We need more systematic research on the effects of BD,
preferably longitudinal studies incorporating biological and
behavioral measures.
l
Prevention and therapeutic interventions should give priority
to BD, promoting protective factors and reducing risk factors
known to affect its appearance and maintenance.
ACKNOWLEDGMENT
This work was supported by a grant from the Spanish Ministry of
Economy and Competitiveness (PSI2012-32669).
396 PART | III Alcohol
REFERENCES
Adan, A. (2012). Functional and dysfunctional impulsivity in young binge
drinkers. Adicciones, 24, 17–22.
Adan, A., Archer, S. N., Hidalgo, M. P., Di Milia, L., Natale, V., & Randler, C.
(2012). Circadian typology: a comprehensive review. Chronobiology
International, 29, 1153–1175.
Bachman, J. G., Johnston, L. D., & O’Malley, P. M. (1981). Smoking, drinking, and drug use among American high school students: correlates and
trends, 1975–1979. American Journal of Public Health, 71, 59–69.
Backhans, M. C., Lundin, A., & Hemmingsson, T. (2012). Binge drinking –
a predictor for or a consequence of unemployment? Alcoholism: Clinical
and Experimental Research, 36, 1983–1990.
Balodis, I. M., Potenza, M. N., & Olmstead, M. C. (2009). Binge drinking
in undergraduates: relationships with sex, drinking behaviours, impulsivity, and the perceived effects of alcohol. Behavioral Pharmacology,
20, 518–526.
Balogun, O., Koyanagi, A., Stickley, A., Gilmour, S., & Shibuya, K. (2014).
Alcohol consumption and psychological distress in adolescents: a
multi-country study. Journal of Adolescent Health, 54, 228–234.
Barnet, N. P., Clerkin, E. M., Wood, M., Monti, P. M., O’Leary Tewyan, T.,
Corriveau, D., … Kahler, W. K. (2014). Description and predictors of
positive and negative alcohol-related consequences in the first year of
college. Journal of Studies on Alcohol and Drugs, 75, 103–114.
Briones, T. L., & Woods, J. (2013). Chronic binge-like alcohol consumption
in adolescence causes depression-like symptoms possible mediated by
the effects of BDNF on neurogenesis. Neurocience, 254, 324–334.
Campanella, S., Peigneux, P., Petit, G., Lallemand, F., Saeremans, M.,
Noël, X., … Verbanck, P. (2013). Increased cortical activity in binge
drinkers during working memory task: a preliminary assessment
through a functional Magnetic Resonance Imaging. PLoS One, 8(4),
e62260. http://dx.doi.org/10.1371/journal.pone.0062260.
Castellanos-Ryan, N., Rubia, K., & Conrod, P. J. (2011). Response inhibition and reward response bias mediate the predictive relationships
between impulsivity and sensation seeking and common and unique
variance in conduct disorder and substance misuse. Alcoholism: Clinical and Experimental Research, 35, 140–155.
Chavez, P. R., Nelson, D. E., Naimi, T. S., & Brewer, R. D. (2011). Impact of the
new gender-specific definition for binge drinking on prevalence estimates
for women. American Journal of Preventive Medicine, 40, 468–471.
Cheng, H., & Furnham, A. (2013). Correlates of adult binge drinking: evidence from a British cohort. PLoS One, 8(11), e78838.
http://dx.doi.org/10.1371/journal.pone.007838.
Clark, A., Tran, C., Weiss, A., Caselli, G., Nikčević, A. V., & Spada, M. M.
(2012). Personality and alcohol metacognitions as predictors of weekly
levels of alcohol use in binge drinking university students. Addictive
Behaviors, 37, 537–540.
Cozzoli, D. K., Courson, J., Wroten, M. G., Greentree, D. I., Lum, E. M.,
Campbell, R. N., … Szumlinski, K. K. (2014). Binge alcohol drinking by mice requires intact group I metabotropic glutamate receptor
signalling within the central nucleus of the amygdale. Neuropsychopharmacology, 39, 435–444.
Crego, A., Rodríguez-Holguín, S., Parada, M., Mota, N., Corral, M., &
Cadaveira, F. (2010). Reduced anterior prefrontal cortex activation in
young binge drinkers during a visual working memory task. Drug and
Alcohol Dependence, 109, 45–56.
Daeppen, J.-B., Bertholet, N., Gaume, J., Fortini, C., Faouzi, M., & Gmel, G.
(2011). Efficacy of brief motivational intervention in reducing binge
drinking in young men: a randomized controlled trial. Drug and
Alcohol Dependence, 113, 69–75.
Dager, A. D., Anderson, B. M., Rosen, R., Khadka, S., Sawyer, B.,
Jiantonio-Kelly, R. E., … Pearlson, G. D. (2013). Functional magnetic
resonance imaging (fMRI) response to alcohol pictures predicts subsequent transition to heavy drinking in college students. Addiction, 109,
585–595.
Dickman, S. J. (1990). Functional and dysfunctional impulsivity: personality and cognitive correlates. Journal of Personality and Social Psychology, 58, 95–102.
Dolan, S. L., Bechara, A., & Nathan, P. E. (2009). Executive dysfunction
as a risk marker for substance abuse: the role of impulsive personality
traits. Behavioral Sciences and the Law, 26, 799–822.
Field, A. E., Sonneville, K. R., Crosby, R. D., Swanson, S. A., Eddy, K. T.,
Camargo, C. A., … Micali, N. (2013). Prospective associations of
concerns about physique and the development of obesity, binge drinking, and drug use among adolescent boys and young adult men. JAMA
Pediatrics, 168, 34–39.
Field, M., Schoenmakers, T., & Wiers, R. W. (2008). Cognitive processes
in alcohol binges: a review and research agenda. Current Drug Abuse
Reviews, 1, 263–279.
Goslawski, M., Piano, M. R., Bian, J.-T., Church, E. C., Szczurek, M., &
Phillips, S. A. (2013). Binge drinking impairs vascular function in
young adults. Journal of the American College of Cardiology, 62,
201–207.
Goudriaan, A. E., Grekin, E. R., & Sher, K. J. (2011). Decision making
and response inhibition as predictor of heavy alcohol use: a prospective study. Alcoholism: Clinical and Experimental Research, 35, 1–8.
Heffernann, T., Clark, R., Bartholomew, J., Ling, J., & Stephens, S. (2010).
Does binge drinking in teenagers affect their everyday prospective
memory. Drug and Alcohol Dependence, 109, 73–78.
Heffernann, T., & O’Neill, T. (2012). Time based prospective memory
deficits associated with binge drinking: evidence from the Cambridge
Prospective Memory Test. Drug and Alcohol Dependence, 123,
207–212.
Hermens, D. F., Lagopoulos, J., Tobías-Webb, J., Tamara De Regt, T.,
Dore, G., Juckes, L., … Hickie, I. B. (2013). Pathways to alcoholinduced brain impairment in young people: a review. Cortex, 49,
3–17.
Hibell, B., Guttormsson, U., Ahlström, S., Balakireva, O., Bjarnason, T.,
Kokkevi, A., & Kraus, L. (2009). The 2007 ESPAD report. Substance
use among students in 35 European countries. Stockholm: The Swedish Council for Information on Alcohol and Other Drugs.
Howell, N. A., Worbe, Y., Lange, I., Tait, R., Irvine, M., Banca, P., …
Voon, V. (2013). Increased ventral striatal volume in college-aged binge
drinkers. PLoS One, 8(9), e74164. http://dx.doi.org/10.1371/journal.
pone.0074164.
International Center for Alcohol Policies (ICAP). (2010). International
drinking guidelines. http://www.icap.org/Table/InternationalDrinking
Guidelines.
Jacobus, J., Squeglia, L. M., Bava, S., & Tapert, S. F. (2013). White matter characterization of adolescent binge drinking with and without
co-­occurring marijuana use: a 3-year investigation. Psychiatry Research:
Neuroimaging, 214, 374–381.
Johnson, C. A., Xiao, L., Palmer, P., Sun, P., Wang, Q., Wei, Y., … Bechara, A.
(2008). Affective decision-making deficits, linked to dysfunctional ventromedial prefrontal cortex, revealed in 10th grade Chinese adolescent
binge drinkers. Neuropsychologia, 46, 714–726.
Kaur, S., Li, J., Stenzel-Poore, M. P., & Ryabynin, A. E. (2012).
Corticotropin-­releasing factor acting on corticotropin-releasing factor
receptor type I is critical for binger alcohol drinking in mice. Alcoholism:
Clinical and Experimental Research, 36, 369–376.
Heavy Episodic Drinking or Binge Drinking Chapter | 36 397
Legrand, F. D., Gomà-i-Freixanet, M., Kaltenbach, M. L., & Joli, P. M.
(2007). Association between sensation seeking and alcohol consumption in French college students: some ecological data collected in “open
bar” parties. Personality and Individual Differences, 43, 1950–1959.
Lindtner, C., Scherer, T., Zielinski, E., Filatova, N., Fasshauer, M., Tonks, N.
K., … Buettner, C. (2013). Binge drinking induces whole-body insulin
resistance by impairing hypothalamic insulin action. Science Translational
Medicine, 5, 170ra14 http://dx.doi.org/10.1126/scitranslmed.3005123.
Marquez-Arrico, J. E., & Adan, A. (2013). Dual diagnosis and personality traits: current situation and future research directions. Adicciones,
25(13), 195–202.
McCarthy, D. M., Niculete, M. E., Treloar, H. R., Morris, D. H., & Bartholow,
B. D. (2012). Acute alcohol effects on impulsivity: associations with
drinking and driving behavior. Addiction, 107, 2109–2114.
McKinney, A., Coyle, K., & Verster, J. (2012). Direct comparison of the
cognitive effects of acute alcohol with the morning after a normal
night’s drinking. Human Psychopharmacology: Clinical and Experimental Research, 27, 295–304.
Modecki, K. L., Barber, B. L., & Eccles, J. S. (2014). Binge drinking trajectories across adolescents: for early maturing youth, extra-curricular
activities are protective. Journal of Adolescent Health, 54, 61–66.
Montgomery, C., Fisk, J. E., Murphy, P. N., Ryland, I., & Hilton, J.
(2012). The effects of heavy social drinking on executive function:
a systematic review and meta-analytic study of existing literature and
new empirical findings. Human Psychopharmacology: Clinical and
Experimental Research, 27, 187–199.
Naimi, T. S., Blachette, J., Nelson, T. F., Nguyen, T., Oussayef, N., Heeren,
T. C., … Xuan, Z. (2014). A new scale of the U.S. alcohol policy
environment and its relationship to binge drinking. American Journal
of Preventive Medicine, 46, 10–16.
National Institute on Alcohol Abuse and Alcoholism. (2000). NIAAA: 10th
special report to the US congress on alcohol and health. Bethesda:
National Institutes of Health.
National Institute on Alcohol Abuse and Alcoholism. (2004). NIAAA council
approves definition of binge drinking. NIAAA Newsletter. No 3. Winter.
Observatorio Español sobre Drogas. Delegación del Gobierno para el
Plan Nacional sobre Drogas. (2013). Encuesta domiciliaria sobre
alcohol y drogas de España (EDADES). 2011/2012. Disponible en:
http://www.pnsd.msc.es/Categoria2/observa/pdf/EDADES2011.pdf.
Parada, M., Corral, M., Caamaño-Isorna, F., Mota, N., Crego, A.,
Rodríguez-­Olguín, S., & Cadaveira, F. (2011a). Definición del concepto de consumo intensivo de alcohol adolescente (binge drinking).
Adicciones, 23, 53–63.
Parada, M., Corral, M., Caamaño-Isorna, F., Mota, N., Crego, A.,
Rodríguez-Olguín, S., & Cadaveira, F. (2011b). Binge drinking and
declarative memory in university students. Alcoholism, Clinical and
Experimental Research, 35, 1–10.
Parada, M., Corral, M., Mota, N., Crego, A., Rodríguez-Olguín, S., &
Cadaveira, F. (2012). Executive functioning and alcohol binge drinking in university students. Addictive Behaviors, 37, 167–172.
Patrick, M. E., Schulenberg, J. E., Martz, M. E., Maggs, J. L., O’Malley,
P. M., & Johnston, L. D. (2013). Extreme binge drinking among 12thgrade students in the United States. JAMA Pediatrics, 167, 1019–1025.
Pedersen, W., & von Soest, T. (2013). Socialization to binge drinking: a
population-based, longitudinal study with emphasis on parental influences. Drug and Alcohol Dependence, 133, 587–592.
Perry, J. L., & Carroll, M. E. (2008). The role of impulsive behavior in drug
abuse. Psychopharmacology, 200, 1–26.
Plunk, A. D., Syed-Mohammed, H., Cavazos-Rehg, P., Bierut, L. J., &
Grucza, R. A. (2014). Alcohol consumption, heavy drinking, and
mortality: rethinking the J-shaped curve. Alcoholism: Clinical and
Experimental Research, 38, 471–478.
Popovici, I., & French, M. T. (2013). Binge drinking and sleep problems
among young adults. Drug and Alcohol Dependence, 132, 207–215.
Prat, G., & Adan, A. (2011). Influence of circadian typology on drug consume, hazardous alcohol use and hangover symptoms. Chronobiology
International, 28, 248–257.
Saunders, J. B., Aasland, G., Amundsen, A., & Grant, M. (1993). Alcohol consumption and related problems among primary health care
patients: WHO collaborative project on early detection of person with
harmful alcohol consumption I. Addiction, 88, 349–362.
Scaife, J. C., & Duka, T. (2009). Behavioural measures of frontal lobe
function in a population of young social drinkers with binge drinking
pattern. Pharmacology, Biochemistry and Behavior, 93, 354–362.
Stephens, D. N., & Duka, T. (2008). Cognitive and emotional consequences
of binge drinking: role of amygdala and prefrontal cortex. Philosophical
Transactions of the Royal Society of Biological Sciences, 363, 3169–3179.
Stickley, A., Koyanagi, A., Koposov, R., Razvodovsky, Y., & Ruchkin, V.
(2013). Adolescent binge drinking and risky health behaviours: findings
from northern Russia. Drug and Alcohol Dependence, 133, 838–844.
Thiele, T. E. (2012). Commentary: studies on binge-like ethanol drinking
may help to identify the neurobiological mechanisms underlying the
transition to dependence. Alcohol Clinical and Experimental Research,
36, 193–196.
Townshend, J. M., Kambouropoulos, N., Griffin, A., Hunt, F. J., & Milani,
R. M. (2014). Binge drinking, reflection impulsivity, and unplanned
sexual behavior: Impaired decision-making in young social drinkers.
Alcoholism: Clinical and Experimental Research, 30, 1143–1150.
Verster, J. C., van Duin, D., Volkerts, E. R., Schreuder, A., & Verbaten,
M. N. (2003). Alcohol hangover effects on memory functioning and
vigilance performance after an evening of binge drinking. Neuropsychopharmacology, 28, 740–746.
Vetreno, R. P., & Crews, F. T. (2012). Adolescent binge drinking increases
expression of the danger signal receptor agonist HMGB1 and Toll-like
receptors in the adult prefrontal cortex. Neuroscience, 226, 475–488.
Viner, R. M., & Taylor, B. (2007). Adult outcomes of binge drinking in
adolescence: findings from a UK national birth cohort. Journal of Epidemiological Community Health, 61, 902–907.
Wechsler, H., Davenport, A., Dowdall, G., Moeykens, B., & Castillo, S.
(1994). Health and behavioral consequences of binge drinking in college. A national survey of students at 140 campuses. Journal of the
American Medical Association, 272, 1672–1677.
Weitzman, E. R., Nelson, T. F., & Wechsler, H. (2003). Taking up binge
drinking in college: the influences of person, social group, and environmental. Journal of Adolescent Health, 32, 26–35.
Wellman, R. J., Contreras, G. A., Dugas, E. N., O’Loughlin, E. K., &
O’Loughlin, J. L. (2014). Determinants of sustained binge drinking
in young adults. Alcoholism: Clinical and Experimental Research,
38, 1409–1415.
White, H. R., Marmorstein, N. R., Crews, F. T., Bates, M. E., Mun, E.-Y., &
Loeber, R. (2011). Associations between heavy episodic drinking and
changes in impulsive behavior among adolescent boys. Alcoholism:
Clinical and Experimental Research, 35, 295–303.
Xing, Y., Ji, C., & Zhang, L. (2006). Relationship of binge drinking and
other health-compromising behaviors among urban adolescents in
China. Journal of Adolescent Health, 39, 495–500.
Zwaluw, C. S., Kleinjan, M., Lemmers, L., Spijkerman, R., & Engels,
R. C. M. E. (2013). Longitudinal associations between attitudes towards
binge drinking and alcohol free-drinks, and binge drinking behaviors in
adolescents. Addictive Behaviors, 38, 2110–2114.