Obat dan Alkohol Ketergantungan 145 (2014) 69-76

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Obat dan Alkohol Ketergantungan

j ourna lho saya pa ge: www.el Sevier. com / cari / drugal CDEP

Ulasan

Asosiasi kegelisahan gangguan dengan risiko perilaku merokok: A meta-analisis bakal studi
observasional

Kipas Jiang, suyun Li, Lulu Pan, Nan Zhang, Chongqi Jia *
Departemen Epidemiologi dan Biostatistik, Shandong University, Jinan 250.012, Shandong, PR China

articleinfo abstrak

Artikel sejarah: Objektif: artikel yang dipublikasikan melaporkan hasil kontroversial tentang hubungan gangguan kecemasan dengan risiko perilaku merokok.
Menerima Juli 2014 9 diterima di direvisi bentuk 13 Oktober Sebuah meta-analisis dilakukan untuk menilai hubungan antara gangguan kecemasan dan perilaku merokok.
2014 Diterima 21 Oktober 2014 Tersedia online 4 November
2014
metode: Sebuah pencarian yang komprehensif dilakukan untuk mengidentifikasi studi observasional prospektif (dari Januari 1990 sampai Maret, 2014)
dari asosiasi tersebut. Itu Q tes dan saya 2 statistik yang digunakan untuk menguji antara-studi heterogenitas. Tetap atau acak effect model dipilih
berdasarkan uji heterogenitas antara studi. Meta-regresi dan “cuti satu dari” analisis sensitif digunakan untuk mengeksplorasi potensi sumber
Kata kunci:
antara-studi heterogenitas. bias publikasi diperkirakan menggunakan uji asimetri regresi Egger ini.
Kecemasan Merokok Nikotin ketergantungan
Meta-analisis

hasil: Fifteen articles were included. After excluding studies that were the key contributors to betweenstudy heterogeneity, the meta-analysis
showed a significant association of anxiety disorders with increased risk of regular smoking (OR = 1.41, 95% CI: 1.23–1.62) and nicotine
dependence (OR = 1.58, 95% CI: 1.45–1.73). No significant influence and publication bias were observed both before and after excluding the
key contributors to heterogeneity.

Conclusion: This meta-analysis suggested that anxiety disorders had significant positive effect on the risk of smoking behaviors. This
association needs to be confirmed by further studies.
© 2014 Elsevier Ireland Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
2. M
Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
21 S
22
23 D m
24 S
3 R 71
31 S
32 Quan a e n he o e a on h p be ween AD and mo ng beha o 71
33 Sou e o he e ogene and en ana 71
34
4 D 71
R C
m R

Em @ C

© E A
70 F. Jiang et al. / Drug and Alcohol Dependence 145 (2014) 69–76

1. Introduction 95% CI: 1.10–4.42), but this association was no longer significant after controlling for the major
depressive disorder. When further extending this investigation to assess the relationship between
Tobacco use remains a main cause of preventable diseases and deaths all over the world. It kills post-traumatic stress disorder (PTSD) and nicotine dependence (ND) ( Breslau et al., 2003 ), it
indicated that compared with those without PTSD, persons with PTSD had an 83% increased
nearly 6 million people and results in enormous economical burden each year, worldwide ( World Health Organization,
2011 ). Thus, the world is facing a public health crisis with current smoking status and it is urgent to take multivariate adjusted risk of ND. Other data also demonstrated the positive association of ADs with
measures for tobacco control intervention. smoking behaviors ( Koenen et al., 2005; Swendsen et al., 2010 ). However, no or negative relation of
ADs to smoking behaviors was also reported by some articles ( Cisler et al., 2011; Isensee et al.,
2003; Johnson and Novak, 2009 ). Therefore, the effect of ADs as a risk factor on smoking behaviors
Previous publications identified increased rates of cigarette smoking among individuals with mental is still controversial. Exploring the exact effect of ADs on smoking behaviors may contribute to
disorders, and increased rates of mental disorders among smokers ( Lawrence et al., 2009 ). Anxiety disorders
tobacco control intervention in the future. Prospective studies should provide better evidence than
(ADs) represent the most common mental disorders in many countries ( Kessler et al., 2005; McEvoy et case–control studies, since they may avoid some bias such as the recall bias. Thus, we conducted a
al., 2011 ), which damage an individual’s health and quality of life ( Mendlowicz and Stein, 2000 ). Numerous meta-analysis for prospective observational studies to: (1) assess the association of ADs with the risk
investigations showed that ADs were associated with smoking behaviors; individuals with ADs had higher of smoking behaviors; (2) evaluate the potential heterogeneity among studies; and (3) explore the
risk of smoking than those without ADs ( Koenen et al., 2005; Swendsen et al., 2010 ). However, smokers potential publication bias.
had a higher risk of ADs than non-smokers ( Grover et al., 2012; Mondin et al., 2013; Richardson et al.,
2012 ). Based on the data from the Oregon Adolescent Depression Project, Goodwin et al. (2005) found
that both before (OR = 5.1, 95% CI: 2.4–10.5) and after (OR = 4.2, 95% CI: 2.0–8.9) adjusting for related confounders,
daily smoking compared with non-daily smoking increased significantly the risk of panic disorder (PD).
By using the New York Adolescent Cohort, Johnson et al. (2000) also found that after adjusting for related confounders,
adult smokers with equal to and more than 1 pack per day at baseline had significant higher risk of ADs
(OR = 10.78, 95% CI: 1.48–78.55), PD (OR = 15.58, 95% CI: 2.31–105.14) and generalized anxiety
disorder (GAD) (OR = 5.53, 95% CI: 1.84–16.66), respectively. In addition, some other studies also consistently
support the relationship between smoking behaviors and ADs ( Grover et al., 2012; Mondin et al., 2013 ).
Since no significant relationship between ADs and regular smoking have been established using prospective
2. Methods
observational data ( Brown et al., 1996 ), several epidemiological studies have been conducted to assess
this association. The research ( Breslau and Klein, 1999 ) utilized a sample of young adults aged 21 to 30
2.1. Search strategy
years, drawn from the Detroit Epidemiological Study and showed that persons with PD had higher risk of
daily smoking (OR = 2.20,
A comprehensive search, restricted to human studies in English and Chinese language papers
was performed using the following databases (PubMed; ISI Web of Science; EMBASE; China
National Knowledge Infrastructure; China Biology Medical literature database; Database of Chinese
Scientific and Technical Periodicals) and the search terms (“anxiety” or “mental disorders” or
“posttraumatic stress” or “panic” or “social phobia” or “agoraphobia” or “specific phobia” or
“psychiatric” or “obsessivecompulsive” and “cigarette” or “nicotine dependence” or “tobacco” or
“smoking”) in various combinations for relevant articles published between January, 1990 and March, 2014.
( Fig. 1 shows details of the search process and study selection). In addition, we searched and
identified studies not captured by our database through reviewing reference lists in retrieved articles.

2.2. Inclusion criteria

The inclusion criteria were as follows: (1) prospective observational studies including prospective
studies or quasi-prospective studies (studies having utilized a single time point analysis and
retrospective data reported by individuals themselves with preexisting ADs) were included; (2) the
exposures of interest were one or more types of ADs defined according to DSM-III-R ( American
Psychiatric Association, 1987 ) or DSM-IV ( American Psychiatric Association, 1994 ) or ICD-10 ( World
Health Organization, 1993 ); (3) the outcomes of interest were smoking behaviors including regular
smoking (daily smoking or smoke more than three times per week) and ND assessed using DSM-III-R
( American Psychiatric Association, 1987 ) or DSM-IV ( American Psychiatric Association, 1994 ) or The
Fagerstrom test for nicotine dependence (FTND;

Heatherton et al., 1991 ) in the articles. (4) The multivariateadjusted odds ratio (OR) or hazard ratio
(HR) with 95% confidence interval (CI) was examined.

Each identified study was independently reviewed by two investigators (Jiang and Zhang) to
determine whether an individual study was eligible for inclusion in this meta-analysis. If there was
disagreement between the two investigators about eligibility of the article, it was resolved by
consensus with a third reviewer (Li).
Fig. 1. Flow chart of study selection.
 F. Jiang et al. / Drug and Alcohol Dependence 145 (2014) 69–76 71

2.3. Data extraction and quality assessment
The following data were extracted from each study: the first author’s name, published year,
ethnicity, sample size, type of study, participant age at baseline, duration of follow-up, diagnosis
criteria of ADs and ND, definition of regular smoking, adjustment for potential confounding factors as
well as multivariate adjusted OR (HR) and 95% CI for risk of regular smoking or ND. For studies ( Breslau
et al., 2004; Chou et al., 2011; Isensee et al., 2003 ) that provided ORs s for different types of anxiety, we
used meta-analysis to incorporate these values into one combined OR that presents the association of
ADs with risk of regular smoking or ND. The study quality was assessed using the 9-star Newcastle–Ottawa
scale ( Wells et al., 2000 ). Data extraction and quality assessment were performed by two reviewers
(Jiang and Pan).
on ND, respectively. Stars in Tables 1 and 2 indicate the quality of study assessed using the Newcastle
Ottawa scale. Of the ten studies in Table 1 , five were scored 7 stars and five scored 6 stars. Of the
nine studies in Table 2 , six were scored 7 stars and three scored 6 stars. The ORs extracted from the
articles were for the adjusted effect sizes of the exposures. Other characteristics such as baseline age
of participants, type of study, sample size, diagnostic criteria of ADs and ND, and definition of regular
smoking are also presented in Tables 1 and 2 .
3.2. Quantitative synthesis for relationship between ADs and smoking behaviors

Risk of regular smoking: Ten articles with ten studies including

41,801 subjects were included in the analysis on the association of ADs with risk of regular smoking.
An REM was used because substantial significant between-study heterogeneity was observed ( P Q < 0.001;
I 2 = 75.9%). Pooled result showed that ADs significantly increased the risk of regular smoking (OR = 1.40,
2.4. Statistical analysis
95% CI: 1.10–1.78) ( Fig. 2 ).

Pooled measure was calculated as the inverse varianceweighted mean of the logarithm of OR (HR)
with 95% CI to assess the strength of association between anxiety disorders and risk of regular smoking
Risk of ND: Nine articles with nine studies including 23,530 subjects were included in the analysis
or ND. Heterogeneity among studies was assessed using the Q test and the I 2 statistic that describes the
on the association of ADs with risk of ND. A FEM was used, because no significant between-study
proportion of total variation attributable to between-study heterogeneity as opposed to random error or
heterogeneity was observed ( P Q = 0.152, I 2 = 33.3%). Pooled result showed that ADs were significantly
chance ( Higgins and Thompson, 2002 ). In the presence of substantial heterogeneity ( I 2 > 50%; Higgins
associated with increased risk of ND (OR = 1.58, 95% CI: 1.44–1.73; Fig. 3 ).
et al., 2003 ), the DerSimonian and Laird random effect model (REM) was applied as the pooling
method; otherwise, the fixed effect model (FEM) was adopted. Meta-regression with restricted maximum likelihood
estimation was performed to assess the potentially important covariates exerting substantial impact on between-study
heterogeneity. The “leave one out” sensitivity analysis ( Patsopoulos et al., 2008 ) was conducted using I
3.3. Sources of heterogeneity and sensitivity analysis
2> 50% as the criterion to assess the key studies with substantial impact on between-study heterogeneity.
An analysis of influence was conducted ( Tobias, 1999 ), which describes how robust the pooled
The between-study heterogeneity was found among studies on regular smoking but not on ND.
estimator is to removal of individual studies. An individual study is suspected of excessive influence if the
The univariate meta-regression, with the covariates of published year, ethnicity (categorized as
point estimate of its omitted analysis lies outside the 95% CI s of the combined analysis. Publication bias
American, European and Oceanian), type of study (categorized as prospective data and
was estimated using Egger’s regression asymmetry test ( Egger et al., 1997 ). All statistical analyses
quasi-prospective data), diagnosis criteria of ADs (categorized as DSM-III-R, DSM-IV, ICD-10) and
were performed with STATA/SE version 13.1 (Stata Corporation, College Station, TX, USA). All p- values
ND (categorized as DSM-III-R, DSM-IV, FTND), sample size and quality, showed that no
were two-sided, and that less than 0.05 was considered statistically significant.
aforementioned covariates had a significant impact on between-study heterogeneity.

In the sensitivity analysis, two studies conducted by Koenen et al. (2006) and Johnson and Novak
(2009) were found to be the key contributors to between-study heterogeneity. After excluding these
two studies, the meta-analysis also showed a significant association of ADs with increased risk of
regular smoking (OR = 1.41, 95% CI: 1.23–1.62).

3.4. Influence and publication bias analyses

3. Results
3.1. Study characteristic
The study identified and selected procedures are summarized in Fig. 1 . Fifteen articles were finally
included in our analysis. Among them, ten articles with ten studies (eight in America, one in Europe and
one in Oceania; Breslau and Klein, 1999; Breslau et al., 2004; Brown et al., 1996; Cisler et al., 2011;
Goodwin et al., 2005; Isensee et al., 2003; Johnson and Novak, 2009; Koenen et al., 2006; McKenzie
et al., 2010; Swendsen et al., 2010 ) were included in the analysis on the association of ADs with risk of
regular smoking. Nine articles with nine studies (six in America, one in Europe and two in Oceania; Breslau
et al., 2003, 2004; Chou et al., 2011; Goodwin et al., 2004; Griesler et al., 2011; Isensee et al., 2003;
Koenen et al., 2005; McKenzie et al., 2010; Swendsen et al., 2010 ) were in the analysis on the association morbidity. Three non-mutually exclusive models were proposed for the relationship between ADs and
of ADs with risk of ND. General characteristics in the published articles included in this meta-analysis are
shown in
Both before and after excluding the two studies as the key contributors to between-study
heterogeneity, no individual study was found to have excessive influence on the pooled effect and no
significant publication bias was detected for studies on regular smoking. For studies on ND, there
were also no significant influence and publication bias observed in this analysis.
4. Discussion
A solid body of evidence proved that both ADs and cigarette smoking are contributors to human
smoking ( Moylan et al., 2012 ). First, smoking may lead to increased risk of anxiety; second, anxiety
may increase smoking rates; third, smoking and anxiety rates may both be influenced by shared
vulnerability factors. However, significant variability exists within the results of current epidemiological
literatures about the relationship between ADs and smoking. For these inconsistent results of previous
publications, one of the mentioned reasons is

Tables 1 and 2 . Ranges of follow-up period were from 1 to 11 years for studies on regular smoking and
from 2 to 21 years for studies
 Prospective Prospective ProspectiveProspective Quasi- ProspectiveQuasi- ProspectiveProspective Prospective Type

of study

prospective prospective

12–17 15–24 14.9 ≥ 18 36–55 15–19 15–54 14–24 21–30 14–18 Age

at baseline

2.5 10 11 3 NA 7 NA 4 5 1 Follow

up (year)

DSM-IV(PTSD) DSM-IV(ADs) ICD-10(ADs)

DSM-IV(ADs) DSM-III-R(PTSD) DSM-IV(PD)
DSM-III-R(ADs)
DSM-IV(ADs)
DSM-III-R(PD) DSM-III-R(ADs)
ADs (diagnosis)
(stars)

Self Self Self Self Self Self Self Self Self Self Regular smoking

report: daily

smokers vs report: every

report: daily smoking report:
never or less than dailydaily smoking
smokers
report:
day/3–6 times per

report: smoked daily ≥report:

1 month
smoked daily ≥ 1 month
week vs 1–2 times a week/not at all
report: daily smoking >4 weeks smoking ≥ 3 vs <3 episodes per week
report: daily smoking ≥ 1 month report: daily smoking ≥ 1 month

1.90 1.90 1.33 0.62 2.36 1.70 1.45 1.01 1.00 1.34 OR

0.93 1.30 0.86 0.39 1.86 0.90 1.30 0.73 0.40 0.64 UL

3.87 2.80 2.05 0.99 2.98 3.30 1.62 1.38 2.48 2.81 LL

Baseline Age, Sex Demographics Demographic Demographics,

Race, Age and gender
Gender Age, Adjustment factors
other mental
and disorders, parental
gender, race, gender, race,
anxiety disorders
and adolescent military service factors
and cigarette
smoking education, marital number of
smoking and the
and SES status
interaction
status, number of biological parents,
alcohol and cannabis use

children, region, parental education, other disorders

behaviors and other predictors
sex, education and age
urbanicity, and employment status and major depressive disorder

7 7 7 7 6 7 6 6 6 6 Quality
 15–24 36–55 15–54 21–3014–24 Age
≥ 60
16.1 14.9 <1

at baseline

2 3 11 10 NA 21 NA 10 4 Follow up (year)

(stars)

DSM-IV(ADs) DSM-IV(ADs) ICD-10(ADs) DSM-IV(ADs) DSM-III-R(PTSD) DSM-IV(ADs)

DSM-III-R(ADs)
DSM-III-R(PTSD)
DSM-IV(ADs)Ads (diagnosis)

DSM-IV DSM-IV FTND DSM-IV DSM-III-R DSM-IV DSM-III-R DSM-III-R

DSM-IV ND

1.68 1.01 2.18 1.50 1.36 1.46 1.81 1.83 1.47 OR

1.12 0.62 1.36 1.10 1.14 0.93 1.58 1.04 1.00 UL

2.52 1.63 3.49 2.00 1.61 2.29 2.12 3.22 2.15 LL

Comorbidity Demographic Sex, Age, maternal/paternal Zygosity, Bad influence

Race, Gender,
Age and gender
Adjustment factors
depression
(alcohol, drug, minority race, father
among disorders characteristics and problems with (mother)did not
gender, race, the law) from family, sexual and
graduate from high
and other and other psychiatric
adolescent
school, physical abuse,
education, marital
disorders race and education
covariates
alcohol, drug, mental illness,
status, number of
alcohol and cannibas use
gender and others sex, education, age
children, region,

urbanicity, and employment status

6 7 7 7 6 7 6 7 7 Quality
74 F. Jiang et al. / Drug and Alcohol Dependence 145 (2014) 69–76

Fig. 2. Forest plot of ORs for the association of anxiety disorders with risk of regular smoking. White diamond denotes the pooled OR. Black squares indicate the OR in each study, with square sizes inversely proportional to the standard error of the
OR. Horizontal lines represent 95% CI.

the study design ( Moylan et al., 2012 ). Theoretically, prospective study is the better one among epidemiological
the reported articles precluded a more robust assessment of sources of this heterogeneity.
researches, because it could provide the clear direction of causality and avoid some biases, such as recall
bias. The under power for each individual study with relatively small sample size should also be worthy
of note. The meta-analysis could be the appropriate approach to copy with the later reason and to obtain
a more definitive conclusion about the cause-disease association
In this paper, we have chosen to focus on the association of ADs with smoking behaviors and used
the meta-analysis to incorporate the prospective observational data. Our analysis showed that ADs
could increase risks of both regular smoking and ND.
In this meta-analysis, the between-study heterogeneity was found among studies on regular smoking
based on the tentative categorization of I 2 values ( Higgins et al., 2003 ). An indeterminate number of characteristics
that vary among studies could be the sources of between-study heterogeneity, e.g., publication year,
ethnicity, type of study, diagnosis criteria of ADs and ND, sample size and quality, etc. Therefore, we
utilized meta-regression and “leave one out” sensitivity analysis ( Patsopoulos et al., 2008 ) to aim to reduce Johnson et al. (2000) , most participants of this study had higher socioeconomic status such as
between-study heterogeneity and explore the potential important causes of between-study heterogeneity
for both covariates and studies. Our meta-analysis did not identify any of the aforementioned covariates
as being an important contributor to between-study heterogeneity. ADs have a complex etiology
generated by the combined effects of biopsychosocial factors. Although the aforementioned covariates
were not found to be important sources of disease–effect heterogeneity across the studies in this
meta-analysis, other variables, as well as their possible interaction, may well be potential contributors to
this disease–effect unconformity. In this respect, the lack of relevant study-level covariates in
In the “leave one out” sensitivity analysis, two studies ( Johnson and Novak, 2009; Koenen et al.,
2006 ) on regular smoking were identified as being key contributors to between-study heterogeneity.
The heterogeneity caused by Koenen et al.’s study might lie in the special study population drawn
from the Vietnam Era Twin (VET) Registry. The VET Registry consisted of male-male twin pairs that
both siblings served on active military duty during the Vietnam War era. Individuals who participated in
the war might suffer from greater stress than the general population, so they were more likely to use
tobacco to reduce their stress ( Harte et al., 2014 ). In addition, tobacco use had been substantially
more common among males than among females ( Shopland et al., 1992 ). Thus, this study revealed
the stronger positive association of ADs with regular smoking than other studies. As for the study
conducted by
educational level, higher household income and better occupation. Data indicated that persons with
higher socioeconomic status had lower risk of smoking prevalence ( Barbeau et al., 2004 ). In addition,
this study controlled more other confounders such as abuse or dependence for alcohol, marijuana,
cocaine, heroin, and other drugs that other studies did not. Thus, we speculate that those may be the
reasons for its different result from other studies, which resulted in as one contributor to betweenstudy
heterogeneity. However, after excluding the two articles as the key contributors to between-study
heterogeneity, our metaanalysis also indicated that ADs were significantly associated with increased
regular smoking risk.

The interrelationship between anxiety disorders and tobacco use is quite complicated; this may
include genetic, biochemical,
 F. Jiang et al. / Drug and Alcohol Dependence 145 (2014) 69–76 75

Fig. 3. Forest plot of ORs for the association of anxiety disorders with risk of nicotine dependence. White diamond denotes the pooled OR. Black squares indicate the OR in each study, with square sizes inversely proportional to the standard error of
the OR. Horizontal lines represent 95% CI.

psychological, interpersonal, and environmental vulnerability factors. Morissette et al. (2007) had one extraction and quality assessment. Jiang did the data analyses and drafted the manuscript. Jia is
review article from the psychological perspective (including conditioning theory, cognitive theory, anxiety sensitivity,
responsible for the whole work. All authors have read and approved of the final version of the
and stress and coping models) to explain in detail the association of anxiety disorders with smoking behaviors.
manuscript.
Other reviews also focused on this issue ( Ameringer and Leventhal, 2010; Zvolensky et al., 2005 ).
Readers interested in these could consult those reviews.

Conflict of interest statement

The authors declare that there are no conflicts of interest associated with this manuscript.
In this meta-analysis, although we could not find any significant publication bias both for regular
smoking and ND studies, it is worthy of caution that this may be due to the small number of studies
with under power in those meta-analysis. Evidence demonstrated that ten or fewer studies would have
low power of detection for publication bias (small-study effects; Sterne et al., 2000 ). In conclusion, this meta-analysis
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