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Obesity
Volume 24, Issue 9 p. 1834-1841
Review
Free Access


THE EFFECT OF TOBACCO CESSATION ON WEIGHT GAIN, OBESITY, AND DIABETES RISK


Terry Bush, 

Corresponding Author

Terry Bush

Alere Wellbeing, Inc., Seattle, Washington, USA

Correspondence: Terry Bush (terry.bush@optum.com)Search for more papers by this
author
Jennifer C. Lovejoy, 

Jennifer C. Lovejoy

Arivale, Inc, Seattle, Washington, USA.

Search for more papers by this author
Mona Deprey, 

Mona Deprey

Alere Wellbeing, Inc., Seattle, Washington, USA

Search for more papers by this author
Kelly M. Carpenter, 

Kelly M. Carpenter

Alere Wellbeing, Inc., Seattle, Washington, USA

Search for more papers by this author
Terry Bush, 

Corresponding Author

Terry Bush

Alere Wellbeing, Inc., Seattle, Washington, USA

Correspondence: Terry Bush (terry.bush@optum.com)Search for more papers by this
author
Jennifer C. Lovejoy, 

Jennifer C. Lovejoy

Arivale, Inc, Seattle, Washington, USA.

Search for more papers by this author
Mona Deprey, 

Mona Deprey

Alere Wellbeing, Inc., Seattle, Washington, USA

Search for more papers by this author
Kelly M. Carpenter, 

Kelly M. Carpenter

Alere Wellbeing, Inc., Seattle, Washington, USA

Search for more papers by this author
First published: 29 August 2016
https://doi.org/10.1002/oby.21582
Citations: 135

Funding agencies: Investigators' time was supported by Grant RO1DA031147 from
the National Institute on Drug Abuse and Grant R21AT007845 from the National
Center for Complementary and Integrative Health, as well as Alere Wellbeing and
Arivale, Inc.

Disclosure: The authors declared no conflict of interest.

Author contribution: All authors contributed to conceptualizing the review
paper, the literature reviews, and writing and editing the paper.

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ABSTRACT


OBJECTIVE

Most smokers gain weight after quitting, and some develop new onset obesity and
type 2 diabetes. The purpose of this paper is to synthesize the current science
investigating the consequences of tobacco cessation on body weight and diabetes,
as well as intervention strategies that minimize or prevent weight gain while
still allowing for successful tobacco cessation.


METHODS

Systematic reviews and relevant studies that were published since prior reviews
were selected.


RESULTS

Smoking cessation can cause excessive weight gain in some individuals and can be
associated with clinically significant outcomes such as diabetes or obesity
onset. Interventions that combine smoking cessation and weight control can be
effective for improving cessation and minimizing weight gain but need to be
tested in specific populations.


CONCLUSIONS

Despite the health benefits of quitting tobacco, post-cessation weight gain and
new onset obesity and diabetes are a significant concern. Promising
interventions may need to be more widely applied to reduce the consequences of
both obesity and tobacco use.




INTRODUCTION

Tobacco use continues to be a major public health problem and the leading
preventable cause of death. Unfortunately, most smokers will gain weight after
quitting, and a significant minority of smokers will gain an excess amount which
may increase their risk for diabetes onset. This article presents a narrative
review of the prevalence and impact of cessation-related weight gain on obesity
and diabetes and a summary of cessation interventions aimed at addressing
post-cessation weight gain. We primarily used PubMed to search for English
language articles describing the effects of tobacco cessation on weight,
diabetes, and glucose control as well as studies examining mechanisms for those
changes. We also searched for systematic reviews and meta-analyses of
interventions for improving smoking cessation and mitigating weight gain in
those quitting tobacco as well as recent articles or those not included in
reviews or meta-analyses. The purpose of this review was to summarize the
literature and provide recommendations for clinicians treating smokers with
overweight or obesity.


PREVALENCE AND IMPACT OF OBESITY AND TOBACCO USE

Smoking and obesity are the two leading causes of death in the U.S. (1-5). Two
thirds of adults in the U.S. have overweight or obesity, and approximately 9
million adults with obesity are smokers (6-8). Among adults screened for weight
loss surgery, two thirds reported a history of smoking, and 27% were smoking at
the time of a presurgical evaluation (9). Similarly, among treatment seeking
smokers, two thirds had overweight or obesity (10-13). Both obesity and smoking
increase the risk for type 2 diabetes, hypertension, and cardiopulmonary
disease. Like smoking, obesity increases diabetes risk by increasing insulin
resistance and decreasing glucose control (14). Most importantly, co-occurrence
of obesity and smoking increases the mortality risk above and beyond either risk
factor alone (15, 16). Furthermore, it has been estimated that people with
obesity cost an average of $1,360 in additional health care expenses each year
compared with the nonobese and that smokers require an average of $1,046 in
additional health care expenses compared with nonsmokers. These estimates do not
include the added costs to society due to absenteeism and loss of productivity
(16, 17).


PREVALENCE AND IMPACT OF WEIGHT GAIN IN SMOKERS

Research has shown that while the majority of people who quit smoking gain
weight, there is considerable variability in the amount of weight gain. The
differences in weight gain between those who quit and those who continue to
smoke range from 2.6 to 5.3 kg (3, 10, 18-24). Using data from 35
population-based prospective cohort studies worldwide and comparing 63,403
smokers who had quit smoking with 388,432 who continued to smoke, Tian et al.
found that people who quit smoking gained an average of 4.1 kg over 5 years,
compared with 1.5 kg for continuing smokers, a difference of 2.6 kg (19). The
authors noted that studies with longer follow-up time and that were conducted in
North America found higher levels of weight gain. An earlier meta-analysis by
Aubin et al. focused on weight gain in those who quit smoking as part of
randomized clinical trials of cessation treatment, including pharmacotherapy,
exercise, and weight gain prevention studies. They reported that the average
weight gain among successful quitters was 1.1 kg at 1 month, 2.3 kg at 2 months,
2.9 kg at 3 months, 4.2 kg at 6 months, and 4.7 kg at 12 months. They noted
substantial variation among smokers with 16% to 21% losing weight and 13% to 14%
gaining more than 10 kg at 12 months (23). Scherr et al. also reported large
variability in weight change at 12 and 24 months among smokers who had
successfully quit and that 10% gained more than 10 kg (25). In another study,
the change in weight among quitters was higher than in previous studies. Over 8
years, successful quitters gained an average of 8.79 kg (SD = 6.36) while
continuing smokers gained 2.24 kg (SD = 6.65), a difference of 6.55 kg (22).
Importantly, for a small number of people, the amount of weight gain after
tobacco cessation is significant enough to move them into an overweight or
obesity categorization (body mass index, BMI >25 mg/m2 or >30 mg/m2) which could
have a significant impact on health. One study reported an increased prevalence
of overweight of 15% and an increased prevalence of obesity of 18% in recent
quitters, whereas in continued smokers prevalence rates increased by 2% and 5%,
respectively (22). According to a meta-analysis of cohort studies, a 2.5 kg/m2
increase in BMI for those with a starting BMI of 22 kg/m2 or higher increased
mortality by 14%, but continued smoking far exceeded this mortality rate (26).
In addition to increased weight, cessation can also result in an increase in
waist circumference or central fat, which could attenuate some of the beneficial
effects of smoking cessation, especially among quitters who reduced their
physical activity and those who had been heavy smokers (27).

It is unclear which smokers are most at risk for the larger weight gain after
quitting. While one study among smokers seeking cessation treatment reported no
correlation between baseline BMI and smoking cessation or cessation-related
weight gain (24), the bulk of studies have reported higher weight gain in those
with higher BMI before quitting (18, 19, 22, 25, 28, 29). For example, for a
starting BMI of 18, 23, 29, or 36 kg/m2, Lycett et al. found that post-cessation
weight gain was 9.8, 7.8, 10.2, and 19.4 kg, respectively, after 8 years (22).
Others at the greatest risk of gaining higher amounts of weight or triggering a
chronic condition after quitting include women, especially African American
women (30, 31), those with lower socioeconomic status (29), and those with poor
diet, limited physical activity, and greater amount of tobacco used (31-36). A
recent study looking at 10-year outcomes and comparing those who quit tobacco
with those who continued to smoke found that degree of tobacco addiction (i.e.,
number of cigarettes per day) was the primary predictor of excessive weight gain
(18). Overall, about 10% of men and 13% of women gain 10 kg or greater after
quitting (19, 29, 31, 32, 35, 37-39). Other groups that are at increased risk
for weight gain after cessation include those with disordered eating patterns.
For example, among overweight former smokers, those who reported regular binge
eating were more likely to gain weight in the year following smoking cessation
than overweight former smokers who were not binge eaters (40).


WHY PEOPLE GAIN WEIGHT WHEN QUITTING

Weight gain associated with quitting tobacco is largely due to increased energy
intake and reduced energy expenditure. Smokers gain weight after they quit
smoking primarily because of the removal of nicotine's effects on the central
nervous system (35, 36, 41, 42). Some smokers also attempt to cope with nicotine
withdrawal by substituting eating for the “hand to mouth” behavior of smoking
which can lead to an increase in caloric intake (35, 43, 44). However, there are
differences in opinion with regard to the relative impact of nicotine-related
metabolism changes and increased caloric intake. Kleppinger et al. found in a
study of women that neither calorie intake nor physical activity level changes
differed significantly between those who quit and those who continued smoking
(45). However, percentage of calories as sugar was increased which, over time,
might lead to increased caloric intake and weight gain. Low satiety, emotional
eating, calorie misperception, and short sleep might also contribute to
post-cessation weight gain (46). Regardless of weight change, those who stop
smoking report an increased preference for sweet tasting foods (44). According
to a recent study, women who smoke had lower ability to perceive fat and
sweetness in foods and derived less pleasure from foods, which could lead to
overconsumption (47). It has also been suggested that the sudden drop in blood
sugar in many people during the first 3 days of quitting could lead to common
withdrawal symptoms such as headaches, dizziness, and craving for sweets which
in turn could lead to overeating in an attempt to cope with these symptoms (35,
41, 43). Research on the neurobiology of nicotine addiction and withdrawal sheds
some light on the problem of post-cessation weight gain. Specifically, the
relationship between nicotine addiction and the neural reward mechanisms
involved could mirror similar neural networks involved in some eating behaviors.
In fact, food addiction appears to activate similar reward pathways in the brain
as does smoking (48). Elevated response to reward has been linked to weight gain
perhaps due to an increase in caloric intake or altered food composition (e.g.,
more sugar which can then increase the glycemic load of the diet) (49). In one
study, Stice et al. compared reward surfeit versus reward deficit treatment
models and suggested that gradual, healthy changes to dietary intake instead of
dramatic weight loss diets may be better at minimizing the sense of deprivation
or loss (50). This notion of deprivation (biological and psychological) could
explain why strict dieting during an attempt to quit smoking can have a negative
impact on cessation (51). Food deprivation can reduce extracellular dopamine
levels, reduce positive mood, and increase drive to use nicotine (51).


CONSEQUENCES OF SMOKING AND SMOKING CESSATION ON DIABETES

Systematic reviews and the recent Surgeon General's Report have confirmed that
active smoking is associated with an increased risk of type 2 diabetes (52-55).
Smokers are 30% to 44% more likely to develop type 2 diabetes than nonsmokers
(52) and the more cigarettes consumed, the higher the risk (52, 53, 55, 56).
Multiple biological mechanisms for the causal connection between smoking and
development of type 2 diabetes have been postulated, including the effects of
smoking on cortisol concentrations, central obesity, inflammatory markers,
oxidative stress, insulin resistance, and an increase in fasting blood glucose
(55, 57-59). Smoking is particularly problematic in people who already have
diabetes. People with diabetes who smoke have higher glycated hemoglobin (HbA1c)
levels than nonsmokers who have diabetes (60), and they are more likely to
experience severe hypoglycemia and to have trouble with insulin dosing and
diabetes control (5, 61). Some of these consequences of smoking improve after
cessation, including improved insulin sensitivity and glycemic control (53,
57-59, 61-63). Paradoxically, however, in some cases, quitting tobacco seems to
worsen glycemic control and increase the risk for new onset type 2 diabetes
(64-67). A recent review reported that the relative risk of developing type 2
diabetes compared with never smokers was 1.54 (95% CI 1.36-1.74) for those who
quit in the past 5 years; 1.18 (95% CI 1.07-1.29) for those abstaining for 5 to
9 years; and 1.11 (95% CI 1.02-1.20) for long-term quitters (≥10 years) (67).
The mechanism by which tobacco cessation leads to diabetes onset or poorer
diabetes control is not clear. The increased risk may be due to increases in
visceral fat accumulation or waist circumference, chronic inflammation, or
excessive weight gain after quitting (56, 68, 69). An early study with Japanese
men with diabetes reported that quitting smoking for at least 6 months was
associated with weight gain along with significant worsening of blood pressure,
total cholesterol, triglycerides, and fasting blood glucose (70). In contrast,
according to a study by Lycett et al., glycemic control in patients with
diabetes deteriorated for about 3 years after quitting smoking after which HbA1c
levels were similar to smokers, and this association was independent of
post-cessation weight gain (65). It has been suggested that the adverse effect
of quitting tobacco on glycemic control may be due to greater consumption of
sugary foods and carbohydrates (44, 71, 72). However, Komiyama et al. reported
no significant change in HbA1c after successful cessation from baseline to 12
weeks in a sample of 132 men and 54 women, despite significant increases in BMI,
LDL-C and HDL-C, and triglycerides (173 ± 105 mg/dL before vs. 199 ± 129 mg/dL)
after cessation (35).

In summary, it is apparent that tobacco cessation, while certainly an important
health behavior change, can also lead to negative metabolic consequences for
some smokers. Regardless of the reported negative effects of cessation on
glycemic control and diabetes risk, quitting smoking has been proven to reduce
the risk of cardiovascular disease and mortality even in people with diabetes
(57, 73, 74). It is increasingly important to develop and test tobacco cessation
interventions for those at risk of negative health consequences of cessation and
to determine who might benefit from these interventions.


TOBACCO CESSATION INTERVENTIONS TO PREVENT POST-CESSATION WEIGHT GAIN:
SYSTEMATIC REVIEWS AND META-ANALYSES

There are two problems with the weight gain that occurs with cessation. First,
concerns about weight gain can be a barrier to cessation attempts. Second, for a
significant minority of people the weight gain can be enough to trigger a
chronic illness like obesity or diabetes. Interventions have been developed that
address both the cognitive concern about weight gain before a quit attempt and
to minimize actual weight gain during and after cessation. It should be
emphasized that these two approaches are fundamentally very different: a “weight
concerns” approach is addressing beliefs about weight gain that could interfere
with quitting smoking and may even encourage tolerance of some weight gain,
whereas a weight loss/weight management intervention is actually trying to
prevent the weight gain that occurs with cessation. An early Cochrane review of
interventions to reduce weight gain among those quitting tobacco was published
in 2009 (75). Recommendations from this review indicated promise for
individualized weight management, nicotine replacement therapy (NRT), and
physical activity interventions when combined with cessation interventions. The
same year Spring et al. conducted a meta-analysis of 10 RCTs that tested
combined weight control and cessation interventions and found evidence of
short-term increased abstinence for smokers and decreased post-cessation weight
gain, but not in the long term (52 weeks). The review concluded that there was
no evidence of harm from addressing weight along with tobacco (76). In 2012,
Farley et al. updated the prior Cochrane review and added 5 studies for total of
16 studies reviewed (77). The results were similar to the prior 2009 reviews.
However, when adding a second article looking at addressing weight concerns
(78), the review concluded that there was no long-term weight suppressive effect
of the weight concerns intervention and there was a possibility for weight gain.
The review also concluded that interventions of weight education were not
effective at any time point and reduced tobacco abstinence at 12 months (77).
However, personalized weight management was associated with reduced weight gain
and had no negative effects on cessation at 12 months (79, 80). Weight
management with very-low-calorie meal replacement was effective at the end of
treatment, but not at 12 months, but it increased tobacco abstinence at 12
months (80, 81). Physical activity interventions designed to increase cessation
rates were also effective at reducing post-cessation weight gain at 12 months
(5), and use of cessation medications such as NRT and varenicline reduced
post-cessation weight gain in the short term but had no effects at 12 months.
These results highlight the difference between weight concerns interventions,
which strive to increase smoking cessation and not surprisingly are not
associated with weight suppression after quitting, and weight loss/weight
management interventions involving diet or targeted behavioral weight loss
approaches, which do reduce weight gain.

The most current systematic reviews (published in 2012) suggest that some
interventions added to tobacco cessation treatment may be safe and effective
such as very-low-calorie diets, physical activity, and NRT (77, 82). Below we
describe some of the key intervention strategies targeting tobacco cessation and
weight by categories, cognitive, behavioral (diet and exercise), and
pharmacologic, and we add relevant studies published since the 2012 reviews.


TOBACCO CESSATION AND WEIGHT MANAGEMENT COMBINED INTERVENTIONS—COGNITIVE AND
BEHAVIORAL APPROACHES

COGNITIVE APPROACHES TARGETING BODY IMAGE AND WEIGHT CONCERNS

Several studies have tested interventions that elicited smokers’ beliefs about
their weight and self-image and intervened on correcting unproductive thoughts
about weight gain (i.e., “weight concern”). The theory behind this line of
research was that excessive worry about weight gain interferes with ones’ effort
and commitment to quit smoking. A number of studies have found that addressing
weight concerns significantly improved smoking cessation compared with standard
cessation treatments alone (79, 80, 83, 84). Many of these weight concerns
studies also have shown a short-term weight suppressive effect of the
intervention as described in three systematic reviews (75-77). Since the weight
concerns intervention encouraged smokers not to worry about gaining weight but
to focus on the benefits of quitting, it is not surprising that one of the
trials showed a negative effect on post-cessation weight gain. The study
recruited women smokers concerned about gaining weight for a 2 × 2 randomized
trial offering standard cessation alone versus the weight concerns intervention
crossed with placebo or bupropion. Results showed that among women offered
bupropion to help with cessation, those randomized to the weight concerns
intervention had significantly greater levels of abstinence at 6 months than did
standard smoking cessation counseling combined with bupropion or placebo and a
nonsignificant increase in weight gain at 6 months with no effect on weight at
12 months (78). This study appeared in the recent Cochrane review (77) which
concluded that this second weight concerns study showed increased cessation at 6
but not 12 months and that the intervention significantly increased
post-cessation weight gain (77). A more recent trial of the weight concerns
intervention tested the effectiveness of this weight acceptance approach in a
population-based setting of a national tobacco “quitline” among 2,000 male and
female smokers seeking help to quit smoking (85). Results were published after
the three systematic reviews (75-77) and showed that at 6 months the
intervention had a weight suppressive effect without impacting cessation rates.
Among those who quit smoking, 50.8% of standard versus 30.0% of those in the
combined intervention gained weight (P = 0.0004), and the intervention group
gained significantly less weight (P = 0.01); the intervention group lost a
little weight overall and the standard group gained weight. Interestingly,
planned subgroup analyses revealed a significant interaction between treatment
group and having diabetes (P = 0.03), indicating that the weight concerns
intervention was particularly successful for those with diabetes (versus smokers
without diabetes). Among those with diabetes, 19.1% in standard versus 31.5% in
the intervention quit smoking (P = 0.03), and the average change in weight among
quitters was +6.8 lbs (+3.84 kg) for standard versus −5.2 lbs (−2.4 kg) for
intervention (P = 0.009). Among those without diabetes, 22.6% in standard versus
21.7% in the intervention quit smoking. The intervention also produced a
significant drop in weight concerns and this differential effect was a
significant factor in producing the outcomes. A weakness of this study is that
tobacco cessation and weight relied on self-report, a common approach in
phone-based interventions. In another study, Copeland et al. found that
individually tailored smoking cessation treatment for weight-concerned women was
superior to group counseling sessions for smoking abstinence, but not for change
in weight (37). The authors concluded that cognitive restructuring of attitudes
about smoking, appetite control, and weight management should be incorporated
into cessation counseling in addition to skills acquisition.

In summary, results from multiple trials suggest that addressing smokers'
concerns about their weight or body image during tobacco cessation counseling is
feasible, acceptable, and important to smokers and, for some, can reduce
post-cessation weight gain without harm to cessation efforts. However, in light
of the 2012 Cochrane review, weight gain during and after cessation needs to be
monitored and addressed. Moreover, the weight concerns quitline study needs to
be replicated and further tested in smokers at risk for diabetes or obesity.

EDUCATIONAL APPROACHES

Systematic reviews have found that education alone had no significant effects on
post-cessation weight gain but may reduce tobacco abstinence at 12 months
(75-77). However, one study not included in prior reviews found that nutritional
advice added to a smoking cessation program increased tobacco abstinence at 12
months but had no significant advantage over cessation treatment alone for
preventing post-cessation weight gain (86). The authors postulated that reducing
anxiety about weight gain and encouraging cessation despite weight gain was a
potential mechanism for why the offer of nutritional advice as part of a smoking
cessation program was successful in facilitating some sustained improvements in
dietary habits and improved quit rates at 12 months. Limitations of this study
include the small sample sizes and the study design. Overall, similar to weight
loss treatments in general, education or nutritional advice alone is not
recommended to prevent those quitting smoking from gaining weight (77).

CALORIE-RESTRICTION APPROACHES

Several studies have tested a combination of smoking cessation and traditional
calorie-restriction interventions using meal replacement or low-calorie diets
and had mixed results on cessation and weight gain. In an early study, Hall et
al. compared two different weight gain prevention treatments with 158 smokers
who completed a 2-week tobacco treatment program and found no effect on weight
outcomes. The two weight-based treatments, however, increased tobacco relapse
rates. The authors concluded that the treatment arms may have been too complex
and time-consuming which may have diverted focus and attention away from
maintaining tobacco abstinence (51). Subsequent studies and meta-analyses of
behavioral weight control and tobacco cessation have found that this was the
only negative trial (75-77). For example, one study involved a very-low-calorie
diet added to standard tobacco cessation treatment. The trial recruited only
women with weight concerns and involved 11 behavioral weight control sessions
over 16 weeks plus nicotine gum and an intermittent very-low-calorie diet
routine (81). Results showed that the very-low-calorie diet arm had a
significant effect on reducing weight gain at the end of treatment but not at 12
months and had a significant effect on increasing abstinence at 12 months. Other
trials have also shown that behavioral weight management programs delivered
sequentially to tobacco cessation treatment provide an effective method for
improving cessation and minimizing weight gain in quitters (80, 87).

PHYSICAL ACTIVITY APPROACHES

Several studies have demonstrated the benefit of increased physical activity and
reduced sedentary activity on both smoking cessation and weight management and
were included in at least one of the prior reviews. In one study, Marcus et al.
found that the exercise group had significantly higher rates of continuous
abstinence relative to the control group at the end of treatment (19.4% vs.
10.2%), at 3 months (16.4% vs. 8.2%), and at 12 months (11.9% vs. 5.4%) (88).
Exercise is helpful for weight management and increases psychological well-being
(88-92). Meta-analytic results of smoking cessation studies reveal that
exercise, irrespective of changes in fitness or body composition, can improve
body image, improve cessation rates, and significantly reduce postcessation
weight gain at 12 months (76, 77, 82).


TOBACCO CESSATION AND WEIGHT MANAGEMENT COMBINED INTERVENTIONS—PHARMACOLOGIC
APPROACHES

Current medications for tobacco cessation include NRT in the form of patches,
gum, lozenges, and spray, as well prescription medications such as varenicline,
bupropion, and cytosine. Combination NRT treatments such as adding nicotine gum
to the patch have been shown to be a more effective cessation strategy than
using only one medication (77). Systematic reviews concluded that some
pharmacological interventions limited post-cessation weight gain in the short
term, but this was not sustained by 6 and 12 months (36, 75, 77). More recently,
Taniguchi et al. found that varenicline significantly reduced weight gain at 12
months as compared with NRT (1.67 kg vs. 2.55 kg gain in weight) (93). Others
have shown that Bupropion SR and NRT, in particular 4 mg nicotine gum and 4 mg
nicotine lozenge, delayed but did not prevent weight gain, but duration of
medication use had a significant effect on weight. Compared with smokers who
received 8 weeks of nicotine patch therapy, those who received 24 weeks of
patches reported significantly less weight gain from pretreatment to week 24
(P = 0.002) and also from week 8 to week 24 (P = 0.03) (78, 94). Noteably,
Schnoll et al. found that NRT was less effective for women with obesity compared
with men with obesity or women and men who were not obese and that a fast-acting
NRT such as the nasal spray was more effective as a cessation aid than the patch
for smokers with obesity (95).

In summary, smoking cessation medications have been shown to delay but not
prevent weight gain associated with smoking cessation. However, there are a
limited number of studies of extended treatment duration or with long-term
follow-up and newer cessation medications have not been sufficiently studied
with regard to weight change. Studies with new drugs available for the treatment
of obesity such as sibutramine and orlistat may be needed to determine the
effects of these medications on smoking cessation and cessation-related weight
gain (36).


TOBACCO CESSATION AND WEIGHT MANAGEMENT COMBINED INTERVENTIONS—FOR PEOPLE WITH
DIABETES

Smokers with diabetes have had less success quitting tobacco in some but not all
studies. In a cross-sectional study of smokers who enrolled in a state quitline,
Schauer et al. found that having diabetes had no impact on the effectiveness of
smoking cessation treatment; 24.3% of those with diabetes versus 22.5% of those
without diabetes quit smoking at 6 months and no significant differences existed
between groups for weight gain, regardless of quit status. However, participants
with diabetes reported more weight gain in previous quit attempts; 34.2% of
those with diabetes vs. 22.4% of those without diabetes gained >20 lbs (8.84 kg)
(P = 0.03) (96). By contrast, an earlier study evaluated 6-month cessation
outcomes of state quitlines by chronic disease and reported that those with
diabetes had lower quit rates than those who did not have diabetes (97). In the
previous weight concerns study in quitlines cited above, addressing weight
concerns, challenging maladaptive beliefs, and encouraging acceptance of a
modest weight gain in smokers with diabetes had a significant effect on both
increasing abstinence and minimizing weight gain associated with cessation (85).
This study appears to be the only randomized trial of combined tobacco and
weight interventions that specifically evaluated cessation and weight outcomes
among smokers with diabetes. A recent review of randomized trials reporting the
effects of tobacco treatments in smokers with diabetes found no evidence of the
efficacy for more intensive versus less intensive tobacco cessation treatments.
In all the eight trials, the tobacco treatment was delivered by health care
providers and usually in clinics. Moreover, considerable heterogeneity existed
between the trials which included counseling, referral, advice, and/or some
diabetes-specific education. The review excluded a small number of trials of
complex interventions targeting those with and without diabetes. While the
authors suggested that more research and development is needed to determine if
cessation treatments tailored to patients with diabetes are needed (98), it is
clear that the positive outcomes of the weight concerns intervention among
people with diabetes need to be replicated.


ROLE OF PHYSICIANS IN HELPING SMOKERS MANAGE THEIR WEIGHT DURING TOBACCO
CESSATION

Health care providers have expressed concerns about asking their patients to
tackle two difficult behaviors simultaneously, such as quitting smoking and
losing weight (99). Providers also lack knowledge of a systematic integration of
multiple behavioral treatments for people with comorbid conditions. Training
opportunities for delivering such interventions or referring patients to
effective treatments for smoking and integrated weight control are either rare
or poorly utilized. Provider attitudes may also be inadvertently affecting their
treatment of smokers with obesity. One study found that among smokers with
overweight, obesity, and severe obesity, 3.7%, 3.4%, and 2.5%, respectively,
were prescribed a smoking cessation medication as compared with 5.11% of
normal-weight smokers (100). These findings of lower rates of prescribing
smoking cessation medications could explain why smokers with obesity may have
worse cessation outcomes. Despite three comprehensive reviews (75-77) indicating
the safety and short-term efficacy of combining cessation and weight-based
treatments, knowledge and availability of such programs have not been widely
disseminated.

The USPHS 2008 tobacco guideline which advises clinicians to help patients quit
smoking first and then address weight gain either personally or by referral may
need to be altered in light of new evidence of the safety and efficacy of
combined tobacco cessation and weight control treatments (94). However, the
following guideline recommendations are in line with current evidence:
 * Start or increase physical activity.
 * Reassure smokers that some weight gain after quitting is common and usually
   is self-limiting with lifestyle changes.
 * Suggest low-calorie substitutes to smoking such as sugarless chewing gum,
   vegetables, or mints.
 * Maintain patients on medication known to delay weight gain (e.g., bupropion
   SR, NRTs—particularly 4 mg nicotine gum and lozenge).
 * Refer smokers to a qualified weight loss professional or evidence-based
   commercial weight loss program for personalized dietary and exercise
   programs.


DISCUSSION

While this is not a systematic review, important studies have been highlighted
and recommendations for improvements are identified. This narrative review on
the broad topic of smoking cessation, weight gain, and diabetes highlights some
of the seminal studies and knowledge gaps in line with the theme of the article.
This appraisal of the research shows that there is evidence that combining
personalized behavioral weight management interventions with tobacco cessation
treatments (either simultaneously or sequentially) can provide a safe and
successful approach for reducing weight gain and improving cessation outcomes
for some individuals (75-77, 79, 82, 85). Overall, results of these trials
suggest that reducing a smoker's excessive fear of gaining weight and providing
personalized dietary and physical activity interventions may limit weight gain
without reducing abstinence in the short term. While the most recent Cochrane
review (77) states there are not enough studies to make strong recommendations
for effective interventions to prevent weight gain, separating studies that
focus on “weight concerns” (not targeting weight gain prevention) from those
that employ evidence-based behavioral weight loss techniques provides reasons to
believe that weight management during cessation can be effective. Smoking
cessation medications can also improve cessation rates, but the long-term
effectiveness on reducing weight gain is unknown. More research is needed with
longer follow-up periods and high-risk populations such as smokers with obesity
and diabetes.

In conclusion, while 80% to 90% of smokers will gain weight after quitting
without a weight management intervention, there is some evidence to suggest that
combining weight management with cessation could improve these numbers. Of
particular concern are the 10% to 20% of smokers who gain in excess of 10 kg.
Unfortunately, current evidence does not provide clear ways to identify this
population in advance, although individuals with more severe obesity or those
with diabetes may be at greater risk and therefore should receive more
aggressive weight management intervention during cessation. While it may be
tempting to ask whether quitting is best for every smoker, it is important to
note that the health benefits of abstaining from tobacco outweigh the health
risks associated with quitting, including those of weight gain. Risk factors can
be minimized by close monitoring and a sensible approach to dietary and
lifestyles changes.


RECOMMENDATIONS AND DIRECTIONS FOR THE FUTURE

Although research has shown the short-term effectiveness of smoking cessation
treatments that also address weight gain, the sustainability of these outcomes
on weight and tobacco cessation in the long term warrants further research.
Similarly, combinations of weight- and tobacco-based treatments need to be
tested with smokers who are at high risk for, or currently have, diabetes and
those who have obesity. Future research and development work should include
economic evaluations of current and new combined treatments, long-term
follow-up, and developing integrated interventions involving tobacco cessation,
weight management, and diabetes risk reduction.

For now, many of the key intervention components of combined tobacco and weight
treatment could be integrated into current clinical and behavioral treatment and
include encouraging smokers to add more physical activity, healthy foods,
regular meals, and self-monitoring to their focus on quitting smoking.
Multifaceted interventions informed by clinical, behavioral, pharmacological,
and genetic research are needed and these interventions should integrate new
learnings from tobacco control and obesity research. Findings reviewed here are
relevant to policy makers, health care professionals, research teams, and
governments interested in continuing to find ways to reduce the burden of
tobacco addiction and excess body weight.


ACKNOWLEDGMENTS

We thank Erica Salmon and Brooke Magnusson for manuscript preparation and
support.

REFERENCES

 * 1 Mokdad AH, Marks JS, Stroup DF, Gerberding JL. Actual causes of death in
   the United States, 2000. JAMA 2004; 291: 1238-1245.
   10.1001/jama.291.10.1238
   
   PubMedWeb of Science®Google Scholar
 * 2 Wadden TA, Brownell KD, Foster GD. Obesity: responding to the global
   epidemic. J Consult Clin Psychol 2002; 70: 510-525.
   10.1037/0022-006X.70.3.510
   
   PubMedWeb of Science®Google Scholar
 * 3 Chiolero A, Faeh D, Paccaud F, Cornuz J. Consequences of smoking for body
   weight, body fat distribution, and insulin resistance. Am J Clin Nutr 2008;
   87: 801-809.
   10.1093/ajcn/87.4.801
   
   CASPubMedWeb of Science®Google Scholar
 * 4 Chiolero A, Peytremann-Bridevaux I, Paccaud F. Associations between obesity
   and health conditions may be overestimated if self-reported body mass index
   is used. Obes Rev 2007; 8: 373-374.
   10.1111/j.1467-789X.2007.00375.x
   
   CASPubMedWeb of Science®Google Scholar
 * 5 Chiolero A, Wietlisbach V, Ruffieux C, Paccaud F, Cornuz J. Clustering of
   risk behaviors with cigarette consumption: a population-based survey. Prev
   Med 2006; 42: 348-353.
   10.1016/j.ypmed.2006.01.011
   
   PubMedWeb of Science®Google Scholar
 * 6 Healton CG, Vallone D, McCausland KL, Xiao H, Green MP. Smoking, obesity,
   and their co-occurrence in the United States: cross sectional analysis. BMJ
   2006; 333: 25-26.
   10.1136/bmj.38840.608704.80
   
   PubMedWeb of Science®Google Scholar
 * 7 Sturm R. The effects of obesity, smoking, and drinking on medical problems
   and costs. Health Aff (Millwood) 2002; 21: 245-253.
   10.1377/hlthaff.21.2.245
   
   PubMedWeb of Science®Google Scholar
 * 8 Freedman DM, Sigurdson AJ, Rajaraman P, Doody MM, Linet MS, Ron E. The
   mortality risk of smoking and obesity combined. Am J Prev Med 2006; 31:
   355-362.
   10.1016/j.amepre.2006.07.022
   
   PubMedWeb of Science®Google Scholar
 * 9 Levine MD, Kalarchian MA, Courcoulas AP, Wisinski MS, Marcus MD. History of
   smoking and postcessation weight gain among weight loss surgery candidates.
   Addict Behav 2007; 32: 2365-2371.
   10.1016/j.addbeh.2007.02.002
   
   PubMedWeb of Science®Google Scholar
 * 10 Bush T, Levine MD, Deprey M, et al. Prevalence of weight concerns and
   obesity among smokers calling a quitline. J Smok Cessat 2008; 4: 74-78.
   10.1375/jsc.4.2.74
   
   PubMedGoogle Scholar
 * 11 Kendzor DE, Businelle MS, Cofta-Woerpel LM, et al. Mechanisms linking
   socioeconomic disadvantage and BMI in smokers. Am J Health Behav 2013; 37:
   587-598.
   10.5993/AJHB.37.5.2
   
   PubMedWeb of Science®Google Scholar
 * 12 Kendzor DE, Costello TJ, Li Y, et al. Race/ethnicity and multiple cancer
   risk factors among individuals seeking smoking cessation treatment. Cancer
   Epidemiol Biomarkers Prev 2008; 17: 2937-2945.
   10.1158/1055-9965.EPI-07-2795
   
   PubMedWeb of Science®Google Scholar
 * 13 LaRowe TL, Piper ME, Schlam TR, Fiore MC, Baker TB. Obesity and smoking:
   comparing cessation treatment seekers with the general smoking population.
   Obesity (Silver Spring) 2009; 17: 1301-1305.
   10.1038/oby.2009.36
   
   PubMedWeb of Science®Google Scholar
 * 14 Kahn SE, Hull RL, Utzschneider KM. Mechanisms linking obesity to insulin
   resistance and type 2 diabetes. Nature 2006; 444: 840-846.
   10.1038/nature05482
   
   CASPubMedWeb of Science®Google Scholar
 * 15 Koster A, Leitzmann MF, Schatzkin A, et al. The combined relations of
   adiposity and smoking on mortality. Am J Clin Nutr 2008; 88: 1206-1212.
   
   CASPubMedWeb of Science®Google Scholar
 * 16 An R, Shi Y. Body weight status and onset of functional limitations in
   U.S. middle-aged and older adults. Disabil Health J 2015; 8: 336-344.
   10.1016/j.dhjo.2015.02.003
   
   PubMedWeb of Science®Google Scholar
 * 17 Moriarty JP, Branda ME, Olsen KD, et al. The effects of incremental costs
   of smoking and obesity on health care costs among adults: a 7-year
   longitudinal study. J Occup Environ Med 2012; 54: 286-291.
   10.1097/JOM.0b013e318246f1f4
   
   PubMedWeb of Science®Google Scholar
 * 18 Veldheer S, Yingst J, Zhu J, Foulds J. Ten-year weight gain in smokers who
   quit, smokers who continued smoking and never smokers in the United States,
   NHANES 2003-2012. Int J Obes (Lond) 2015; 39: 1727-1732.
   10.1038/ijo.2015.127
   
   CASPubMedWeb of Science®Google Scholar
 * 19 Tian J, Venn A, Otahal P, Gall S. The association between quitting smoking
   and weight gain: a systemic review and meta-analysis of prospective cohort
   studies. Obes Rev 2015; 16: 883-901.
   10.1111/obr.12304
   
   CASPubMedWeb of Science®Google Scholar
 * 20 Klesges RC, Winders SE, Meyers AW, et al. How much weight gain occurs
   following smoking cessation? A comparison of weight gain using both
   continuous and point prevalence abstinence. J Consult Clin Psychol 1997; 65:
   286-291.
   10.1037/0022-006X.65.2.286
   
   CASPubMedWeb of Science®Google Scholar
 * 21 Pistelli F, Aquilini F, Carrozzi L. Weight gain after smoking cessation.
   Monaldi Arch Chest Dis 2009; 71: 81-87.
   
   CASPubMedGoogle Scholar
 * 22 Lycett D, Munafo M, Johnstone E, Murphy M, Aveyard P. Associations between
   weight change over 8 years and baseline body mass index in a cohort of
   continuing and quitting smokers. Addiction 2011; 106: 188-196.
   10.1111/j.1360-0443.2010.03136.x
   
   PubMedWeb of Science®Google Scholar
 * 23 Aubin HJ, Farley A, Lycett D, Lahmek P, Aveyard P. Weight gain in smokers
   after quitting cigarettes: meta-analysis. BMJ 2012; 345: e4439.
   10.1136/bmj.e4439
   
   PubMedWeb of Science®Google Scholar
 * 24 Bush TM, Levine MD, Magnusson B, et al. Impact of baseline weight on
   smoking cessation and weight gain in quitlines. Ann Behav Med 2014; 47:
   208-217.
   10.1007/s12160-013-9537-z
   
   PubMedWeb of Science®Google Scholar
 * 25 Scherr A, Seifert B, Kuster M, et al. Predictors of marked weight gain in
   a population of health care and industrial workers following smoking
   cessation. BMC Public Health 2015; 15: 520.
   10.1186/s12889-015-1854-7
   
   PubMedWeb of Science®Google Scholar
 * 26 Whitlock G, Lewington S, Sherliker P, et al. Body-mass index and
   cause-specific mortality in 900 000 adults: collaborative analyses of 57
   prospective studies. Lancet 2009; 373: 1083-1096.
   10.1016/S0140-6736(09)60318-4
   
   PubMedWeb of Science®Google Scholar
 * 27 Pisinger C, Jorgensen T. Waist circumference and weight following smoking
   cessation in a general population: the Inter99 study. Prev Med 2007; 44:
   290-295.
   10.1016/j.ypmed.2006.11.015
   
   PubMedWeb of Science®Google Scholar
 * 28 Froom P, Kristal-Boneh E, Melamed S, Gofer D, Benbassat J, Ribak J.
   Smoking cessation and body mass index of occupationally active men: the
   Israeli CORDIS Study. Am J Public Health 1999; 89: 718-722.
   10.2105/AJPH.89.5.718
   
   CASPubMedWeb of Science®Google Scholar
 * 29 Swan GE, Carmelli D. Characteristics associated with excessive weight gain
   after smoking cessation in men. Am J Public Health 1995; 85: 73-77.
   10.2105/AJPH.85.1.73
   
   CASPubMedWeb of Science®Google Scholar
 * 30 Sanchez-Johnsen LA. Smoking cessation, obesity and weight concerns in
   black women: a call to action for culturally competent interventions. J Natl
   Med Assoc 2005; 97: 1630-1638.
   
   PubMedGoogle Scholar
 * 31 Williamson DF, Madans J, Anda RF, Kleinman JC, Giovino GA, Byers T.
   Smoking cessation and severity of weight gain in a national cohort. N Engl J
   Med 1991; 324: 739-745.
   10.1056/NEJM199103143241106
   
   CASPubMedWeb of Science®Google Scholar
 * 32 Prod'hom S, Locatelli I, Giraudon K, et al. Predictors of weight change in
   sedentary smokers receiving a standard smoking cessation intervention.
   Nicotine Tob Res 2013; 15: 910-916.
   10.1093/ntr/nts217
   
   CASPubMedWeb of Science®Google Scholar
 * 33 Klesges RC, Meyers AW, Klesges LM, La Vasque ME. Smoking, body weight, and
   their effects on smoking behavior: a comprehensive review of the literature.
   Psychol Bull 1989; 106: 204-230.
   10.1037/0033-2909.106.2.204
   
   CASPubMedWeb of Science®Google Scholar
 * 34 Kokkinos P. Physical activity, health benefits, and mortality risk. ISRN
   Cardiol 2012; 2012: 718789. Epub 2012/12/01.
   10.5402/2012/718789
   
   PubMedGoogle Scholar
 * 35 Komiyama M, Wada H, Ura S, et al. Analysis of factors that determine
   weight gain during smoking cessation therapy. PLoS One 2013; 8: e72010.
   10.1371/journal.pone.0072010
   
   CASPubMedWeb of Science®Google Scholar
 * 36 Filozof C, Fernandez Pinilla MC, Fernandez-Cruz A. Smoking cessation and
   weight gain. Obes Rev 2004; 5: 95-103.
   10.1111/j.1467-789X.2004.00131.x
   
   CASPubMedGoogle Scholar
 * 37 Copeland AL, Martin PD, Geiselman PJ, Rash CJ, Kendzor DE. Smoking
   cessation for weight-concerned women: group vs. individually tailored,
   dietary, and weight-control follow-up sessions. Addict Behav 2006; 31:
   115-127.
   10.1016/j.addbeh.2005.04.020
   
   PubMedWeb of Science®Google Scholar
 * 38 Rabkin S. Relationship between weight change and the reduction or
   cessation of cigarette smoking. Int J Obes 1984; 8: 665-673.
   
   CASPubMedWeb of Science®Google Scholar
 * 39 Flegal KM, Troiano RP, Pamuk ER, Kuczmarski RJ, Campbell SM. The influence
   of smoking cessation on the prevalence of overweight in the United States. N
   Engl J Med 1995; 333: 1165-1170.
   10.1056/NEJM199511023331801
   
   CASPubMedWeb of Science®Google Scholar
 * 40 White MA, Peters EN, Toll BA. Effect of binge eating on treatment outcomes
   for smoking cessation. Nicotine Tob Res 2010; 12: 1172-1175.
   10.1093/ntr/ntq163
   
   PubMedWeb of Science®Google Scholar
 * 41 Carney RM, Goldberg AP. Weight gain after cessation of cigarette smoking.
   A possible role for adipose-tissue lipoprotein lipase. N Engl J Med 1984;
   310: 614-616.
   10.1056/NEJM198403083101002
   
   CASPubMedWeb of Science®Google Scholar
 * 42 Audrain-McGovern J, Benowitz NL. Cigarette smoking, nicotine, and body
   weight. Clin Pharmacol Ther 2011; 90: 164-168.
   10.1038/clpt.2011.105
   
   CASPubMedWeb of Science®Google Scholar
 * 43 Jo YH, Talmage DA, Role LW. Nicotinic receptor-mediated effects on
   appetite and food intake. J Neurobiol 2002; 53: 618-632.
   10.1002/neu.10147
   
   CASPubMedWeb of Science®Google Scholar
 * 44 Rodin J. Weight change following smoking cessation: the role of food
   intake and exercise. Addict Behav 1987; 12: 303-317.
   10.1016/0306-4603(87)90045-1
   
   CASPubMedWeb of Science®Google Scholar
 * 45 Kleppinger A, Litt MD, Kenny AM, Oncken CA. Effects of smoking cessation
   on body composition in postmenopausal women. J Womens Health (Larchmt) 2010;
   19: 1651-1657.
   10.1089/jwh.2009.1853
   
   PubMedWeb of Science®Google Scholar
 * 46 Biedermann L, Zeitz J, Mwinyi J, et al. Smoking cessation induces profound
   changes in the composition of the intestinal microbiota in humans. PLoS One
   2013; 8: e59260..
   10.1371/journal.pone.0059260
   
   CASPubMedWeb of Science®Google Scholar
 * 47 Pepino MY, Mennella JA. Cigarette smoking and obesity are associated with
   decreased fat perception in women. Obesity (Silver Spring) 2014; 22:
   1050-1055.
   10.1002/oby.20697
   
   CASPubMedWeb of Science®Google Scholar
 * 48 Blum K, Liu Y, Shriner R, Gold MS. Reward circuitry dopaminergic
   activation regulates food and drug craving behavior. Curr Pharm Des 2011; 17:
   1158-1167.
   10.2174/138161211795656819
   
   CASPubMedWeb of Science®Google Scholar
 * 49 Stice E, Burger KS, Yokum S. Reward region responsivity predicts future
   weight gain and moderating effects of the TaqIA allele. J Neurosci 2015; 35:
   10316-10324.
   10.1523/JNEUROSCI.3607-14.2015
   
   CASPubMedWeb of Science®Google Scholar
 * 50 Stice E, Rohde P, Gau J, Shaw H. Effect of a dissonance-based prevention
   program on risk for eating disorder onset in the context of eating disorder
   risk factors. Prev Sci 2012; 13: 129-139.
   10.1007/s11121-011-0251-4
   
   PubMedWeb of Science®Google Scholar
 * 51 Hall SM, Tunstall CD, Vila KL, Duffy J. Weight gain prevention and smoking
   cessation: cautionary findings. Am J Public Health 1992; 82: 799-803.
   10.2105/AJPH.82.6.799
   
   CASPubMedWeb of Science®Google Scholar
 * 52 Willi C, Bodenmann P, Ghali WA, Faris PD, Cornuz J. Active smoking and the
   risk of type 2 diabetes: a systematic review and meta-analysis. JAMA 2007;
   298: 2654-2664.
   10.1001/jama.298.22.2654
   
   CASPubMedWeb of Science®Google Scholar
 * 53 National Center for Chronic Disease P, Health Promotion Office on S,
   Health. Reports of the Surgeon General. The Health Consequences of Smoking-50
   Years of Progress: A Report of the Surgeon General. Centers for Disease
   Control and Prevention (US): Atlanta, GA; 2014.
   
   Google Scholar
 * 54 Tonstad S. Cigarette smoking, smoking cessation, and diabetes. Diabetes
   Res Clin Pract 2009; 85: 4-13.
   10.1016/j.diabres.2009.04.013
   
   PubMedWeb of Science®Google Scholar
 * 55 Nakanishi N, Nakamura K, Matsuo Y, Suzuki K, Tatara K. Cigarette smoking
   and risk for impaired fasting glucose and type 2 diabetes in middle-aged
   Japanese men. Ann Intern Med 2000; 133: 183-191.
   10.7326/0003-4819-133-3-200008010-00009
   
   CASPubMedWeb of Science®Google Scholar
 * 56 Yeh HC, Duncan BB, Schmidt MI, Wang NY, Brancati FL. Smoking, smoking
   cessation, and risk for type 2 diabetes mellitus: a cohort study. Ann Intern
   Med 2010; 152: 10-17.
   10.7326/0003-4819-152-1-201001050-00005
   
   PubMedWeb of Science®Google Scholar
 * 57 Clair C, Rigotti NA, Meigs JB. Smoking cessation, weight change, and risk
   of cardiovascular disease-reply. JAMA 2013; 310: 323.
   10.1001/jama.2013.7945
   
   CASPubMedWeb of Science®Google Scholar
 * 58 Benowitz NL. Cigarette smoking and cardiovascular disease: pathophysiology
   and implications for treatment. Prog Cardiovasc Dis 2003; 46: 91-111.
   10.1016/S0033-0620(03)00087-2
   
   CASPubMedWeb of Science®Google Scholar
 * 59 Eliasson B, Attvall S, Taskinen MR, Smith U. Smoking cessation improves
   insulin sensitivity in healthy middle-aged men. Eur J Clin Invest 1997; 27:
   450-456.
   10.1046/j.1365-2362.1997.1330680.x
   
   CASPubMedWeb of Science®Google Scholar
 * 60 Nilsson PM, Gudbjornsdottir S, Eliasson B, Cederholm J. Smoking is
   associated with increased HbA1c values and microalbuminuria in patients with
   diabetes-data from the National Diabetes Register in Sweden. Diabetes Metab
   2004; 30: 261-268.
   10.1016/S1262-3636(07)70117-9
   
   CASPubMedWeb of Science®Google Scholar
 * 61 Eliasson B, Mero N, Taskinen MR, Smith U. The insulin resistance syndrome
   and postprandial lipid intolerance in smokers. Atherosclerosis 1997; 129:
   79-88.
   10.1016/S0021-9150(96)06028-5
   
   CASPubMedWeb of Science®Google Scholar
 * 62 Qin R, Chen T, Lou Q, Yu D. Excess risk of mortality and cardiovascular
   events associated with smoking among patients with diabetes: meta-analysis of
   observational prospective studies. Int J Cardiol 2013; 167: 342-350.
   10.1016/j.ijcard.2011.12.100
   
   PubMedWeb of Science®Google Scholar
 * 63 Celermajer DS, Sorensen KE, Georgakopoulos D, et al. Cigarette smoking is
   associated with dose-related and potentially reversible impairment of
   endothelium-dependent dilation in healthy young adults. Circulation 1993; 88:
   2149-2155.
   10.1161/01.CIR.88.5.2149
   
   CASPubMedWeb of Science®Google Scholar
 * 64 Balkau B, Vierron E, Vernay M, et al. The impact of 3-year changes in
   lifestyle habits on metabolic syndrome parameters: the D.E.S.I.R study. Eur J
   Cardiovasc Prev Rehabil 2006; 13: 334-340.
   10.1097/00149831-200606000-00007
   
   PubMedWeb of Science®Google Scholar
 * 65 Lycett D, Nichols L, Ryan R, et al. The association between smoking
   cessation and glycaemic control in patients with type 2 diabetes: a THIN
   database cohort study. Lancet Diabetes Endocrinol 2015; 3: 423-430.
   10.1016/S2213-8587(15)00082-0
   
   PubMedWeb of Science®Google Scholar
 * 66 Stein JH, Asthana A, Smith SS, et al. Smoking cessation and the risk of
   diabetes mellitus and impaired fasting glucose: three-year outcomes after a
   quit attempt. PLoS One 2014; 9: e98278.
   10.1371/journal.pone.0098278
   
   PubMedWeb of Science®Google Scholar
 * 67 Pan A, Wang Y, Talaei M, Hu FB, Wu T. Relation of active, passive, and
   quitting smoking with incident type 2 diabetes: a systematic review and
   meta-analysis. Lancet Diabetes Endocrinol 2015; 3: 958-967.
   10.1016/S2213-8587(15)00316-2
   
   PubMedWeb of Science®Google Scholar
 * 68 Oba S, Noda M, Waki K, et al. Smoking cessation increases short-term risk
   of type 2 diabetes irrespective of weight gain: the Japan Public Health
   Center-Based Prospective Study. PLoS One 2012; 7: e17061.
   10.1371/journal.pone.0017061
   
   CASPubMedWeb of Science®Google Scholar
 * 69 Morimoto A, Ohno Y, Tatsumi Y, et al. Impact of smoking cessation on
   incidence of diabetes mellitus among overweight or normal-weight Japanese
   men. Diabetes Res Clin Pract 2012; 96: 407-413.
   10.1016/j.diabres.2012.03.007
   
   PubMedWeb of Science®Google Scholar
 * 70 Tamura U, Tanaka T, Okamura T, et al. Changes in weight, cardiovascular
   risk factors and estimated risk of coronary heart disease following smoking
   cessation in Japanese male workers: HIPOP-OHP study. J Atheroscler Thromb
   2010; 17: 12-20.
   10.5551/jat.1800
   
   PubMedWeb of Science®Google Scholar
 * 71 Hall SM, McGee R, Tunstall C, Duffy J, Benowitz N. Changes in food intake
   and activity after quitting smoking. J Consult Clin Psychol 1989; 57: 81-86.
   10.1037/0022-006X.57.1.81
   
   CASPubMedWeb of Science®Google Scholar
 * 72 Perkins KA, Epstein LH, Pastor S. Changes in energy balance following
   smoking cessation and resumption of smoking in women. J Consult Clin Psychol
   1990; 58: 121-125.
   10.1037/0022-006X.58.1.121
   
   CASPubMedWeb of Science®Google Scholar
 * 73 Luo J, Rossouw J, Margolis KL. Smoking cessation, weight change, and
   coronary heart disease among postmenopausal women with and without diabetes.
   JAMA 2013; 310: 94-96.
   10.1001/jama.2013.6871
   
   CASPubMedWeb of Science®Google Scholar
 * 74 Pirie K, Peto R, Reeves GK, Green J, Beral V. The 21st century hazards of
   smoking and benefits of stopping: a prospective study of one million women in
   the UK. Lancet 2013; 381: 133-141.
   10.1016/S0140-6736(12)61720-6
   
   PubMedWeb of Science®Google Scholar
 * 75 Parsons AC, Shraim M, Inglis J, Aveyard P, Hajek P. Interventions for
   preventing weight gain after smoking cessation. Cochrane Database Syst Rev
   2009; Cd006219.
   
   PubMedWeb of Science®Google Scholar
 * 76 Spring B, Howe D, Berendsen M, et al. Behavioral intervention to promote
   smoking cessation and prevent weight gain: a systematic review and
   meta-analysis. Addiction 2009; 104: 1472-1486.
   10.1111/j.1360-0443.2009.02610.x
   
   CASPubMedWeb of Science®Google Scholar
 * 77 Farley AC, Hajek P, Lycett D, Aveyard P. Interventions for preventing
   weight gain after smoking cessation. Cochrane Database Syst Rev 2012; 1:
   Cd006219.
   
   PubMedWeb of Science®Google Scholar
 * 78 Levine MD, Perkins KA, Kalarchian MA, et al. Bupropion and cognitive
   behavioral therapy for weight-concerned women smokers. Arch Intern Med 2010;
   170: 543-550.
   10.1001/archinternmed.2010.33
   
   PubMedWeb of Science®Google Scholar
 * 79 Perkins KA, Marcus MD, Levine MD, et al. Cognitive-behavioral therapy to
   reduce weight concerns improves smoking cessation outcome in weight-concerned
   women. J Consult Clin Psychol 2001; 69: 604-613.
   10.1037/0022-006X.69.4.604
   
   CASPubMedWeb of Science®Google Scholar
 * 80 Spring B, Pagoto S, Pingitore R, Doran N, Schneider K, Hedeker D.
   Randomized controlled trial for behavioral smoking and weight control
   treatment: effect of concurrent versus sequential intervention. J Consult
   Clin Psychol 2004; 72: 785-796.
   10.1037/0022-006X.72.5.785
   
   PubMedWeb of Science®Google Scholar
 * 81 Danielsson T, Rossner S, Westin A. Open randomised trial of intermittent
   very low energy diet together with nicotine gum for stopping smoking in women
   who gained weight in previous attempts to quit. BMJ 1999; 319: 490-493;
   discussion 4.
   10.1136/bmj.319.7208.490
   
   CASPubMedWeb of Science®Google Scholar
 * 82 Aveyard P, Lycett D, Farley A. Managing smoking cessationrelated weight
   gain. Pol Arch Med Wewn 2012; 122: 494-498.
   
   PubMedWeb of Science®Google Scholar
 * 83 Napolitano MA, Lloyd-Richardson EE, Fava JL, Marcus BH. Targeting body
   image schema for smoking cessation among college females: rationale, program
   description, and pilot study results. Behav Modif 2011; 35: 323-346.
   10.1177/0145445511404840
   
   PubMedWeb of Science®Google Scholar
 * 84 Clark MM, Hays JT, Vickers KS, et al. Body image treatment for weight
   concerned smokers: a pilot study. Addict Behav 2005; 30: 1236-1240.
   10.1016/j.addbeh.2004.10.009
   
   PubMedWeb of Science®Google Scholar
 * 85 Bush T, Levine MD, Beebe LA, et al. Addressing weight gain in smoking
   cessation treatment: a randomized controlled trial. Am J Health Promot 2012;
   27: 94-102.
   10.4278/ajhp.110603-QUAN-238
   
   PubMedWeb of Science®Google Scholar
 * 86 Leslie WS, Koshy PR, Mackenzie M, et al. Changes in body weight and food
   choice in those attempting smoking cessation: a cluster randomised controlled
   trial. BMC Public Health 2012; 12: 389.
   10.1186/1471-2458-12-389
   
   PubMedWeb of Science®Google Scholar
 * 87 Filia SL, Baker AL, Kulkarni J, Williams JM. Sequential behavioral
   treatment of smoking and weight control in bipolar disorder. Transl Behav Med
   2012; 2: 290-295.
   10.1007/s13142-012-0111-1
   
   PubMedWeb of Science®Google Scholar
 * 88 Marcus BH, Albrecht AE, King TK, et al. The efficacy of exercise as an aid
   for smoking cessation in women: a randomized controlled trial. Arch Intern
   Med 1999; 159: 1229-1234.
   10.1001/archinte.159.11.1229
   
   CASPubMedWeb of Science®Google Scholar
 * 89 Donnelly JE, Blair SN, Jakicic JM, Manore MM, Rankin JW, Smith BK,
   American College of Sports Medicine Position Stand. Appropriate physical
   activity intervention strategies for weight loss and prevention of weight
   regain for adults. Med Sci Sports Exerc 2009; 41: 459-471.
   10.1249/MSS.0b013e3181949333
   
   PubMedWeb of Science®Google Scholar
 * 90 Hoffman MD, Hoffman DR. Exercisers achieve greater acute exercise-induced
   mood enhancement than nonexercisers. Arch Phys Med Rehabil 2008; 89: 358-363.
   10.1016/j.apmr.2007.09.026
   
   PubMedWeb of Science®Google Scholar
 * 91 Jakicic JM, Marcus BH, Lang W, Janney C. Effect of exercise on 24-month
   weight loss maintenance in overweight women. Arch Intern Med 2008; 168:
   1550-1559. discussion 9-60.
   10.1001/archinte.168.14.1550
   
   PubMedWeb of Science®Google Scholar
 * 92 Ussher M, Nunziata P, Cropley M, West R. Effect of a short bout of
   exercise on tobacco withdrawal symptoms and desire to smoke.
   Psychopharmacology (Berl) 2001; 158: 66-72.
   10.1007/s002130100846
   
   CASPubMedWeb of Science®Google Scholar
 * 93 Taniguchi C, Tanaka H, Oze I, et al. Factors associated with weight gain
   after smoking cessation therapy in Japan. Nurs Res 2013; 62: 414-421.
   10.1097/NNR.0000000000000000
   
   PubMedWeb of Science®Google Scholar
 * 94 Fiore MC, Jaén CR, Baker TB, et al. Treating Tobacco Use and Dependence:
   2008 Update. Clinical Practice Guideline. Rockville, MD: U.S. Department of
   Health and Human Services. Public Health Service. May 2008.
   
   Google Scholar
 * 95 Schnoll RA, Patterson F, Wileyto EP, Tyndale RF, Benowitz N, Lerman C.
   Nicotine metabolic rate predicts successful smoking cessation with
   transdermal nicotine: a validation study. Pharmacol Biochem Behav 2009; 92:
   6-11.
   10.1016/j.pbb.2008.10.016
   
   CASPubMedWeb of Science®Google Scholar
 * 96 Schauer GL, Bush T, Cerutti B, Mahoney L, Thompson JR, Zbikowski SM. Use
   and effectiveness of quitlines for smokers with diabetes: cessation and
   weight outcomes, Washington State Tobacco Quit Line, 2008. Prev Chronic Dis
   2013; 10: E105.
   10.5888/pcd10.120324
   
   PubMedWeb of Science®Google Scholar
 * 97 Bush T, Zbikowski SM, Mahoney L, Deprey M, Mowery P, Cerutti B. State
   quitlines and cessation patterns among adults with selected chronic diseases
   in 15 states, 2005-2008. Prev Chronic Dis 2012; 9: E163.
   10.5888/pcd9.120105
   
   PubMedWeb of Science®Google Scholar
 * 98 Nagrebetsky A, Brettell R, Roberts N, Farmer A. Smoking cessation in
   adults with diabetes: a systematic review and meta-analysis of data from
   randomised controlled trials. BMJ Open 2014; 4: e004107.
   10.1136/bmjopen-2013-004107
   
   PubMedWeb of Science®Google Scholar
 * 99 Siddiqi KDO, Siddiqi N. Smoking cessation in long-term conditions: is
   there ‘‘an opportunity in every difficulty’’? Int J Popul Res 2013; 2013: 10.
   
   Google Scholar
 * 100 Yu Y, Rajan SS, Essien EJ, Yang M, Abughosh S. The relationship between
   obesity and prescription of smoking cessation medications. Popul Health Manag
   2014; 17: 172-179.
   10.1089/pop.2013.0059
   
   PubMedWeb of Science®Google Scholar


CITING LITERATURE




Volume24, Issue9

September 2016

Pages 1834-1841





 * REFERENCES


 * RELATED


 * INFORMATION


RECOMMENDED

 * Smoking cessation and weight gain
   
   C. Filozof, M. C. Fernández Pinilla, A. Fernández-Cruz, 
   Obesity Reviews

 * Smoking cessation, weight gain, and DRD4 −521 genotype
   
   Marcus R. Munafò, Michael F.G. Murphy, Elaine C. Johnstone, 
   American Journal of Medical Genetics Part B: Neuropsychiatric Genetics

 * Fueling the Obesity Epidemic? Artificially Sweetened Beverage Use and
   Long‐term Weight Gain
   
   Sharon P. Fowler, Ken Williams, Roy G. Resendez, Kelly J. Hunt, Helen P.
   Hazuda, Michael P. Stern, 
   Obesity

 * Weight gain and obesity after liver transplantation
   
   James Richards, Bridget Gunson, Jill Johnson, James Neuberger, 
   Transplant International

 * Cigarette Smoking, Nicotine, and Body Weight
   
   J Audrain-McGovern, NL Benowitz, 
   Clinical Pharmacology & Therapeutics




METRICS

Citations: 135



DETAILS

© 2016 The Obesity Society



 * Check for updates


RESEARCH FUNDING

 * National Institute on Drug Abuse . Grant Number: RO1DA031147
 * National Center for Complementary and Integrative Health as well as Alere
   Wellbeing and Arivale, Inc . Grant Number: R21AT007845


PUBLICATION HISTORY

 * Issue Online: 29 August 2016
 * Version of Record online: 29 August 2016
 * Manuscript accepted: 17 May 2016
 * Manuscript revised: 21 April 2016
 * Manuscript received: 05 October 2015




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