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    Fax +41 61 306 12 34

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    Original Paper

    Neuropsychobiology 2009;60:3743

    DOI: 10.1159/000235800

    Sex-Specific Associations of BodyMass Index with Mood Disturbanceduring Smoking Abstinence

    Natalie A. Ceballosa Stephanie Hookerb Mustafa alAbsibd

    aDepartment of Psychology, Texas State University, San Marcos, Tex., Departments ofbBehavioral Sciences, cFamily

    Medicine, and dPhysiology and Pharmacology, University of Minnesota Medical School, Duluth, Minn., USA

    Introduction

    For decades, scientific literature has acknowledged thejolly fat hypothesis, which predicts that overweight peo-ple will have a lower risk of depression and exhibit a low-er number of depressive symptoms relative to individualsof normal weight [1, 2]. More recently, the hypothesis hasresurfaced emphasizing sex differences in the relation-ship between obesity and mood. For instance, Oinonen

    and Mazmanian [3] observed an inverse relationship be-tween body mass index (BMI) and negative mood in asample of young female participants. The authors attrib-uted this effect to potential increases in estrogen avail-ability in individuals with a higher level of fatty tissues.

    Although estrogen levels were not assessed in the afore-mentioned study, the authors theory is worthy of furtherresearch, as estrogen is known to increase the availabilityof serotonin, a neurotransmitter linked with depression[2, 4]. Thus, this mechanism may partly account for theinverse relationship noted between BMI and negativemood among females. However, it is important to ac-

    knowledge that a number of studies have reported con-flicting results on this issue [5, 6]. Further, the reason forhigher estrogen levels in persons with high levels of fattytissue would also apply to males; thus, the literature re-mains contentious regarding the jolly fat hypothesis anda number of comorbid factors remain to be considered.

    Tobacco use is one factor that has not been addressedin previous investigations of the relationship between

    Key Words

    Body mass index Nicotine Smoking Gender Mood

    Abstract

    Objective:Previous reports have suggested an inverse rela-

    tionship between body mass index (BMI) and negative mood

    in women. However, little is known about the potential as-

    sociation of these variables under stressful conditions, such

    as those experienced during smoking cessation. The currentinvestigation examined the relationship of BMI and various

    indices of mood in a sample of male and female cigarette

    smokers undergoing cessation. Methods: Along with base-

    line assessments of variables such as depression and anxiety,

    total mood disturbance and perceived stress were assessed

    via self-report during both baseline (e.g. the smoking peri-

    od) and the early phases of smoking cessation. Results:

    Among female participants, higher BMI was associated with

    lower levels of mood disturbance, perceived stress and de-

    pression. Similar analyses in male participants were non-sig-

    nificant. Conclusions: The results of the current study con-

    firm previous reports regarding the relationship of BMI andmood in women and extend these findings to the early stag-

    es of smoking cessation. Copyright 2009 S. Karger AG, Basel

    Received: April 22, 2008

    Accepted after revision: May 4, 2008

    Published online: September 1, 2009

    Mustafa alAbsi, PhDDepartment of Behavioral Sciences, University of Minnesota Medical School1035 University Drive, 236 Medical School Building

    Duluth, MN 55812-3031 (USA)Tel. +1 218 726 8332, Fax +1 218 726 7559, E-Mail [email protected]

    2009 S. Karger AG, Basel

    Accessible online at:www.karger.com/nps

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    BMI and mood. Nicotine may increase energy expendi-ture and suppress appetite, which may account for theinverse relationship between tobacco use and body weight[7, 8]. This finding, as well as nicotines ability to increasethe availability of serotonin in the brain [9], suggests thattobacco use may be an important consideration in studies

    on the connections between body mass and mood.Smoking cessation is inherently stressful and elicits

    negative mood. Traditionally, smokers with a history ofnegative affect often have more difficulty quitting [1012]. Further, previous work has suggested that this rela-tionship may be particularly important in women [7]. Xuet al. [13] reported that overnight nicotine abstinenceproduces more negative mood and craving among fe-males than in males, contributing to the greater likeli-hood of females to relapse during cessation attempts. Al-though weight concern has been noted as a reason whywomen are more reluctant to quit smoking [14], no stud-

    ies to date have found a relationship between BMI andlength of abstinence.

    The current study addresses these issues by examiningseveral indices of mood state in both male and femaleparticipants who enrolled in a larger study of smokingcessation. Data collection was timed to examine changesin mood during the early phases of abstinence [10]. Self-reported mood state was assessed: (1) during a periodwhen participants were smoking normally (i.e., the smok-ing period) and (2) in the initial phases of abstinencefrom nicotine (i.e., the ambulatory abstinence period).

    The current study had a dual focus. First, the authors

    sought to replicate and extend the findings of Oinonenand Mazmanian [3] by examining the relationship be-tween BMI and mood in a sample of male and femalecigarette smokers. The authors predicted that the report-ed inverse relationship of BMI and mood would be appar-ent among female participants compared to males. Theseanalyses focused on data from the smoking period.

    A second aim of the study examined whether or notbaseline BMI would predict mood alterations during theinitial phase of smoking abstinence. The authors soughtto determine whether or not the jolly fat effect mightconfer some mood protection for high BMI individuals

    during stress (e.g. smoking cessation).

    Methods

    ParticipantsNinety-two participants were recruited by advertisements

    placed in the university community as part of a larger ongoingstudy of stress and tobacco cessation. All participants signed con-

    sent forms approved by the Institutional Review Board of the Uni-versity of Minnesota and received monetary incentives for theirparticipation. Participants confirmed they had no recent historyof a medical or psychiatric disorder or medication intake (exceptoral contraceptives), and consumed 2 or fewer alcoholic drinksper day. To meet study requirements, participants smoked a min-imum of 10 cigarettes per day for at least 2 years and had a sig-

    nificant motivation to quit. Of those who initially qualified forthe study, 20 (8 males) were discontinued due to failure to attend1 or more subsequent appointments. Thus, data from 72 partici-pants (39 males) remained. Twelve female participants from thissample reported use of oral contraceptives.

    Participants began the study with the intention to schedule aspecific quit date on which they would stop smoking. For femaleparticipants, the quit date was scheduled during the follicularphase (day 310) of the menstrual cycle, as determined by self-re-port. Menstrual phase at the screening session was matched to thephase at subsequent laboratory visits. In the laboratory, carbonmonoxide (MicroCO; Micro Direct, Auburn, Me., USA) and sali-vary cotinine (EIA; DRG Diagnostics, Marburg, Germany) sam-ples were obtained for comparison purposes to verify smokingabstinence at a later date. Prior to their quit date, participants at-tended a 45-min educational session focusing on the negative ef-fects of smoking and the positive impact of cessation. No phar-macological or behavioral interventions were employed.

    MeasuresBackground variables were assessed during the baseline labo-

    ratory visit during the smoking period. These variables includedthe following: age, BMI, level of nicotine dependence [15], numberof cigarettes smoked per day and chronicity of tobacco use, de-pression, as measured via the CES-D (Center for EpidemiologicStudies Depression Scale) [16], and anxiety, as measured using theSpielberger State-Trait Anxiety Inventory [17].

    The dependent variables of interest included the following as-sessments. The Profile of Mood States (POMS) [18] and the Per-

    ceived Stress Scale [19] were administered on 2 occasions: (1) dur-ing the smoking period, and (2) after 24 h of abstinence from to-bacco (i.e., the ambulatory abstinence period).

    The POMS consists of a set of 65 five-point adjective ratingscales, with a 6-factor structure: tension-anxiety, anger-hostility,depression-dejection, vigor-activity, fatigue and confusion. A to-tal mood disturbance score (TMD) was derived from the POMSby summing the 6 subscales with vigor weighted negatively toproduce a possible range of scores from 40 to 192 [18, 20].

    The Perceived Stress Scale [19] is a 14-item scale that measuresthe amount of stress the participants perceive in their daily livesat the time of the assessment. For the ambulatory abstinence pe-riod, the time of the last cigarette was approximately 24 h prior tothe laboratory session. It is important to note that state measures

    obtained during the smoking period and ambulatory abstinenceperiod were collected in the participants natural environment.To screen for any anomalies in the participants environment atthe time of sample collection (e.g. traumatic incidents), informa-tion regarding the setting of data collection was documented;however, these data were not coded for analysis. Participants withsignificantly stressful environmental events were excluded fromfurther study and are not included in the final sample of 72 par-ticipants included in the current analyses.

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    Data AnalysisData were analyzed using SPSS version 16. Separate t tests were

    used to determine potential sex di fferences in age, years of educa-tion, BMI, level of nicotine dependence, number of cigarettessmoked per day, chronicity of tobacco use, as well as baseline lev-els of anxiety and depression.

    Initial Correlational AnalysesFor the first focus of the study, replication/extension of thejolly fat hypothesis, individual correlational analyses were con-ducted to determine the nature of the relationships between BMIto self-reported mood state, indexed via the POMS TMD scoreand perceived stress, measured using the Perceived Stress Scale.Separate analyses were conducted for males and females.

    To address issues related to the interaction of sex and BMI onmood and perceived stress scores, separate median splits of BMIscores were created for males and females. BMI (high or low) andsex (male or female) were used as grouping factors in separate2-factorial ANOVAs with the dependent variables of TMD scoreand perceived stress during the smoking period.

    Analysis of Change ScoresTo address the secondary aim of the study, examination of the

    potential protective effects of BMI on mood state alterations dur-ing smoking cessation, a second set of analyses were conducted.

    First, separate repeated-measures ANOVAs were conductedfor males and females to examine the differences between pre-(during the smoking period) and post-assessments (during theambulatory abstinence period) for TMD and perceived stress.

    Second, change scores were created by subtracting values col-lected at initial abstinence from values collected at the baselineassessment during the smoking period. Separate correlationalanalyses were used to examine the relationship between BMI andchange scores for TMD and perceived stress, partialling out val-ues collected during the smoking period. Data for males and fe-males were analyzed separately.

    Finally, separate ANCOVAs were conducted using BMI (me-dian split: high or low) and sex (male or female) as grouping vari-ables in the examination of change scores for TMD and perceivedstress. Values of the dependent variables obtained during thesmoking period were entered as covariates.

    Results

    Background VariablesMale and female participants were matched on age,

    years of education, level of nicotine dependence, number

    of cigarettes smoked per day, years of cigarette smoking,anxiety level, and depression level (table 1). Baseline lev-els of anxiety and depression were below the level of clin-ical significance. The BMIs of males were statisticallyhigher overall compared to females [t(70) = 2.20; p =003].

    Analyses were also performed to determine relation-ships between BMI and factors such as anxiety and de-

    pression. For women, BMI was negatively related to de-pression [r(33) = 0.46; p = 0.007] with a trend toward asignificant correlation with anxiety [r(33) = 0.33; p =0.06]. For men, these relationships were all highly non-significant [values of p1 0.83]. It is important to note thatmeasures of anxiety and depression are highly related tothe mood scores which were the variables of interest inthe current study.

    Initial Correlational AnalysesThese analyses addressed the first aim of the study,

    that is, the replication and extension of the previous find-

    ings [3] by examining the relationship between BMI andmood in a sample of male and female cigarette smokers.

    For females, BMI was significantly related to TMDscore during the smoking period [r(33) = 0.42; p = 0.02].Women with higher BMIs reported less mood distur-bance (fig. 1). Among males, no significant relationshipwas found between BMI and TMD [r(39) = 0.09; p =0.58].

    BMI was significantly related to perceived stress dur-ing the smoking period among women [r(33) = 0.35;p = 0.045]. Women with higher BMIs reported less per-ceived stress (fig. 1). However, this relationship was not

    significant among male participants [r(39) = 0.02; p =0.89].

    ANOVA was used as a confirmatory method for theanalysis of main and interactive effects of sex and BMIgroup. For analyses of TMD, main effects of sex [F(1,68) = 0.69; p = 0.41] and BMI group [F(1, 68) = 0.22; p =0.64] were not significant; however, a significant interac-tion of BMI group and sex was noted for TMD scores

    Table 1. Background characteristics of male and female partici-pants

    Men(n = 39)

    Women(n = 33)

    Age, years 36.9814.0 34.9814.6

    Education, years 14.383.0 14.582.2BMI* 25.984.0 23.983.9Nicotine dependence1 5.682.1 5.482.2Cigarettes/day 19.886.5 19.187.7Smoking chronicity, years 14.482.3 10.189.3Trait anxiety, STAI score 37.289.0 37.9810.3Depression, CES-D score 10.788.8 15.1810.2

    STAI = Spielberger State-Trait Anxiety Inventory. * p < 0.05.1 Measured by Fagerstrom Test for Nicotine Dependence.

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    during the smoking period [F(1, 68) = 5.05; p = 0.03]. Pair-wise comparison revealed significant sex differences in

    TMD during the smoking period within the low BMIgroup [t(34) = 2.41; p = 0.02], in which females report-ed higher levels of total mood disturbance relative tomales.

    For analysis of perceived stress, main effects of sex[F(1, 68) = 2.84; p = 0.10], BMI group (F(1, 68) = 1.96; p =0.17) and their interaction [F(1, 68) = 2.70; p = 0.11] dur-ing the smoking period were non-significant.

    Analysis of Change ScoresTo address the second aim of the study, determining

    whether or not baseline BMI would predict mood altera-tions during the initial phase of smoking abstinence, aseparate set of analyses were conducted.

    First, separate repeated-measures ANOVAs were con-ducted for males and females to examine the differencesbetween pre- (during the smoking period) and post-as-sessments (during the ambulatory abstinence period) forTMD and perceived stress.

    5

    Perce

    ive

    dstress

    score

    (smo

    kingperio

    d)

    10

    15

    20

    25

    30

    35

    15 20 25 30 35

    BMI

    r(33) = 0.35; p = 0.045

    0

    Perce

    ive

    dstress

    score

    (smo

    kingperio

    d)

    35

    20 35

    BMI

    r(39) = 0.02; p = 0.89

    5

    10

    15

    20

    25

    30

    25 30

    TMD(smo

    kingperiod

    )

    0

    120

    15 20 25 30 35

    BMI

    r(33) = 0.42; p = 0.02

    30

    60

    90

    Women

    20

    TMD(smo

    kingperiod

    )

    120

    20 35

    BMI

    r(39) = 0.09; p = 0.58

    25 30

    Men

    0

    20

    40

    60

    80

    100

    Fig. 1. TMD and perceived stress scores during the smoking period in men and women. Statistical ly significantrelationships were noted for female, but not male, participants.

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    Womens TMD values during the smoking period(mean = 25.15, SD = 29.03) and during the ambulatoryabstinence period (mean = 16.09, SD = 36.38) demon-strated a trend toward a significant difference (p = 0.09),and mens TMD values during the smoking period(mean = 19.73, SD = 34.47) and the ambulatory absti-

    nence period (mean = 18.08, SD = 36.44) did not differsignificantly (p = 0.60).

    The perceived stress scores of women during the smok-ing period (mean = 16.61, SD = 6.22) and during the am-bulatory abstinence period (mean = 15.66, SD = 7.25) didnot differ significantly [F(1, 31) = 1.18; p = 0.29]. How-ever, the difference between mens perceived stress valuesduring the smoking period (mean = 14.08, SD = 6.34) andthe ambulatory abstinence period (mean = 15.47, SD =5.93) did reach statistical significance [F(1, 37) = 4.19; p =0.048]. Men perceived themselves as being significantlymore stressed during the ambulatory abstinence period

    relative to the smoking period.Second, separate correlational analyses partialling out

    values collected during the smoking period revealed asignificant relationship between BMI and TMD changescores for women [r(30) = 0.38; p = 0.03] but not for men[r(35) = 0.009; p = 0.96]. For measures of perceived stresschange, no significant relationships were noted betweenperceived stress and BMI for females [r(29) = 0.15; p =0.41] or males [r(35) = 0.06; p = 0.72].

    Finally, analysis via ANCOVA revealed nonsignif icanteffects of sex [F(1, 66) = 3.91; p values 1 0.13] on TMDchange scores. However, a significant effect of BMI group

    was noted [F(1, 66) = 4.27; p = 0.04], in which the low BMIgroup exhibited negative change scores (i.e., stress duringthe smoking period was higher than stress during theambulatory abstinence period) and the high BMI groupexhibited positive change scores (i.e., stress during thesmoking period was lower than stress during the ambula-tory abstinence period). The interaction of BMI groupand sex was also non-significant [F(1, 66) = 1.38; p =0.25].

    Analysis of perceived stress via ANCOVA revealednon-significant effects of sex [F(1, 65) = 2.60; p = 0.11],BMI group [F(1, 65) = 0.42; p = 0.52] and their interaction

    [F(1, 65) = 0.02; p = 0.90].

    Discussion

    The first aim of the current study was the replicationand extension of the jolly fat hypothesis. The currentfindings support this hypothesis among female partici-

    pants, with an inverse relationship between obesity andmood (TMD) and obesity and perceived stress during thesmoking period in females, but not males (fig. 1). Theserelationships were investigated initially using correla-tional analyses, and ANOVAs were used as a confirma-tory follow-up method. Given the typical increase in BMI

    with age, as well as the potentially increased relevance forthe jolly fat hypothesis in older versus younger women,additional analyses explored the relationship betweenBMI and mood while controlling for age. Partial correla-tions failed to replicate the significant relationship be-tween BMI and mood disturbance among women duringthe smoking period [r(30) = 0.26; p = 0.15]. This is a par-ticularly important point given that previous studies ofthe jolly fat hypothesis have focused on young women[3], whereas the age range of women in the current studywas quite broad (1868 years). Thus, a number of par-ticipants in the current study may have reached meno-

    pause prior to participation in the study, an issue whichcould have significant implications for the hypothesizedinvolvement of estrogen in the jolly fat effect [3].

    The finding of a trend toward differential sex effectsin the relationship between body mass and mood distur-bance is a unique addition to the literature. Further, dis-entangling gender differences in the jolly fat phenome-non may also serve to extend and clarify previous workby Roberts et al. [21], who failed to find a significant pos-itive association between mood and body weight in alarge epidemiological study.

    The mechanisms underlying this sex-specific effect

    are not known. However, low levels of circulating sex ste-roids and correspondingly low levels of the neurotrans-mitter serotonin have been previously associated with anincreased risk of depression and/or mood disturbance [2,79]. It is also important to note that serotonin is also oneof several key neurotransmitter systems that play a rolein nicotine withdrawal [22]. Further, although estrogenlevels were not directly addressed in the current study,our data support the notion presented by Oinonen andMazmanian [3] that increased estrogen availability in fe-males of greater body mass may be a factor associatedwith decreased negative mood in female participants who

    have larger BMIs. Thus, one might expect to f ind that in-creased BMI and estrogen levels in women function asprotective factors against the negative mood states thatare often observed in the early stages of abstinence fromnicotine. However, as stated previously, it is important tonote that the reason for higher estrogen levels in personswith high levels of fatty tissue would also apply to males;thus, the estrogen hypothesis does not completely explain

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    the presence of sex differences in the data. Additionalresearch is needed to specifically address the potentialmechanisms underlying sex differences in the relation-ship between BMI and mood.

    Although it is clear that additional research is war-ranted, a recent report by Connan et al. [23] provides a

    relevant framework for the discussion of our findings.The authors observed increased estrogen among re-fedanorexic women and speculated that these changes wererelated to increased levels of leptin, a peptide hormoneprimarily synthesized and secreted by adipocytes [24].These findings, although not directly related to the cur-rent study, support the notion of an interrelationship be-tween body mass and estrogen levels among female par-ticipants.

    Clinical ImplicationsPrevious studies have shown that women often relapse

    to cigarette smoking after periods of abstinence for differ-ent reasons than do men [25, 26]. One of the reasons thatwomen frequently start smoking and find it hard to quitis because nicotine may be equated with the notion ofweight loss for women; some studies have suggested thataddressing issues of body image among such individualsmay help to improve smoking cessation treatments [14].Thus, the findings of the current study could conceivablybe used as part of an educational program to help womendeal with issues of weight and body image and the con-nection of these phenomena to tobacco dependence.

    LimitationsAlthough these findings represent a significant con-

    tribution to the ongoing literature, a number of limita-tions remain to be addressed in future research. First,given the naturalistic design of the current study, no bal-anced order could be achieved between the data gatheredwhen participants were still smoking and the data gath-ered after smoking cessation. As a result, the findings ofthe current study should be interpreted within a natural-istic framework rather than in the context of a more strin-gent experimental design.

    Secondly, although information regarding perceived

    stress levels was available in the current study, specificstress levels related to smoking cessation alone were notcollected. It may be argued that the difference betweeneveryday stress before versus after smoking cessation isan indirect reflection of smoking-related stress levels,and a more sensitive measurement of smoking cessation-related stress could be a relevant focus for future re-search.

    The collection of additional biological samples foranalysis of estrogen and leptin levels would potentiallyprovide insight into the mechanisms underlying the jol-ly fat effect. Via BMI, our data indirectly support thejolly fat hypothesis; however, the aforementioned assaysare needed to substantiate the connection between body

    fat, estrogen levels and mood stability among women.Further, such sensitive measures may detect subtle rela-tionships between body fat and mood that may not reachstatistical significance in analyses using height andweight. Such follow-up studies are currently underwayin our laboratory.

    In addition, it is well-known that participants self-perception of body size and shape impacts mood andoverall health [27], and some studies suggest that bodyimage may play a role in suicidal ideation, particularlyamong adolescents [28]. Gender differences in body im-age are also frequently apparent [29, 30]. The extent to

    which these factors may have influenced the current find-ings is unknown, but this remains a target of ongoingresearch.

    Further, perceptions of body shape and size, as well asattitudes toward obesity, may be socially and culturallyspecific [31, 32]. For instance, being born into and/or ac-culturating to modern Western culture may increase thelikelihood that overweight/obese individuals will inter-nalize negative messages about their appearance, a phe-nomenon which may lead to depressive symptomatology[33]. As identified previously, the participant sample ofthe current study was predominantly born within the

    United States and of Caucasian origins with similar so-cioeconomic backgrounds. Interestingly, this participantsample composition is typical of previous studies of thejolly fat hypothesis, suggesting that the factors associ-ated with increased positive mood among women withhigh BMI levels is in opposition to the notion that west-ernized cultures internalize negative messages regardingobesity. Thus, future studies with an emphasis on the po-tential social and cultural influences on the interactionsof body mass and mood are needed to clarify this issue,particularly among female participants.

    Conclusion

    Our results support and extend the jolly fat hypoth-esis with respect to female participants undergoing theinitial phases of smoking cessation. In women, but not inmen, greater BMI was significantly associated with lowerlevels of mood disturbance. Although the mechanisms

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    underlying this gender-specific effect remain to be eluci-dated, predictions focus on the positive relationship be-tween BMI and subsequent levels of estrogen and sero-tonin. Future studies should consider more sensitivemeasures of body fat content and biochemical signalingas well as culturally specific differences in the perception

    of obesity.

    Acknowledgements

    The authors thank Angie Harju, Laurie Franks and HuongTimp for their assistance with data collection and management.We thank Clemens Kirschbaum of the University of Dresden,Germany, for his assistance with the project. This research wassupported in part by grants from the National Cancer Institute

    (CA88272) and National Institute on Drug Abuse (DA013435 andDA016351).

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