Original Article

European Journal of Clinical Nutrition (2012) 66, 1247–1253; doi:10.1038/ejcn.2012.70; published online 27 June 2012

Epidemiology

Fruit and vegetable intake and smoking cessation

T Poisson1, J Dallongeville1, A Evans2, P Ducimetierre3, P Amouyel1, J Yarnell2, A Bingham3, F Kee2 and L Dauchet1

  1. 1Service d'Epidémiologie et Santé Publique, Lille, France
  2. 2UKCRC Centre of Excellence for Public Health (NI), Queen’s University, Belfast, UK
  3. 3INSERM, Villejuif, France

Correspondence: Dr L Dauchet, Institut Pasteur de Lille, INSERM U744, 1 rue du Pr Calmette, F-59019 Lille Cedex, France. E-mail: luc.dauchet@pasteur-lille.fr

Received 12 January 2012; Revised 11 May 2012; Accepted 17 May 2012
Advance online publication 27 June 2012

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Abstract

Background/Objectives:

 

In cohort studies, fruit and vegetable (F&V) intake is associated with lower cardiovascular diseases (CVDs). Former smokers often have a higher F&V intake than current smokers. If a high intake of F&V precedes smoking cessation, the latter may explain the favorable association between F&V intake and CVD among smokers. The objective was to assess whether higher F&V intake precedes smoking cessation.

Subjects/Methods:

 

The study population comprised 1056 male smokers from Lille (France) and Belfast (Northern Ireland) aged 50–59 years on inclusion in 1991. At baseline, participants completed self-administered questionnaires related to smoking habits, demographic, socioeconomic factors and diet. At the 10-year follow-up, smoking habits were assessed by mailed questionnaire.

Results:

 

After 10 years, 590 out of 1056 smokers had quit smoking (70.7% of smoker in Lille and 37.8% in Belfast). After adjusting for center, consumption of F&V was associated with quitting (odds ratio (OR) for high versus low F&V intake: 1.73; 95% confidence interval (CI): (1.22–2.45); P-trend=0.002). After further adjustment for sociodemographic factors, body mass index and medical diet, the association was still statistically significant (OR: 1.59; 95% CI (1.12–2.27); P-trend=0.01). In a model fully adjusted for age, smoking intensity, alcohol consumption and physical activity, the association was no longer significant (P=0.14).

Conclusions:

 

Higher F&V intake precedes smoking cessation. Hence, smoking cessation could affect the causal interpretation of the association between F&V and CVD in smokers.

Keywords:

fruit; vegetable; cardiovascular disease; smoking; confounding factors (epidemiology); smoking cessation

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Introduction

Most of the evidence for a relationship between consumption of fruit and vegetables (F&Vs) and cardiovascular disease (CVD) has been generated in cohort studies. The associations are usually weak and not always statistically significant. Meta-analyses have evidenced moderate associations.1, 2, 3, 4, 5, 6 Given the moderate strength of the relationship, the relative impact of residual confounding is elevated, which hampers the interpretation of a causal relationship.7, 8 In fact, F&V consumers differ from nonconsumers in many respects, such as educational level, social and economic status,9 smoking habits and vitamin supplement intake.5 These characteristics are not always adjusted for in cohort studies. Indeed, to our knowledge, the association between F&V intake and the propensity to give up smoking has never been investigated in a prospective study.

Smoking is a major risk factor for CVD.10 The risk associated with smoking decreases rapidly and reaches that of never-smokers within 2–5 years of quitting.10, 11, 12, 13 Several studies have reported larger reductions in the coronary heart disease risk for F&V consumption in smokers than in nonsmokers.14, 15, 16 The causal hypothesis underlying this finding is that consumption of F&V lowers the risk by providing sufficient amounts of antioxidant vitamins to smokers exposed to oxidative stress. However, the protective effect of antioxidant vitamins has not been confirmed in clinical trials.16 An alternative hypothesis is that smokers who consume large amounts of F&V are more health conscious than smokers who eat F&V rarely and thus are more likely to give up smoking. Most of the cohort studies, however, only analyzed smoking habits at baseline with risk of CVD and did not take into account changes in smoking habits during follow-up. Therefore, the association may be confounded by smoking cessation.

Several studies have shown that nutritional behavior is linked to smoking habits.17 In general, current smokers have less healthy food habits than never-smokers. In contrast, former smokers tend to adopt better food habits than current smokers and are positioned midway between current smokers and never-smokers in terms of diet quality in general18, 19 and F&V intake in particular.20, 21 However, the cross-sectional, observational nature of most studies has prevented researchers from establishing whether or not these nutritional habits predated the smoking cessation.

We hypothesized that the nutritional habits of smokers who plan to quit smoking (and then actually do so) are healthier than those of smokers who maintain their smoking habits. Hence, the goal of the present study in smokers was to examine the putative association between initial F&V intake and smoking cessation after 10 years of follow-up.

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Materials and methods

Population recruitment

Briefly, the PRIME study was established in 1991 with the populations from four WHO-MONICA centers in Belfast (Northern Ireland), Lille (Northern France), Strasbourg (Eastern France) and Toulouse (South-Western France). The goal was to recruit 2500 men aged 50–59 years in each center. The PRIME study was approved by the appropriate local independent ethics committees and conducted in accordance with the current legislation in France and Northern Ireland. From the original PRIME cohort, two centers only, Lille and Belfast, followed up smoking habits of participants until 10 years. Thus, the current analyses were carried out only in smokers at baseline from Lille and Belfast.

Questionnaire

At baseline, self-administered questionnaires related to demographic and socioeconomic factors and diet were completed at home by the participants and then checked in the latter’s presence by survey staff at the investigating center. Data related to educational level, employment status, personal and family medical history, tobacco and alcohol consumption and physical activity during leisure time were also collected. The personal history of cardiovascular risk factors was assessed by asking the subject to state whether a medical doctor had ever reported a given risk factor, followed by a question on past and present medical treatments. Subjects on a diet for medical reasons (for example, because of high blood pressure, dyslipidemia, diabetes or obesity) were identified by specific questions. Anthropometric parameters (height, weight and blood pressure values) were measured using standardized methods.22, 23

Smoking status was determined from the answers to questions on present and past habits. Subjects were classified into three categories: never-smokers, former smokers and current smokers. Current smokers were asked to state their age at first cigarette and to give information on the number and type of cigarettes, cigars or pipes smoked per day over the previous 5 years.

Dietary assessment

Alcohol consumption was assessed by means of a questionnaire in which the subject reported the mean consumption in standard serving for each beverage of wine, beer, cider and spirits on each day of the week. Then, standard units were translated to ml of alcohol per day by summing the alcohol content of each beverage serving.

Dietary information on the frequency of F&V intake was obtained for four categories of F&V (‘fresh citrus fruits’, ‘other fresh fruits’, ‘raw vegetables’ and ‘cooked vegetables’, all excluding potatoes and legumes). In a face-to-face home interview, subjects were asked to indicate the usual frequency of consumption of a standard portion of fruit and/or vegetables at the time of interview. The frequencies of ‘fruit’, ‘vegetable’ and ‘F&V’ intake were calculated as the sum of the number of servings per day of fruit and/or vegetables. Consumption classes were defined according to a cutoff used in previous articles24 (less than or equal to1.57, 1.6–2.57 and greater than or equal to2.6 serving per day for F&V; less than or equal to0.57, 0.64–1.14 and greater than or equal to1.29 serving per day for fruit; and less than or equal to0.79, 1–1.29 and greater than or equal to1.5 serving per day for vegetable).16 In a previous analysis, the frequency of F&V consumption measured with this questionnaire was found to be associated with plasma vitamin concentrations. The frequency of fruit intake was correlated with beta-cryptoxanthin (r=0.32, P<0.005) and vitamin C (r=0.33, P<0.004) levels. Similarly, the frequency of citrus fruit intake was correlated with beta-cryptoxanthin (r=0.34, P<0.002) and vitamin C (r=0.37, P<0.0007) levels. Finally, the frequency of vegetable intake was correlated with alpha-carotene (r=0.26, P<0.03), beta-carotene (r=0.29, P<0.02), beta-cryptoxanthin (r=0.32, P<0.04) and vitamin C (r=0.24, P<0.04).24

Follow-up

In the Belfast cohort, the participant’s smoking habits were investigated by means of a questionnaire sent by post after a 10-year follow-up period (in 2001). In Lille, a postal questionnaire was sent to participants every year during the 10-year follow-up period. ‘Quitters’ were defined as nonsmokers in the last questionnaire. Smoking habits were not investigated in Toulouse and Strasbourg during follow-up; thus, only subjects from Lille (689) and Belfast (871) were included in the analysis. Among these 1560 subjects, we excluded those with known history of angina or myocardial infarction (n=117) or with missing data at baseline—dietary assessment or adjustment variables (n=112)—resulting in 1331 subjects. Among them, 1056 completed follow-up at 10 years for smoking status, resulting in a 79% response rate. The characteristics of nonresponders are presented in Supplementary Table 1.

Statistical analysis

Student’s t-test and the Chi-square test were used to compare quantitative and qualitative variables, respectively. Alcohol consumption was coded as a class variable, as we expected a nonlinear association. Because the exact time of smoking cessation was not recorded during follow-up, it was not possible to use survival analysis. Thus, we compared the baseline characteristics, including F&V intake, of quitters and nonquitters at 10 years by logistic regression. Three models were used, with different adjustments: (1) center (Lille, Belfast); (2) model 1 plus age (year), marital status (single, married), educational level (number of years in full-time education), social category (upper, intermediate and lower), employment status (active and not active), body mass index (BMI kg/m2) and prescription of a diet for medical reasons (hypertension, hypercholesterolemia or diabetes); and (3) model 2 plus behavioral data such as age at first cigarette, number of cigarettes, cigars or pipes smoke daily, alcohol consumption (teetotalers, less than or equal to225, >225, less than or equal to460.8 and >460.8ml/w) and physical activity (none, light, moderate and intense). Sensitivity analyses were performed excluding subjects with at least one cardiovascular risk factor (diabetes, hypertension and hypercholesterolemia) and to assess the impact for missing data. To this end, we used multiple imputation for quitting smoking at 10 years using the Proc Mi and Proc Mianalyze procedure from SAS. All statistical analyses were performed with the SAS software (version 9.1, SAS Institute, Cary, NC, USA).

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Results

The smokers’ demographic and lifestyle characteristics at baseline are summarized according to F&V intake and center in Table 1. In Lille, high F&V consumers were lighter smokers (P<0.01) and drank less alcohol (P<0.0001). In Belfast, high F&V consumption was associated with higher educational level (P<0.01), higher social category (P<0.001), greater physical activity and lower tobacco (P<0.0001) and alcohol (P<0.03) consumption. High consumers were more likely to be working (P<0.01) and on a diet for medical reasons (P<0.01).


During the follow-up period, 590 of the initial 1056 smokers gave up smoking (70.7% of the smokers in Lille and 37.8% of those in Belfast). Characteristics at baseline of quitters and nonquitters are summarized in Table 2. Quitters consumed more F&V (P<0.01) and fruit alone (P<0.01) but not vegetables alone. Quitters were older (P<0.0001) and had a lower alcohol intake (P<0.0001). In Lille, quitters smoked fewer cigarettes a day (P<0.0001) and had begun to smoke at a later age (P=0.03). These associations were not observed in Belfast (P interaction <0.05 in both cases).


Table 3 reports the multivariate associations between F&V consumption and quitting. After adjusting on center (model 1), consumption of F&V was associated with quitting. The odds ratio (OR) for increment of one time per day was 1.21 (95% confidence interval (CI) 1.07–1.37; P-trend=0.002). The corresponding OR for higher consumers versus lower consumers was 1.73 (95% CI (1.22–2.44)). After further adjustment for sociodemographic factors, diet for medical reasons and BMI (model 2), the association remained statistically significant (OR for one time per day increment was 1.17 (95% CI 1.04–1.32); P-trend=0.01). Finally, after further adjustment for smoking behavior (intensity and age at first cigarette), alcohol consumption and physical activity (model 3), the association between F&V intake and quitting was no longer significant (OR for one time per day increment was 1.10 (95% CI 0.97–1.25); P-trend=0.14). Quitting was significantly associated with the number of cigarettes smoked and with alcohol consumption.


Fruit consumption was significantly associated with quitting in model 1 (Table 4). The OR for increment of one time per day was 1.28 (95% CI 1.07–1.54; P-trend<0.01). This association was attenuated by further adjustment (model 2: OR for one time per day increment was 1.25 (95% CI 1.04–1.50; P-trend=0.02) and was no longer significant in the fully adjusted model. No significant associations were observed in any of the models with regard to the consumption of vegetables only.


In the sensitivity analysis including only subjects without any cardiovascular risk factor (n=365), the associations were very slightly strengthened. The OR for increment of one time per day F&V intake was 1.28 (95% CI 1.05–1.58), 1.21 (95% CI 0.98–1.50) and 1.19 (95% CI 0.96–1.50) for model 1, 2 and 3, respectively. All interactions with cardiovascular risk factors were statistically nonsignificant (all P>0.30). Analyses were repeated using multiple imputation for missing data on quitting smoking (n=1331) The results are presented in Supplementary Table 2. The OR for increment of one time per day F&V intake was 1.18 (95% CI 1.05–1.33), 1.15 (95% CI 1.02–1.30) and 1.08 (95% CI 0.96–1.22) for model 1, 2 and 3, respectively.

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Discussion

The present study’s main finding is that smokers who quit smoking had a higher F&V consumption at the time they were still smoking than those who maintain their smoking habit. This suggests that in cohort studies, the relationship between F&V intake and cardiovascular risk may be overestimated because of confounding by smoking cessation.

Smoking cessation and F&V intake were both associated with a later age at first cigarette, lower levels of tobacco use and a moderate alcohol intake, suggesting that both parameters were part of a healthier attitude. After adjustment for the later variables, the relationship between smoking cessation and F&V consumption was no longer statistically significant, suggesting that F&V intake is part of a broader, healthier attitude held by smokers who intend to give up the habit. This interpretation is consistent with the observation that health awareness is the main reason for giving up smoking.25

The practical consequence of this observation is that smoking cessation by participants who are smokers at the time of inclusion in cohort studies is a confounder of the association between F&V consumption and cardiovascular risk. This is particularly true for middle-aged male smokers, where the cessation rate is particularly high (over 50% in the present study). Of 31 cardiovascular nutrition cohort studies,14, 15, 24, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54 29 were adjusted for smoking status. Only the Nurses’ Health Study and the Health Professionals’ Follow-up Study15 have accounted for changes in smoking habits (recorded every 2 years during the follow-up period). In this pooled cohort, modest but significant associations between F&V intake and CVD were observed. However, because smoking cessation was recorded at 2-year intervals, this interval is large enough to be affected by confounding by smoking cessation. Adjustment for the number of cigarettes and alcohol intake suppresses the association between F&V and smoking cessation, which could partially attenuate the confounding effect of smoking cessation in cohort studies. The quantity of tobacco smoked was accounted for in only 16 of the 31 cardiovascular nutrition cohorts that we reviewed. Thus, in the remaining studies, the association between F&V intake and CVD may have been overestimated in smokers because of confounding related to smoking cessation.

In models 1 and 2, smoking cessation was associated with fruit intake but not vegetable intake. Similarly, fruit intake (but not vegetable intake) is associated with favorable cardiovascular outcomes in cohort studies.1, 2, 3, 4 It is not known whether these two observations are linked, however, they are consistent with the hypothesis that a part of the association observed between F&V intake and cardiovascular risk in cohort studies may be explained by confounding of smoking cessation. In addition to being a cardiovascular risk factor, smoking is a major risk factor of cancer. Given that food habits have also been associated with the risk of cancer, the same question arises as to whether smoking cessation could confound this relationship. However, this is less likely, in view of a much slower decrease in the cancer risk after smoking cessation.55

The present study had several limitations. The food frequency questionnaire was too simple to provide an accurate, quantitative assessment of intake. Hence, the results of the present study should be considered as an analysis of relationships with the frequency of F&V intake, rather than with the absolute amount. However, in a validation report on the food frequency questionnaire used here, F&V intake was correlated with serum vitamin level.24 Missing data for quitting smoking at 10 years could have biased the results. However, imputation for missing data provided similar results. ORs were slightly modified but trend remained similar, suggesting that missing data do not strongly bias the results of the present study. The present study was conducted in men in the 50–59-year age group only. Thus, the results may not be applicable to other age groups and/or to women (owing to differences in the prevalence and characteristics of men and women smokers, in particular). In the present study, smoking cessation status was assessed during follow-up in most centers. However, the single data point after 10 years of follow-up in Belfast prevents analyzing delay of quitting smoking.

In conclusion, higher F&V intake precedes smoking cessation in current smokers. This suggests that smoking cessation could explain, at least partially, the lower CVD rates among F&V consumers that have been observed in cohort studies, and thus affect the causal interpretation of the association. Adjustment for other behavioral variables decreased this confounding, highlighting the necessity to carefully adjust for smoking cessation or behavioral indicators of healthy lifestyle when assessing the relationship between F&V intake and CVD risk.

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Conflict of interest

The authors declare no conflict of interest.

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Acknowledgements

We thank the following organizations for facilitating the recruitment of the PRIME subjects: the Health ScreeningCentres coordinated by the Social Security Department in Lille (Institut Pasteur), Strasbourg, Toulouse and Tourcoing; the Occupational Medicine Services in the Haute-Garonne county and the Strasbourg Urban Area; the Association Interenterprises des Services Medicaux du Travail de Lille et environs; the Comité pour le Développement de la Médecine du Travail; the Mutuelle Générale des PTT du Bas-Rhin; the Laboratoire d’Analyses de l’Institut de Chimie Biologique de la Faculté de Médecine de Strasbourg; and the Department of Health (NI) and the Northern Ireland Chest Heart and Stroke Association. We also thank the external members of the event validation committees (Professor L Guize, Dr CMorrison, Dr M-T Guillanneuf and Professor M Giroud) and the Alliance Partnership Program for its financial support. The PRIME study was supported by grants from INSERM, the Lille Pasteur Institute and the Merck, Sharpand Dohme-Chibret Laboratory.

Supplementary Information accompanies the paper on European Journal of Clinical Nutrition website

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