Effects of smoking, obesity and physical activity on the risk of type 2 diabetes in middle-aged Finnish men and women

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1 Journal of Internal Medicine 2005; 258: doi: /j x Effects of smoking, obesity and physical activity on the risk of type 2 diabetes in middle-aged Finnish men and women K. PATJA 1, P. JOUSILAHTI 1,2, G. HU 1,2, T. VALLE 1, Q. QIAO 1,2 & J. TUOMILEHTO 1,2 From the 1 Department of Epidemiology and Health Promotion, National Public Health Institute; and 2 Department of Public Health, University of Helsinki, Helsinki, Finland Abstract. Patja K, Jousilahti P, Hu G, Valle T, Qiao Q, Tuomilehto J (National Public Health Institute and University of Helsinki, Helsinki, Finland). Effects of smoking, obesity and physical activity on the risk of type 2 diabetes in middle-aged Finnish men and women. J Intern Med 2005; 258: Objective. To examine the association of cigarette smoking with the risk of type 2 diabetes and to find out whether the association is modified by obesity and physical activity. Design and subjects. A prospective study comprising men and women aged years without a history of diabetes, coronary heart disease or stroke at baseline. Data on incident cases of diabetes were ascertained through the nationwide Drug Register and the Hospital Discharge Register. During the mean follow-up of 21 years 2770 subjects were diagnosed with type 2 diabetes. The Cox proportional hazards model was used to estimate the effect of smoking and other factors on the risk of type 2 diabetes. Results. Smoking had a graded association with the risk type 2 diabetes, and it remained significant after controlling for age and major risk factors. The multifactorial-adjusted (age, study year, education, body mass index (BMI), systolic blood pressure, physical activity and coffee and alcohol drinking) hazard ratio was 1.22 [95% confidence interval (CI) ] amongst men smoking less than 20 cigarettes per day and 1.57 (95% CI ) amongst men smoking 20 cigarettes per day or more. In women the corresponding hazard ratios were 1.46 (95% CI ) and 1.87 (95% CI ) respectively. Smoking increased the risk of type 2 diabetes at all levels of BMI and physical activity. Conclusion. Smoking is a risk factor for type 2 diabetes independently of BMI and physical activity. Prevention of smoking should be encouraged as a part of efforts to reduce the risk of type 2 diabetes, and it will result in other health benefits, too. Keywords: alcohol, physical activity, obesity, smoking, type 2 diabetes. Introduction Type 2 diabetes is a chronic disease with a high and still increasing prevalence worldwide. Obesity and physical inactivity are the major modifiable risk factors for type 2 diabetes [1]. Several studies have shown that high blood pressure and low socioeconomic status are also associated with the increased risk [2, 3]. Recent studies have suggested that coffee drinking may decrease the risk of type 2 diabetes [4]. In studies published since 1990, current smokers have a 1.2- to 2.6-times higher risk of type 2 diabetes than nonsmokers [5 10], with one exception of a lower risk for smokers related to survival bias [11]. The risk of type 2 diabetes seems to increase with pack-years in a graded manner. Quitting smoking decreases the risk of type 2 diabetes to close to that in nonsmokers, but the risk still remains higher after 10 years since quitting smoking [7]. The aim of the present study was to examine the association of cigarette smoking with the risk of type 2 diabetes and also to find out whether the association is modified by obesity and physical activity. Research design and methods Subjects Baseline surveys were carried out in two eastern Finnish provinces, north Karelia and Kuopio, in 356 Ó 2005 Blackwell Publishing Ltd

2 SMOKING AND THE RISK OF TYPE 2 DIABETES , 1977, 1982, 1987 and The survey was expanded to the Turku-Loimaa region in southwestern Finland in 1982 and the Helsinki capital area in In the five surveys, the sample included subjects who were aged years. In 1972 and 1977, a randomly selected sample of 6.6% of the population born between 1913 and 1947 was drawn. Since 1982, the sample was stratified by area, gender and 10-year age group according to the WHO MONICA (MONItoring trends and determinants of CArdiovascular disease) protocol [12]. Because no significant interaction between study year and smoking on the risk of type 2 diabetes was found, the 1972, 1977,1982, 1987 and 1992 cohorts were combined in this analysis. Subjects who participated in more than one survey are included only in their first survey cohort. The total sample size of the six surveys was The participation rate varied from 74% to 88%. The final sample comprised men and women excluding subjects diagnosed with coronary heart disease or stroke (n ¼ 1444), subjects with known diabetes (n ¼ 804) at baseline, subjects who had type 1 diabetes (n ¼ 64) at baseline or during follow-up, and subjects with incomplete data on smoking or any other required factors (n ¼ 1222). These surveys were conducted according to the ethical rules of the National Public Health Institute and the investigations were carried out in accordance with the Declaration of Helsinki. Measurements A self-administered questionnaire was sent to the participants to be completed at home. The questionnaire included questions on medical history, socioeconomic factors, coffee and alcohol consumption, physical activity and smoking habits. Education level, measured as the total number of school years, was divided into birth cohort-specific tertiles. Coffee consumption was determined by the number of cups of coffee the participants drank daily [4]. As questions on alcohol consumption were different between the first two surveys (1972 and 1977) and the later surveys, alcohol consumption was categorized into two categories: yes and no. Using a set of standardized questions the participants were classified into three smoking categories: current smokers, ex-smokers and lifelong nonsmokers. Current smokers were categorized into those whose daily smoking either was less than 20 or more than 20 cigarettes. In this analyses those ex-smokers who had not smoked for 6 months or more were considered as exsmokers, and those who had quit within 6 months were considered as current smokers. Questions about occupational and leisure time physical activity were also asked and the participants were classified into two categories: low, or moderate/active. As our previous study has shown that moderate and high occupational or leisure time physical activity independently and significantly reduces risk of type 2 diabetes, occupational and leisure time physical activity were merged and regrouped into three categories in some analyses: (i) low was defined as subjects who reported light levels of both occupational and leisure time physical activity; (ii) moderate was defined as subjects who reported moderate or high level of either occupational or leisure time physical activity; (iii) high was defined as subjects who reported moderate or high level of both occupational and leisure time physical activity [13]. At the study site, specially trained nurses measured height, weight, and blood pressure using a standardized protocol according to the WHO MON- ICA project. Blood pressure was measured from the right arm of the participant who was seated for 5 min before the measurement and used a standard sphygmomanometer. Weight (rounded to the nearest 0.1 kg) and height (rounded to the nearest 0.5 cm) were measured in light clothing and without shoes. Body mass index (BMI) was calculated as weight (kg) divided by the square of the height (m). In stratified analyses, the subjects were classified in three BMI categories: <25 (normal weight), (overweight) and >30 kg m )2 (obese). Diagnosis of diabetes Incident cases of diabetes were ascertained from the National Hospital Discharge Register and the National Social Insurance Institution s Drug Register. Register data were linked to the risk factor survey data with the unique identification numbers assigned to every resident of Finland. Antidiabetic drugs prescribed by a doctor are free of charge in Finland. Reimbursement is subject to approval of the application by the Social Insurance Institution that includes the review of the case history. The doctor confirms the diagnosis of diabetes on the basis of the World Health Organization criteria and clinical

3 358 K. PATJA et al. symptoms. All patients receiving free medication (either oral antidiabetic agents or insulin) are entered into a register maintained by the Social Insurance Institution. Data collection was completed using the National Hospital Discharge Register. An incident diabetes event was defined as the date of special reimbursement, or hospital discharge due to diabetes. Codes distinguishing between type 1 and type 2 diabetes have been entered in the Hospital Discharge Register in Finland since Follow-up of each participant in our present analysis continued through the end of December 2002 or until death. There were 2770 cases of type 2 diabetes identified during the follow-up. Statistical analyses SPSS for Windows 11.0 was used for statistical analysis. Differences in risk factors between subjects in different smoking categories were tested using analysis of variance (anova) or logistic regression after adjustment for age and study year. The Cox proportional hazards model was used to estimate the effect of smoking status on the risk of type 2 diabetes; and also to assess the magnitude of a joint effect of smoking with BMI and physical activity on the risk of type 2 diabetes. The analyses were first carried out adjusting for age and study year, and then further for education, systolic blood pressure, coffee and alcohol consumption, occupational and leisure time physical activity, and BMI. Results Table 1 shows the major risk factors (adjusted for age and study year) of diabetes by the smoking status. Male ex-smokers were older and had markedly higher BMI and than never smokers or current smokers. Amongst women, never smokers were older than former and current smokers. In both genders current smokers were physically less active, had a lower education level and drank more coffee and alcohol than never and former smokers. Smoking had a graded association with the risk of type 2 diabetes, and it remained significant after controlling for age, BMI, physical activity, blood pressure, education and coffee drinking (Table 2). The adjusted hazard ratio of type 2 diabetes was 1.22 amongst daily smoking men less than 20 cigarettes and 1.57 amongst men smoking over 20 Table 1 General characteristics of study subjects by baseline smoking status Smoking status (women) Smoking status (men) P-value <20 cigarettes 20 cigarettes day )1 day )1 day )1 P-value Never Former <20 cigarettes 20 cigarettes day )1 Never Former No. of participants Age (years) 41.7 (10.6) 46.7 (10.3) 42.5 (11.0) 41.5 (10.0) < (10.8) 39.9 (10.5) 39.0 (10.5) 39.7 (9.7) <0.001 Body mass index 25.9 (3.3) 26.9 (3.6) 25.6 (3.6) 25.9 (3.7) < (4.7) 26.1 (4.4) 25.5 (4.2) 25.9 (4.7) <0.001 (kg m )2 ) Diastolic blood 88 (12) 89 (12) 87 (12) 88 (12) < (12) 84 (12) 83 (12) 84 (13) <0.001 pressure (mmhg) Systolic blood 142 (18) 144 (19) 143 (19) 144 (18) < (23) 138 (19) 138 (20) 139 (21) <0.001 pressure (mmhg) Education (years) 9.3 (3.9) 9.0 (3.7) 8.8 (3.8) 8.3 (3.1) < (3.8) 9.5 (3.6) 9.0 (3.4) 8.6 (3.2) <0.001 Daily coffee 4.6 (2.9) 5.1 (2.9) 5.6 (3.0) 6.8 (3.5) < (2.3) 4.8 (2.5) 5.4 (2.6) 6.9 (3.3) <0.001 consumption (cups) Alcohol drinker (%) < <0.001 Low occupational < <0.001 physical activity (%) Low leisure time < <0.001 physical activity (%) Age and study year were adjusted. Values are mean (SD) or percentage.

4 SMOKING AND THE RISK OF TYPE 2 DIABETES 359 Table 2 Hazard ratios for the incidence of type 2 diabetes according to smoking habits Smoking status Never smoking Ex-smoking Current smoker <20 cigarettes day )1 Current smoker 20 cigarettes day )1 Men Number of new cases of diabetes Person-years Adjustment for age and study year ( ) a 1.19 ( ) a 1.64 ( ) a Multivariate adjustment b ( ) 1.22 ( ) a 1.57 ( ) a Women Number of new cases of diabetes Person-years Adjustment for age and study year ( ) 1.05 ( ) 1.56 ( ) a Multivariate adjustment b ( ) 1.46 ( ) a 1.87 ( ) a Men and women combined c No. of new cases Person-years Adjustment for age and study year ( ) 1.04 ( ) 1.50 ( ) a Multivariate adjustment b ( ) 1.30 ( ) a 1.65 ( ) a a P < 0.05 compared with reference group. b Adjusted for age, study year, education, body mass index, systolic blood pressure, coffee consumption (0 2, 3 4, 5 6, 7 9, and 10 cups per day), alcohol consumption (yes and no), occupational (light, moderate or active) and leisure time (low, moderate or high) physical activity. c Adjusted also for sex. cigarettes. In women these hazard ratios were 1.46 and 1.87 respectively. Formerly smoking men tended to have a slightly increased, and formerly smoking women had a slightly decreased risk of type 2 diabetes compared with never smoking men. The number of incident cases of diabetes was, however, fairly small amongst former female smokers. When both genders were combined, the multivariate adjusted risk of type 2 diabetes was increased in former smokers by 9%, in current smokers smoking <20 cigarettes daily by 30%, and in current smokers smoking 20 cigarettes daily by 65% higher compared with never smokers. As expected, BMI was a strong predictor of type 2 diabetes (Table 3). Smoking increased the risk in all BMI levels, and similarly overweight increased the risk in all smoking categories. Obese smoking subjects had a 10-fold risk of type 2 diabetes compared with never smokers who had normal weight. Physical activity had a protective effect on the risk of type 2 diabetes (Table 4). At any physical activity level, never smokers had a lower risk of type 2 diabetes compared with current smokers. In all smoking categories physically active subjects had a lower diabetes risk than that in sedentary subjects. Discussion Cigarette smoking increased the risk of type 2 diabetes in a graded manner. The association was independent of age, systolic blood pressure, coffee and alcohol consumption, BMI and physical activity level. Amongst smokers smoking less than 20 cigarettes daily the multifactorially adjusted elevation in risk was 30%, and amongst those who smoked 20 cigarettes or more daily, the risk increased by 65%. Thus, the risk of type 2 diabetes associated with smoking is of the same magnitude as the risk associated with moderate overweight or sedentary lifestyle [14]. Smoking increased the risk of diabetes at all BMI and physical activity levels; thus, smoking has an additive effect on the risk of type 2 diabetes with the major risk factors. The smoking-associated risk of type 2 diabetes in this study was comparable with recent studies carried out in large populations with similar criteria for type 2 diabetes [5 10]. However, the populations of those studies are not fully comparable to ours for reasons varying from type of medical staff [5, 7] to

5 360 K. PATJA et al. Body mass index (kg m )2 ) Smoking status Never-smoking Ex-smoking Current smoking Men < ( ) 1.35 ( ) ( ) 3.40 ( ) 4.33 ( ) ( ) 9.83 ( ) 12.7 ( ) Women < ( ) 1.73 ( ) ( ) 1.64 ( ) 4.06 ( ) ( ) 7.79 ( ) 10.4 ( ) Men and women combined b < ( ) 1.43 ( ) ( ) 3.04 ( ) 4.19 ( ) ( ) 8.86 ( ) 11.5 ( ) Table 3 Hazard ratios for the incidence of type 2 diabetes according to smoking habits and body mass index a a Adjusted for age, study year, education, systolic blood pressure, coffee consumption (0 2, 3 4, 5 6, 7 9, and 10 cups per day), alcohol consumption (yes and no) and physical activity. b Adjusted also for sex. Physical activity Smoking status Never-smoking Ex-smoking Current smoking Men High ( ) 1.36 ( ) Moderate 1.15 ( ) 1.14 ( ) 1.67 ( ) Low 1.46 ( ) 1.81 ( ) 1.72 ( ) Women High ( ) 1.42 ( ) Moderate 0.99 ( ) 0.58 ( ) 1.58 ( ) Low 1.23 ( ) 1.39 ( ) 1.87 ( ) Men and women combined b High ( ) 1.32 ( ) Moderate 1.03 ( ) 0.99 ( ) 1.58 ( ) Low 1.26 ( ) 1.71 ( ) 1.72 ( ) Table 4 Hazard ratios for the incidence of type 2 diabetes according to smoking habits and physical activity a a Adjusted for age, study year, education, systolic blood pressure, coffee consumption (0 2, 3 4, 5 6, 7 9, and 10 cups per day), alcohol consumption (yes and no) and body mass index. b Adjusted also for sex. different age groups and risk factors included in the analyses. In studies with comparable middle-aged female populations, the risk of type 2 diabetes related to smoking in this study was higher [5, 6]. Amongst men, the risk of diabetes related to smoking in this study was slightly lower than in most previous studies [6, 9, 15, 16], except one [10]. A graded increase in risk has been also found in previous studies [7], but the gradient is difficult to compare as studies vary by sex, age group and other confounding factors. Male former smokers had a slightly higher and female former smokers had a slightly lower risk of type 2 diabetes compared with never smokers. Amongst males the result is in accordance with previous findings indicating that smoking cessation reduces the risk of diabetes over time [17]. The number of female former smokers was fairly small because fewer than 10% of Finnish women smoked in the 1960s and the 1970s [18]. Moreover, even though smoking amongst women is nowadays associated with a low socio-economic status, the situation used to be opposite in the past. This could result in female ex-smokers being better educated and thus better protected against other co-morbidities that increase the risk of type 2 diabetes. A causal association between smoking and type 2 diabetes is biologically plausible. Tobacco smoke

6 SMOKING AND THE RISK OF TYPE 2 DIABETES 361 damages all organs and it is no surprise that smoking increases the risk of type 2 diabetes. Tobacco and its ingredients have many potential ways to induce type 2 diabetes. Smoking can acutely impair insulin action both in patients with type 2 diabetes and in persons with normal glucose tolerance [19]. In experimental studies smokers have higher insulin response and C-peptide activity to a glucose load than nonsmokers. Smokers also have increased hepatic lipase activity, which is linked with increased insulin resistance [20]. Cigarette smoke can directly harm the pancreas as it enhances ethanol-induced pancreatic injury leading to impaired beta cell function and insulin receptor sensitivity [21, 22]. Moreover, smoking drastically increases oxidative stress, indicated by an increase in the concentration of free radicals [23]. Vascular changes and reduced blood flow to skeletal muscles may also contribute to insulin resistance [7]. The degree of insulin resistance is associated with the amount of cigarettes smoked [24]. When quitting smoking, the risk of weight gain is greater if physical activity and dietary control are not used to compensate the increase in appetite. Smokers in this study were less physically active, a phenomenon also found in other studies [10, 25]. Dietary habits of current smokers are also less favourable [26, 27]. Physical activity has been found both to protect from type 2 diabetes, obesity and smoking, but also to act as a promoter for other life style changes [28]. Smoking cessation often leads to weight gain with an average gain of 3 kg [29], also shown in our first cohorts [30]. As a result of weight gain by 5% it has been proposed that the risk of type 2 diabetes by about 20% [31], but the average weight gain following the smoking cessation would still not overcome the reduction of risk gained by smoking cessation. A limitation of the present study is that due to the large sample size, biological markers of smoking were not measured at baseline, and glucose tolerance tests were not performed during the follow-up. However, serum cotinine levels were determined for a sub-sample of our study showing that self-reporting of smoking is fairly reliable in Finland [32]. Use of two nationwide databases ascertained the most incident type 2 diabetes cases, though some delay may have occurred. Furthermore, in the Drug Register, diabetes is first diagnosed by the person s own doctor, and then confirmed by the Social Insurance Institution s specialist using the standard criteria, which improves the validity of our outcome data. However, our register data do not include those diabetic subjects, who were treated with diet alone. Even though the misclassification of exposure and outcome data can never be fully avoided in large epidemiological studies, a misclassification in this study is most probably random and may weaken the true association between smoking and the risk of type 2 diabetes. Moreover, because the risk of type 2 diabetes increases exponentially with age, selective high mortality of smokers most probably decreases the estimated smoking-associated risk of type 2 diabetes [33, 34]. Another limitation of our study is that we did not have nutritional data available for our analyses. Other studies have shown that the diet of smokers is usually less healthy than that of nonsmokers. Finally, due to some differences in the data collection in different study years, the data on alcohol drinking were fairly crude, and we could not classify people according to the type and the amount of drinking. Smoking is an independent and modifiable risk factor for type 2 diabetes. Obese and sedentary smokers form a high-risk population in need for multiple lifestyle change promotion. Recently, it has been proposed that the prevention of type 2 diabetes, cardiovascular disease and cancer share the same principles [35]. Avoiding smoking is one of the most efficient ways of preventing these serious diseases. Amongst smokers, information about the risk of type 2 diabetes should be provided for individuals considering smoking cessation. Conflict of interest statement No conflict of interest was declared. Acknowledgement This study was supported by grants from the Finnish Academy (grants 46558, 53585, , ). References 1 Hu G, Lindstrom J, Valle TT et al. Physical activity, body mass index, and risk of type 2 diabetes in patients with normal or

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