IJE Advance Access originally published online on November 3, 2005
International Journal of Epidemiology 2006 35(1):181-187; doi:10.1093/ije/dyi213
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Article |
Obesity has a greater impact on cardiovascular mortality in younger men than in older men among non-smoking Koreans
1 Department of Family Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
2 Department of Family Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Irwondong, Gangnamgu, Seoul 135–710, Korea
3 Institute of Health and Environment, School of Public Health, Seoul National University, Seoul, Korea
* Corresponding author. Institute of Health and Environment, School of Public Health, Seoul National University, 28 Yongon-Dong, Chogno-Gu, Seoul 110-799, Korea (South). E-mail: scho{at}snu.ac.kr
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Abstract |
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Introduction We investigated the effects of age on the relationship between body mass index (BMI) and cardiovascular risk factors and cardiovascular mortality in non-smoking Korean men.
Methods We performed a prospective cohort study of 246 146 non-smoking Korean men aged 20–69 years at baseline (1992) who were initially without history of cancer or weight change. The associations between BMI and cardiovascular risk factors and mortality during an 9-year follow-up period (2000) were stratified by age group after adjustment for family history, alcohol consumption, exercise habits, and economic status.
Results Calculations of odds ratios (ORs) revealed that younger men (<40 years) with greater BMI (
28 kg/m2) were at greater risk of high blood pressure, high blood glucose, and high total cholesterol than older men. The ORs for cardiovascular risk factors associated with greater BMI declined linearly with age. The relative risks for mortality from stroke and from all cardiovascular diseases associated with greater BMI were also higher among younger men and declined linearly with age.
Conclusions The cardiovascular risk factors and mortality associated with greater BMI were higher among younger than older non-smoking Korean men. These findings indicate that obesity has a greater impact among younger men with respect to premature cardiovascular related deaths.
Keywords Obesity, cardiovascular risk factors, mortality, age effect
Accepted 26 September 2005
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Introduction |
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The relationship between obesity and all-cause mortality is not fully known, although there is thought to be a U-shaped1–7 or J-shaped8–12 association between body mass index (BMI) and mortality. The relationship between BMI and mortality has been shown to vary according to sex,4,12–15 age,16–20 cohort effects,16 socioeconomic status,16 and ethnic background.18
A linear relationship is commonly observed between cardiovascular disease (CVD) mortality and increasing BMI.11,21,22 However, all-cause mortality studies have reported U-shaped or J-shaped relationships2,14,23,24 between mortality and BMI, with much variation according to pre-existing disease and smoking status. Several prospective cohort studies comparing the relationships between BMI and mortality among age groups have shown that the relative risk (RR) associated with greater BMI is higher among younger than among older subjects.20,25
Over the past several decades, South Korea has experienced rapid socioeconomic growth and transformation, resulting in lifestyle changes that have promoted the development of overweight. The prevalence of obesity is increasing more rapidly in young people than in middle-aged or older people in this population.26,27 The risk of CVD has been shown to be increased for subjects having a higher BMI, regardless of age.28 CVD is an increasing health problem in South Korea, and stroke is now a leading cause of death, ranking second among causes of mortality in Korean men.29
Few studies have examined whether age modifies the relationship between BMI and cardiovascular mortality in Asian populations. Using data from a large prospective cohort study, we analysed the associations between BMI and cardiovascular risk factors and mortality in four age groups of healthy non-smoking Korean men.
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Methods |
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Subjects
The sample comprised office workers and teachers insured by the Korean Medical Insurance Corporation, which provides all South Korean civil service personnel with medical insurance and biennial health examinations. This study involved data from 746 221 relatively healthy Korean men aged 20–69 years who had undergone a baseline health examination in 1992. All health examinations were conducted by medical staff at local hospitals using a standardized method. A few days prior to the examination, a questionnaire was administered to each participant. Participants were asked to record their past medical histories, including pre-existing disease, family history (including hypertension, diabetes, and stroke), smoking habits, alcohol consumption, and exercise habits. Participants were also asked to document any experience of involuntary weight change of >3 kg (loss or gain) in the 1 year leading up to the study. Completed questionnaires were reviewed by trained staff. In order to improve the quality of the data, we excluded all individuals who had a history of alleged cancer (n = 1172) or an involuntary weight change of >3 kg in the 1 year leading up to the study (n = 141 097) to eliminate the effect of pre-existing disease or weight fluctuation on the relationship between BMI and cardiovascular mortality. Among them (n = 603 952), we restricted the present analysis to subjects who were non-smokers (n = 246 403) in order to avoid confounding by smoking status. After removing subjects with inadequate or missing data (n = 257), the final study sample included 246 146 men.
BMI and cardiovascular risk factors
Height and weight were measured while subjects were wearing light clothing and no shoes. BMI was calculated as weight (in kilogrammes) divided by height (in metres squared). Blood pressure was measured in the seated position using a standard mercury sphygmomanometer or automatic manometer. When manual manometers were used, systolic and diastolic blood pressures were measured as the first and fifth Korotkoff sounds, respectively. A fasting blood sample was obtained from each subject and analysed for fasting glucose and total cholesterol. All participating medical institutions were equipped with standardized, high-quality laboratories with internal and external quality control procedures authorized by the Korean Association of Laboratory Quality Control. High blood pressure was defined as a systolic blood pressure of at least 140 mm Hg or a diastolic blood pressure of at least 90 mm Hg,30 with participants having a medical history of hypertension included in that group. High blood glucose was defined by a fasting serum glucose level of 7.0 mmol/l (126 mg/dl) or higher,31 with participants having a medical history of diabetes included in that group. High total cholesterol was defined as a serum cholesterol level of at least 6.2 mmol/l (240 mg/dl).32
Mortality data
Mortality within the sample between 1992 and 2000 was mainly based on nationwide death certificate data from the Korean National Statistical Office, supplemented by death benefit records from the Korean Medical Insurance Corporation. The vital status of study subjects between 1992 and 2000 was confirmed through exact data linkage on the basis of a unified 13-digit identification number. The principal outcome variables were (i) mortality from stroke alone (ICD-9 codes 430–438), and (ii) mortality from all CVDs, including hypertensive disease (ICD-9 codes 401–405), ischaemic heart disease (ICD-9 codes 410–414), stroke (ICD-9 codes 430–438), other heart diseases likely related to atherosclerosis (ICD-9 codes 426–429), sudden death (ICD-9 code 798), and other vascular diseases (ICD-9 codes 440–444). To exclude the effects of pre-existing disease on the relationship between BMI and mortality, subjects who died within the first 3 years of the study were excluded from the analyses. The 9-year follow-up period ran from January 1992 to December 2000.
Statistical analyses
Subjects were categorized by BMI categories of <18.0, 18.0–19.9, 20.0–21.9, 22.0–23.9, 24.0–25.9, 26.0–27.9, and 28 kg/m2. Study subjects were categorized into groups for a number of variables, including alcohol drinking habits (non-drinkers, occasional drinkers, and frequent drinkers), physical exercise habits (engaging and not engaging in regular exercise), and economic status (five levels based on monthly salary).
To evaluate the effects of age on the association between BMI and cardiovascular risk factors and mortality, we used the odds ratio (OR) to estimate cardiovascular risk factors and the relative risk (RR) for cardiovascular mortality stratified by four age groups. Multiple logistic regression analysis was performed to examine the relationship between BMI and cardiovascular risk factors, with adjustments for family history, alcohol consumption, exercise status, and economic status. ORs are presented together with their 95% confidence intervals (CIs) for the BMI categories listed above.
Associations of BMI with mortality from stroke and from any CVD were analysed with the Cox proportional hazards regression model. The RRs of death from stroke and from all cardiovascular causes according to BMI category were estimated in models that included family history, alcohol consumption, exercise habit, and economic status. RRs are presented together with their 95% CIs for the BMI categories as above, with the exception that the first category included was <20 kg/m2 because the subjects who had BMIs of <18.0 kg/m2 included two or fewer deaths. Separate analyses were conducted for the four age groups 20–39, 40–49, 50–59, and 60–69 years, with the BMI category 22.0–23.9 kg/m2 used as the reference. We used the likelihood-ratio test to assess the interactions between age and BMI in the proportional-hazards models. Statistical analyses were conducted using the statistical software SAS version 8.1. All analyses were two-tailed, and a P-value <0.05 was considered statistically significant.
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Results |
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The basic characteristics and outcomes of the study cohort assorted by age group are presented in Table 1. Older subjects were more likely to exercise than younger subjects. During the 9 years of follow-up, the mortality rate per 100 000 person years from all CVDs ranged from 10.7 among 20- to 39-year old men to 226.5 among 60- to 69-year old men. The mortality rate from stroke ranged from 4.8 among 20- to 39-year old men to 114.8 among 60- to 69-year old men.
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Family history, lifestyle factors, and pre-existing disease according to BMI category in the study cohort are shown in Table 2. Reports of family history of hypertension, diabetes or stroke, frequent alcohol drinking, and pre-existing diseases of hypertension or diabetes increased with BMI category. However, pre-existing diseases of the respiratory or gastroenterology system decreased with BMI range.
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The ORs and 95% CIs for cardiovascular risk factors according to age and BMI are presented in Table 3. The ORs for high blood pressure, high blood glucose, and high total cholesterol increased with BMI in all age groups. The ORs for cardiovascular risk factors in the subjects with highest BMI (
28 kg/m2) decreased significantly with age, and were higher in the younger age groups than in the older age groups.
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Table 4 shows the RRs and 95% CIs for mortality from stroke according to BMI and stratified by age group. The RRs for mortality from stroke in the subjects with BMI
28 kg/m2 also decreased significantly with age, being higher in the younger age groups than in the older age groups.
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The RRs and 95% CIs for mortality from all CVDs according to BMI and stratified by age group are presented in Table 5. The RRs for all CVD mortality in the subjects with BMI
28 kg/m2 again decreased significantly with age, being higher in the younger age groups than in the older age groups. In subjects aged 20–39 years only, the RR for all cardiovascular mortality linearly increased with BMI range.
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Discussion |
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Among non-smoking Korean men aged 20–69 years, the ORs for cardiovascular risk factors and the RRs of death from stroke and from all CVDs associated with greater BMI were higher among younger than among older men in a prospective sample examined over a 9 year period. Moreover, the ORs for cardiovascular risk factors and the RRs of cardiovascular mortality associated with greater BMI declined with age.
BMI was positively associated with higher risk of cardiovascular risk factors in all age groups. As the BMI range increased, the ORs for cardiovascular risk factors were more prominent in younger than in older subjects. Although the magnitude of RR may be weaker in older men, the absolute difference is probably large. In addition, for death from stroke and death from all CVDs, the increase in risk associated with a higher BMI tended to be greater among younger subjects. Among 20–39 year olds, the RR for mortality from stroke in subjects with BMI 28 kg/m2 was 5.82 (CI 1.79–18.9) compared with 1.36 (CI 0.48–3.91) among 60–69 year olds, showing that the RR for mortality from stroke declined with age.
The association between BMI and cardiovascular mortality found in the present study may have depended on the exclusion criteria used to select study subjects or the cut-off points used for the BMI and age categories. We excluded subjects above the age of 70 because government workers and teachers in this age bracket were scarce. The exclusions limit our ability to generalize from our results, but they increase their internal validity. We also combined the 20–29 year old and 30–39 year old age groups because there were too few deaths in the former to make statistically powerful comparisons for age-specific risk estimates. We also used a BMI of 28 kg/m2 as the highest BMI category because there were insufficient numbers of subjects in our cohort who had a BMI of 30 kg/m2 to enable us to evaluate the association between BMI and mortality stratified by age group.
Pre-existing illness may confound the relationship between BMI and mortality.16,33 Although we excluded the subjects who had a history of alleged cancer and/or an involuntary weight change, we could not completely exclude hidden malignancy, debilitating diseases, or fatal CVDs, which were not found in the initial health examinations. To remove the effect of pre-existing disease, we performed our analyses after excluding deaths during the first 3 years of follow-up. Since smoking is also an important factor that is predictive of low BMI and poor survival,5,8,18 we restricted the present analysis to subjects who were non-smokers. Other lifestyle factors such as alcohol drinking or exercise may have been residual confounding factors that are influenced by age, and indeed older men engaged in regular exercise more than younger subjects in this study.
The design of this study might not allow the effects of age to be distinguished from temporal or birth-cohort effects. The low risks observed for obesity-related cardiovascular risk factors and mortality from stroke and from all CVDs in the older subjects were owing to the longer survival of low-risk individuals compared with high-risk individuals. Such cohort groups still contain subjects of different ages with different birth years. Moreover, they may or may not share time periods that affect both mortality and body weight. These findings may, therefore, be owing to the effects of different histories and unshared exposures that may affect body weight and mortality, in addition to the effects of age.16
The impact of age on the relationship between BMI and mortality may also depend on the methodology used to determine the association,17 such as the use of RR (mortality of obese/mortality of reference) vs risk difference (mortality of obese – mortality of reference). Although the crude death rate from stroke and from any CVD increased substantially with increasing age, being highest in the oldest age group in each BMI category, the RR of death associated with greater BMI declined with increasing age. The impact of BMI on mortality is, therefore, greater in the younger group in terms of the RR, but it should be noted that absolute rates in older subjects are much greater and even a small increase in RR is associated with a substantial increase in absolute numbers of deaths. Other studies have shown that waist circumference is better than BMI at predicting cardiovascular risk factors in older populations.34,35
An additional limitation of this study may be measurement errors in the basic questionnaires, anthropometric variables, blood pressure, and biochemical data. However, all the medical institutions that performed the health examinations were equipped with standardized, high-quality laboratories authorized by Laboratory Quality Control. Each measurement was performed only once at baseline and we did not take into account changes in the variables of participants. In addition, the follow-up period of this study was 9 years. Prolonging the follow-up period may more clearly delineate the effect of age. Another limitation might be crude classifications of alcohol habit and exercise status since there may be potential for residual confounding, which may be modified by age. Unfortunately, detailed information about family history, history of weight change, and pre-existing diseases was not available in the stored data used in this study. Despite these limitations, this cohort study included a very large number of subjects in a wide range of age groups to investigate the effects of age on the association between BMI and cardiovascular risk factors and mortality.
Our results indicate that obesity has a greater impact on cardiovascular risk factors and mortality from stroke and from all CVDs in younger men than in older men among non-smokers. In South Korea, obesity has increased more in younger age groups than in middle-aged or older age groups. To prevent obesity related premature cardiovascular deaths among younger age groups, our results emphasize the importance of managing obesity in younger men.
KEY MESSAGES
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Acknowledgments |
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This study was supported by a grant from the Korean Ministry of Health and Welfare (#01-PJ1-PG1-01CH10-0007).
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