Alcohol and Alcoholism Advance Access published online on February 18, 2008
Alcohol and Alcoholism, doi:10.1093/alcalc/agn005
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Associations of Alcohol Drinking and Cigarette Smoking with Serum Lipid Levels in Healthy Middle-Aged Men
1 Department of Environmental and Preventive Medicine, Hyogo College of Medicine, Hyogo, Japan
2 Department of Hygiene and Preventive Medicine, Yamagata University School of Medicine, Yamagata, Japan
* Author to whom correspondence should be addressed at: Department of Environmental and Preventive Medicine, Hyogo College of Medicine, Mukogawa-cho 1–1, Nishinomiya, Hyogo 663–8501, Japan. Tel.: +81-798-45-6561; Fax: +81-798-45-6563; E-mail: wakabaya{at}hyo-med.ac.jp
Received 29 August 2007;
first review notified 30 October 2007; in revised form 29 November 2007;
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ABSTRACT |
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Aims: The aim of this study is to determine whether influences of drinking alcohol on serum lipid levels are different in smokers and non-smokers. Methods: Subjects were 25,689 healthy male workers aged 40 to 59 years. Serum total and HDL cholesterol and triglyceride concentrations were measured and LDL cholesterol concentrations were estimated by using the Friedewald formula. The subjects were divided into three groups by average daily consumption of cigarettes (non-smokers; light smokers, less than 20 cigarettes per day; heavy smokers, 20 or more cigarettes per day) and by average daily alcohol consumption (non-drinkers; light drinkers, less than 30 g of ethanol per day; heavy drinkers, 30 g or more of ethanol per day). Results: In overall subjects, serum HDL, LDL and total cholesterol were significantly lower and triglyceride was significantly higher in heavy smokers than in non-smokers. In the smoker groups, serum total cholesterol was significantly lower in heavy drinkers than in non-drinkers, while no difference in total cholesterol was observed in non- and heavy drinkers of the non-smoker group. Both in the smoker and non-smoker groups, HDL cholesterol was higher and LDL cholesterol was lower in drinkers than in non-drinkers. The difference in LDL cholesterol between non-drinkers and drinkers was more prominent in smokers than in non-smokers. The above associations were not altered after the adjustment for age, body weight and alcohol intake. Conclusions: The results suggest that smoking increases the lowering effect of alcohol drinking on LDL cholesterol, but does not affect the relationship of alcohol drinking with HDL cholesterol.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONReferences |
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Alcohol drinking and cigarette smoking are social habits of lifestyle that are closely related to a variety of diseases. Smoking is a major risk factor for atherosclerotic cerebro- and cardiovascular diseases. Various pathophysiological mechanisms, including injury of the vascular endothelium and lipid peroxidation, have been known to be involved in facilitation of the atherosclerotic progression due to smoking (Tsiara et al., 2003
; Ambrose and Barua, 2004). Smoking affects the blood lipid profile: serum HDL and LDL cholesterol concentrations have been reported to be lower and higher, respectively, in smokers than in non-smokers (Whitehead et al., 1996; Cullen et al., 1998; Lee et al., 1998). Thus, smoking may exert its atherogenic effects through blood lipid levels. On the other hand, moderate alcohol consumption is known to lower the incidence of coronary heart disease (Corrao et al., 2000; Meister et al., 2000), and this preventive effect of alcohol drinking is known to be explained mainly by the increasing action of alcohol on blood HDL cholesterol levels (Gaziano et al., 1993; Rimm et al., 1999). In addition, LDL cholesterol has been reported to be decreased by alcohol drinking (Savolainen and Kesäniemi, 1995; Nakanishi et al., 2001). These findings suggest that cigarette smoking and alcohol drinking have opposite effects on atherogeneity through altering the blood lipid profile. Interactions of smoking and drinking on blood lipids have also been suggested. The HDL cholesterol/non-HDL cholesterol ratio was lower in non-drinkers than in drinkers, and this association was stronger among smokers than in non-smokers (Salonen et al., 1987). Serum total cholesterol was inversely associated with smoking in drinkers but not in non-drinkers, while HDL cholesterol decreased with increasing degree of cigarette consumption in non-drinkers but not in drinkers (Handa et al., 1990). Total cholesterol and triglycerides were positively associated with alcohol intake in non-smokers but not in smokers, while alcohol was positively associated with HDL cholesterol both in smokers and non-smokers (Wannamethee and Shaper 1992). LDL cholesterol increased with increasing alcohol consumption in non-smokers but decreased in smokers (Whitehead et al., 1996). Furthermore, alcohol drinking showed a depressive effect on LDL cholesterol concentrations and this effect was significant only in smokers (Wu et al., 2001). Thus, no consistent results on the interactions of alcohol drinking and cigarette smoking on blood lipids have been obtained so far.
The purpose of this study was to investigate whether the effects of alcohol drinking on blood lipids were influenced by cigarette smoking. Since there is a strong relationship between alcohol consumption and smoking (Veenstra et al., 1993), amount of alcohol intake should be taken into account when the effects of alcohol are compared in different groups defined by cigarette consumption. However, there have been no studies on relationships between alcohol drinking and blood lipids in different smoking categories with adjustment for alcohol intake. For this purpose, alcohol intake-matched groups of smokers and non-smokers were also used in this study.
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METHODS |
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Subjects
The subjects were 25,689 healthy men, aged between 40 and 59 years, who underwent periodic health examinations at their workplaces. In Japan, workers in companies with 50 employees or more must undergo annual health checkups, and the companies are required by law to pay the costs for health checkups of the workers. The subjects of this cross-sectional study were workers generally enrolled in Yamagata, a prefecture of Japan (total population: about 1.2 million). Thus, workers from various kinds of companies (e.g. construction, manufacturing, information and communications, transport, wholesale and retail trade, eating and drinking places, accommodations, and services) were included in the subjects. Data from a periodic medical checkup database, which was prepared by a major health-checkup company, were used in this study, and the data for each subject were registered in the database only by code numbers. The present study protocol was approved by the Ethics Committee of Yamagata University School of Medicine. Workers who were receiving therapy for any illnesses were excluded from the subjects of this study. The major illnesses for exclusion were hypertension (8.32%), peptic ulcer (3.72%), diabetes mellitus (2.60%), low back pain (1.39%), dyslipidemia (1.26%), liver disease (1.02%), hyperuricemia (1.00%), arrhythmia (0.70%) and ischemic heart disease (0.65%).
Measurements
Blood was sampled from each subject, and serum total cholesterol and HDL cholesterol were measured by an enzymatic method (cholesterol oxidase) using commercial kits, L-type CHO H (Wako Pure Chemical Industries, Osaka, Japan) and Cholestest N HDL (Daiichi Pure Chemicals, Tokyo, Japan), respectively. HDL cholesterol measurement was performed in the presence of a detergent that specifically solubilizes HDL cholesterol. Serum triglyceride was measured by an enzymatic method (lipoprotein lipase) using a commercial kit, Pureauto S TG-N (Daiichi Pure Chemicals, Tokyo, Japan). The reproducibility of measurements of total cholesterol, HDL cholesterol and triglyceride was sufficiently high (coefficient of variation < 5%). Atherogenic index was calculated as [(total cholesterol) – (HDL cholesterol)]/(HDL cholesterol). Serum LDL cholesterol concentration was estimated by using the Friedewald formula as follows: (LDL cholesterol) = (total cholesterol) – (HDL cholesterol) – [(triglyceride)/5]. Serum LDL cholesterol concentrations estimated by the Friedewald formula were used for analysis only in subjects with serum triglyceride concentrations less than 400 mg/dl. Body mass index (BMI) was calculated as [weight (kg)]/ [height (m)]2.
Classification of alcohol drinkers and smokers
Average alcohol consumption of each subject per week and average cigarette consumption per day were reported on questionnaires during the health examinations at each workplace. There are a variety of drinking styles such as daily regular consumption and weekend binge drinking. In order to cover these styles in this study, usual weekly alcohol consumption was recorded in the questionnaires and then the average daily alcohol intake was calculated. Usual weekly alcohol consumption was recorded in terms of the equivalent number of "go", a traditional Japanese unit of amount of sake (rice wine). One "go" contains about 28 ml of ethanol. The amounts of other alcoholic beverages, including beer, wine and whisky, were converted and expressed as units of "go". Average daily alcohol intake (grams of ethanol per day) was then calculated. The subjects in each age group were divided into three groups according to ethanol consumption per day (non-drinkers; light drinkers, less than 30 g per day; heavy drinkers, 30 g or more per day). In a part of the analysis, super-light drinker group (less than 15 g of ethanol per day) was also used. The subjects were also divided into three groups by average cigarette consumption (non-smokers; light smokers, less than 20 cigarettes per day; heavy smokers, 20 or more cigarettes per day). Since alcohol consumption was different in smokers and non-smokers, alcohol intake-matched groups of non-, light and heavy smokers were also used in a part of the analysis in order to compare the relationships of alcohol drinking with serum lipids in the different smoking groups. Alcohol intake-matched groups were prepared as follows. Subjects were randomly selected from each alcohol intake category and the number of subjects from each alcohol intake category was adjusted to be the same among the non-smoker, light smoker and heavy smoker groups. The mean with standard deviation of alcohol consumption in each smoking group was 32.06 ± 29.92 g/day (n = 6643).
Statistical analysis
Statistical analyses were performed using computer software (SPSS version 14.0J for Windows). Mean levels of each lipid-related variable were compared in the different alcohol groups or in the different smoking groups using analysis of variance (ANOVA) followed by Scheffé's F-test. In multivariate analysis, the mean levels of each variable were calculated after adjustment for age and body weight and were compared in different groups using ANOVA and then Student's t-test after Bonferroni correction. Since there is a possibility that serum triglyceride levels do not fit a normal distribution, they were used for analysis after log-conversion. The mean LDL levels in each alcohol group were also compared in different smoking subgroups after adjustment for age, body weight and alcohol consumption. Probability (P) values less than 0.05 were defined as significant.
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RESULTS |
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Table 1 shows profiles of subjects divided into groups by cigarette consumption. The mean age and alcohol consumption were significantly lower and higher, respectively, in smokers than in non-smokers. Body weight, body mass index and total cholesterol were significantly lower in light and heavy smokers than in non-smokers, but were significantly higher in heavy smokers than in light smokers. HDL and LDL cholesterol levels were significantly lower and log-converted triglyceride level and atherogenic index were significantly higher in heavy smokers than in non-smokers. LDL cholesterol was significantly lower in light smokers than in non-smokers and heavy smokers.
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Serum lipid levels and atherogenic index in each group divided by cigarette consumption were compared in the different subgroups divided by alcohol intake (Fig. 1). In the smoker groups, total cholesterol level was significantly lower in the heavy drinker subgroup than in the non-drinker subgroup, while no difference was found for total cholesterol levels in the non-drinker and heavy drinker subgroups of the non-smoker group (Fig. 1A). Both in smokers and non-smokers, HDL cholesterol was higher and LDL cholesterol was lower in the drinker subgroups than in the non-drinker subgroup (Fig. 1B,C). The difference in LDL cholesterol concentrations between the non-drinker and drinker subgroups was more prominent in smokers than in non-smokers (Fig. 1C). There were tendencies for log-converted triglyceride levels to be lower in light drinkers than in non-drinkers and heavy drinkers (Fig. 1D). Both in smokers and non-smokers, atherogenic index was lower in the drinker subgroups than in the non-drinker subgroup, and this difference was more prominent in smokers than in non-smokers (Fig. 1E). The above relationships of drinking with serum lipid levels and atherogenic index in smokers and non-smokers were not altered after adjustment for age and body weight (Table 2). The above relationships were also obtained when alcohol intake-matched groups of non-smokers, light smokers, and heavy smokers were used (Table 3). The relationships of serum non-HDL cholesterol levels (total cholesterol – HDL cholesterol) with alcohol drinking in each smoking group were also analysed (Table 4). Non-HDL cholesterol levels of all three smoking groups were significantly lower in the heavy drinker subgroup than in the non-drinker and light drinker subgroups and were significantly lower in the light drinker subgroup than in the non-drinker subgroup. The differences in non-HDL cholesterol between non-drinkers and drinkers were more prominent in smokers than in non-smokers (Table 4). Furthermore, the above results for the relationships of alcohol drinking with blood lipid levels and atherogenic index in different smoking groups were not changed when data for subjects with a history of therapy for any illnesses were included in the analysis (data not shown).
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) and P < 0.01 (
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The effects of a smaller amount of alcohol intake [super-light drinking (less than 15 g per day of ethanol)] on blood lipid levels were also investigated in different smoking groups of alcohol intake-matched subjects (Table 5). Both in non-smokers, light smokers and heavy smokers, HDL cholesterol was significantly higher and atherogenic index was significantly lower in the super-light drinker subgroup than in non-drinker subgroup. However, LDL cholesterol, total cholesterol and log-converted triglyceride were not significantly different in the non- and super-light drinker subgroups of smokers and non-smokers.
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LDL cholesterol levels in each alcohol group were also compared in different smoking subgroups after adjusting the amount of alcohol consumption, in addition to age and body weight. In heavy drinkers, the mean LDL cholesterol levels were significantly lower in the light and heavy smoker subgroups than in the non-smoker subgroup [108.6 ± 0.6 mg/dl (non-smokers) vs. 103.5 ± 0.5 mg/dl** (light smokers) vs. 103.5 ± 0.5 mg/dl** (heavy smokers) (**P < 0.01 compared with non-smokers)], while there was a tendency for the mean LDL cholesterol level in non-drinkers to be higher in the heavy smoker subgroup (P = 0.061 vs. non-smokers and P = 0.002 vs. light smokers) than in the non-smoker and light smoker subgroups [119.0 ± 0.6 mg/dl (non-smokers) vs. 117.8 ± 0.7 mg/dl (light smokers) vs. 121.3 ± 0.8 mg/dl (heavy smokers)]. In light drinkers, there was a U-shaped tendency between smoking and LDL cholesterol levels [114.8 ± 0.5 mg/dl (non-smokers) vs. 111.7 ± 0.5 mg/dl** (light smokers) vs. 115.3 ± 0.6 mg/dl (heavy smokers) (**P < 0.01 compared with non- and heavy smokers)].
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONReferences |
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This study demonstrated the interactions of alcohol drinking and cigarette smoking on serum lipid levels. Serum total cholesterol in smokers was lower in the drinker subgroups than in the non-drinker subgroup, while total cholesterol in non-smokers was not different for the drinker and non-drinker subgroups. This difference in the relationship of drinking alcohol with total cholesterol levels between smokers and non-smokers is related to LDL cholesterol levels, which were lower in drinkers than in non-drinkers, and this difference in LDL cholesterol levels between drinkers and non-drinkers was much greater in smokers than in non-smokers. On the other hand, the difference in HDL cholesterol levels between drinkers and non-drinkers was comparable in smokers and non-smokers. Thus, it is thought that LDL cholesterol is more prone to be affected by alcohol drinking in smokers than in non-smokers.
A strong relationship between alcohol consumption and smoking is known, and it should be taken into account when the effects of alcohol are compared for different smoking groups. This may explain in part why no consistent results have been obtained so far for the interactions of alcohol drinking and cigarette smoking on blood lipids in several previous studies, none of which used alcohol intake-matched subjects. Thus, one possible explanation for the above finding about the relationships between LDL cholesterol and alcohol drinking in smokers and non-smokers is the difference in amount of alcohol consumption between smokers and non-smokers. In fact, the amount of alcohol consumption was significantly higher in the smoker groups than in the non-smoker group in the present study (Table 1). In order to test this possibility, blood lipid levels were compared in alcohol intake-matched subgroups of non-, light and heavy smokers, and the above relationships between smoking, drinking and blood lipids were also found in the alcohol intake-matched subject groups. Therefore, the difference in the drinking-related decrease in LDL levels between smokers and non-smokers is thought to be independent of amount of alcohol consumption. The prominent lowering effects of drinking on LDL levels in smokers were also reflected by the prominent lowering effects of drinking on atherogenic index. The present study is the first study using alcohol intake-matched subjects to show the interrelationships of alcohol drinking and smoking with blood lipids. Further studies using a prospective design are needed to confirm the causal relationships among alcohol drinking, smoking and blood lipids.
Both in the non-, light and heavy smoker groups, HDL cholesterol was higher and atherogenic index was lower in the super-light drinker subgroup than in non-drinker subgroup. However, LDL cholesterol and total cholesterol were not significantly different in the non- and super-light drinker subgroups of smokers and non-smokers. These results suggest that serum HDL cholesterol level is more easily affected by low doses of alcohol drinking compared to serum LDL cholesterol level, regardless of smoking status.
There is a difference in results with respect to the relationship between alcohol drinking and LDL cholesterol: Whitehead et al. (1996) reported that LDL cholesterol concentration rose with increasing alcohol intake in non-smokers, while LDL cholesterol decreased with increasing alcohol consumption in heavy smokers. Wu et al. (2001) showed that LDL cholesterol concentration decreased with increasing alcohol consumption in heavy smokers, but this tendency was not observed in non-smokers and light smokers. In the present study, LDL cholesterol decreased with increasing alcohol consumption both in smokers and non-smokers, and the effect of alcohol drinking on LDL cholesterol was more prominent in smokers than in non-smokers. Thus, the main difference in results of these studies is the relationship between LDL cholesterol concentrations and alcohol drinking in non-smokers. Although the reason for the above differences in results is not clear and further investigation is needed to clarify it, possible reasons include differences in age and race of subjects and environmental exposure to smoking, which may confound the interrelationships of drinking and smoking with LDL cholesterol concentrations. In fact, the relationship between alcohol drinking and LDL cholesterol has been reported to differ by age (Wakabayashi and Kobaba-Wakabayashi, 2002) and the sensitivity to alcohol is known to be higher in Orientals than in Caucasians, mainly due to genetic difference in alcohol-metabolizing enzymes (Mizoi et al., 1979; Harada et al., 1981). On the other hand, a consistent finding in the studies is that smoking appears to augment the LDL lowering effect of alcohol drinking. This possible biological action of smoking should also be clarified in the future. There is also a discrepancy in the results regarding the smoking-LDL cholesterol relationship in overall subjects: higher serum LDL cholesterol levels in smokers than in non-smokers have been shown in some studies (Whitehead et al., 1996; Cullen et al., 1998; Lee et al., 1998), but a study using Taiwanese subjects showed no significant difference between LDL cholesterol levels in smokers and non-smokers (Wu et al., 2001), and the present study using Japanese subjects showed lower LDL cholesterol levels in smokers than in non-smokers. In the present study, LDL cholesterol levels in each alcohol group were also compared in subgroups divided by cigarette consumption after adjustment for amount of alcohol consumption as well as age and body weight. LDL cholesterol of heavy drinkers was lower in the light and heavy smoker subgroups than in the non-smoker subgroup, while in non-drinkers, LDL cholesterol was slightly higher in the heavy smoker subgroup than in the non- and light smoker subgroups. Thus, drinking alcohol strongly confounds the relationship between smoking and LDL cholesterol. In addition, the above-mentioned reasons such as ethnic and age differences are also possible for the different findings among the studies regarding the relationship between smoking and LDL cholesterol.
In the present study, HDL cholesterol concentrations increased with increasing alcohol intake, and this relationship was not different for smokers and non-smokers. This finding agrees with those of previous studies (Whitehead et al., 1996; Wu et al., 2001). Thus, smoking influences the relationship of alcohol drinking with LDL cholesterol, but not the relationship of alcohol drinking with HDL cholesterol. The present study also showed a greater decrease in atherogenic index by alcohol drinking reflecting LDL cholesterol/HDL cholesterol ratio in smokers than in non-smokers, and this may be largely due to the higher sensitivity of LDL cholesterol concentration to alcohol drinking in smokers. Smoking per se is a major risk factor for atherosclerotic disease, while alcohol drinking shows both beneficial and harmful effects on atherosclerotic progression mainly through influencing blood lipid profile and blood pressure, respectively, and light-to-moderate alcohol drinking is known to be negatively related to atherosclerotic progression. The present findings suggest that alcohol drinking shows elevating effects on HDL cholesterol in both smokers and non-smokers and that the lowering action of drinking on LDL cholesterol is stronger in smokers than in non-smokers. Therefore, light-to-moderate drinking is beneficial for smokers as well as for non-smokers through improvement of blood lipid profile from the viewpoint of prevention of cardiovascular disease.
The following possibilities of biases in this study are raised. There is a possibility of a bias caused by not including ex-smokers and ex-drinkers in the present study. The conditions of diet and physical activity, which could confound the relationships among alcohol drinking, smoking and blood lipid levels, were not surveyed in the present study, and this may also cause a bias, although adjustment for body mass index, which reflects these factors, did not alter the findings of this study (data not shown). Furthermore, there is a possibility of a bias that a part of the decreases in LDL cholesterol observed in heavy smokers with increasing alcohol consumption was originated from increases in triglyceride since triglyceride level is included in the Friedewald formula for estimation of LDL cholesterol level. However, in multivariate analyses using total subjects and alcohol intake-matched subjects, log-converted triglyceride levels were not significantly different in non-drinkers and heavy drinkers independently of smoking status (Tables 2 and 3). Moreover, the differences in non-HDL cholesterol between non-drinkers and drinkers were more prominent in smokers than in non-smokers, and this finding is similar to the results of the analysis for the relationship between alcohol drinking and serum LDL cholesterol calculated by using the Friedewald formula. Therefore, it is unlikely that the calculation of LDL cholesterol concentrations using the formula influenced the conclusion of this study.
In conclusion, smoking influenced the relationship of alcohol drinking with LDL cholesterol but not the relationship of alcohol drinking with HDL cholesterol, and alcohol-induced anti-atherogenic action through lowering of LDL cholesterol is suggested to be stronger in smokers than in non-smokers.
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ACKNOWLEDGEMENTS |
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This work was supported by a grant for scientific research from the Ministry of Education, Science and Culture of Japan (No. 19590656).
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References |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONReferences |
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Ambrose J. A., Barua R. S. The pathophysiology of cigarette smoking and cardiovascular disease: An update. Journal of the American College of Cardiology (2004) 43:1731–1737.
Corrao G., Rubbiati L., Bagnardi V., Zambon A., Poikolainen K. Alcohol and coronary heart disease: A meta-analysis. Addiction (2000) 95:1505–1523.[CrossRef][Web of Science][Medline]
Cullen P., Schulte H., Assmann G. Smoking, lipoproteins and coronary heart disease risk. Data from the Münster heart study (PROCAM). European Heart Journal (1998) 19:1632–1641.
Gaziano J. M., Buring J. E., Breslow J. L., et al. Moderate alcohol intake, increased levels of high-density lipoprotein and its subfractions, and decreased risk of myocardial infarction. The New England Journal of Medicine (1993) 329:1829–1834.
Handa K., Tanaka H., Shindo M., Kono S., Sasaki J., Arakawa K. Relationship of cigarette smoking to blood pressure and serum lipids. Atherosclerosis (1990) 84:189–193.[CrossRef][Web of Science][Medline]
Harada S., Agarwal D. P., Goedde H. W. Aldehyde dehydrogenase deficiency as cause of facial flushing reaction to alcohol in Japanese. Lancet (1981) 2:982.[Web of Science][Medline]
Lee K. S., Park C. Y., Meng K. H., et al. The association of cigarette smoking and alcohol consumption with other cardiovascular risk factors in men from Seoul, Korea. Annals of Epidemiology (1998) 8:31–38.[CrossRef][Medline]
Meister K. A., Whelan E. M., Kava R. The health effects of moderate alcohol intake in humans: An epidemiologic review. Critical Reviews in Clinical Laboratory Sciences (2000) 37:261–296.[CrossRef][Web of Science][Medline]
Mizoi Y., Ijiri I., Tatsuno Y., et al. Relationship between facial flushing and blood acetaldehyde levels after alcohol intake. Pharmacology Biochemistry and Behavior (1979) 10:303–311.[CrossRef][Web of Science][Medline]
Nakanishi N., Yoshida H., Nakamura K., Kawashimo H., Tatara K. Influence of alcohol intake on risk for increased low-density lipoprotein cholesterol in middle-aged Japanese men. Alcoholism: Clinical and Experimental Research (2001) 25:1046–1050.[CrossRef][Web of Science][Medline]
Rimm E. B., Williams P., Fosher K., Criqui M., Stampfer M. J. Moderate alcohol intake and lower risk of coronary heart disease: Meta-analysis of effects on lipids and haemostatic factors. British Medical Journal (1999) 319:1523–1528.
Salonen J. T., Happonen P., Salonen R., et al. Interdependence of associations of physical activity, smoking, and alcohol and coffee consumption with serum high-density lipoprotein and non-high-density lipoprotein cholesterol—a population study in eastern Finland. Preventive Medicine (1987) 16:647–658.[CrossRef][Web of Science][Medline]
Savolainen M. J., Kesäniemi Y. A. Effects of alcohol on lipoproteins in relation to coronary heart disease. Current Opinion in Lipidology (1995) 6:243–250.[Web of Science][Medline]
Tsiara S., Elisaf M., Mikhailidis D. P. Influence of smoking on predictors of vascular disease. Angiology (2003) 54:507–530.[Web of Science][Medline]
Veenstra J., Schenkel J. A., van Erp-Baart A. M., et al. Alcohol consumption in relation to food intake and smoking habits in the Dutch National Food Consumption Survey. European Journal of Clinical Nutrition (1993) 47:482–489.[Web of Science][Medline]
Wakabayashi I., Kobaba-Wakabayashi R. Effects of age on the relationship between drinking and atherosclerotic risk factors. Gerontology (2002) 48:151–156.[CrossRef][Medline]
Wannamethee G., Shaper A. G. Blood lipids: The relationship with alcohol intake, smoking, and body weight. Journal of Epidemiology and Community Health (1992) 46:197–202.
Whitehead T. P., Robinson D., Allaway S. L. The effects of cigarette smoking and alcohol consumption on blood lipids: A dose-related study on men. Annals of Clinical Biochemistry (1996) 33:99–106.[Web of Science][Medline]
Wu D. M., Pai L., Sun P. K., Hsu L. L., Sun C. A. Joint effects of alcohol consumption and cigarette smoking on atherogenic lipid and lipoprotein profiles: Results from a study of Chinese male population in Taiwan. European Journal of Epidemiology (2001) 17:629–635.[CrossRef][Medline]
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