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Diabetes Care 28:2064-2066, 2005
© 2005 by the American Diabetes Association, Inc.

Metabolic Syndrome/Insulin Resistance Syndrome/Pre-Diabetes
Brief Report

Association Between Cigarette Smoking and Metabolic Syndrome

The Korea National Health and Nutrition Examination Survey

Sang Woo Oh, MD, PHD1, Yeong Sook Yoon, MD1, Eon Sook Lee, MD, PHD1, Woo Kyung Kim, MD2, Cheolyoung Park, MD, PHD3, Sangyeoup Lee, MD, PHD4, Eun-Kyeong Jeong, MD, PHD5 and Taiwoo Yoo, MD, PHD6

1 Department of Family Medicine and Center for Health Promotion, Ilsan-Paik Hospital, College of Medicine, Inje University, Gyeonggi-Do, Korea
2 Department of Internal Medicine, Ilsan-Paik Hospital, College of Medicine, Inje University, Gyeonggi-Do, Korea
3 Department of Internal Medicine, Hallym Sacred Heart Hospital, College of Medicine, Hallym University, Gyeonggi-Do, Korea
4 Department of Family Medicine, College of Medicine, Pusan National University, Busan, Korea
5 Division of Chronic Disease Surveillance, Korea Center for Disease Control and Prevention, Seoul, Korea
6 Department of Family Medicine, College of Medicine, Seoul National University, Seoul, Korea

Address correspondence and reprint requests to Taiwoo Yoo, MD, PhD, Department of Family Medicine, Seoul National University, College of Medicine, 28 Yeongon-Dong, Chongno-Gu, 110-744, Seoul, Korea (South). E-mail: tyoo{at}snu.ac.kr

Abbreviations: CVD, cardiovascular disease


   INTRODUCTION
TOP
 INTRODUCTION
RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 REFERENCES
 
Metabolic syndrome is highly prevalent in the U.S. (age-adjusted prevalence of 23.7%) (1) and in Korea (20.8% for men and 26.9% for women) (2). This syndrome is well documented to increase the risk for developing type 2 diabetes and cardiovascular diseases (CVDs) and is associated with an all-cause mortality (3–5). Physical inactivity, excessive weight gain, high alcohol intake, and certain dietary factors have been identified as important modifiable risk factors for metabolic syndrome and its consequences (2,6,7).

Smoking is also a strong risk factor for atherosclerosis and CVD, with a dose-dependent relationship (8). Smokers have abnormalities in lipoprotein metabolism (9) and endothelial function (10). Moreover, there is some evidence that smokers are at greater risk than nonsmokers of becoming insulin resistant and hyperinsulinemic (11,12). Thus, based on these findings, smoking may be considered as an important modifiable risk factor for metabolic syndrome. However, this relationship has not been clarified, and reports on this issue are also scarce. The aim of this study was to search for associations between smoking and metabolic syndrome with a representative population-based sample in Korea.


   RESEARCH DESIGN AND METHODS
TOP
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
RESULTS
 CONCLUSIONS
 REFERENCES
 
This study was based on the 1998 Korea National Health and Nutrition Examination Survey. Selection methods for a nationwide representative sample of Koreans and other survey methods were detailed elsewhere (2). Complete data were obtained for 9,771 of 10,876 individuals (89.8%) who participated in the Health Examination Study. We restricted our analyses to men because the proportion of Korean women who smoked was too small (8.3%) to allow detailed analyses (2). Finally, data from 3,452 men ≥20 years of age formed the basis of this analysis.

The surveys included questions about age, education level, occupation, income, marital status, smoking habits, alcohol consumption, exercise, previous and current diseases, and family disease history, among others. The nutrition survey employed in this study assessed daily energy and nutrient intakes by using 24-h recall and a food-intake frequency method.

Past smokers were defined as those who had abstained from smoking for >3 months at the time of examination. Information on the daily smoking habits of current smokers was obtained from questions about the average number of cigarettes smoked daily during the month before the interview. Because participants often reported their current smoking amounts by the unit of pack (20 cigarettes), five categories were established: <10, 10–19, 20–29, 30–39, and ≥40 cigarettes/day. The total number of pack-years of cigarettes smoked was also calculated from the total number of years spent smoking multiplied by the number of packs smoked daily. Total pack-years were divided into quartiles for the analyses.

The 2001 definition of metabolic syndrome provided by the National Cholesterol Education Program Adult Treatment Panel III was used (13). However, because Asians have greater risk of fitting the metabolic profile at lower waist circumferences than Caucasians (14), we used the abdominal obesity guidelines for waist circumference (>90 cm for men and >80 cm for women) suggested by the 1998 World Health Organization Asian Pacific Guideline (14). Multiple logistic regression was used to calculate odds ratios (ORs). After several models were tested using a hierarchical approach, a model adjusted for age, education level, exercise, alcohol consumption, weight change during the past year, and amount of dietary fat and fiber consumed was constructed. The linear trend in the OR was evaluated using the trend test.


   RESULTS
TOP
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
CONCLUSIONS
 REFERENCES
 
Table 1 shows that current smoking amounts had a statistically significant dose-dependent association with metabolic syndrome (P = 0.023 for trend). In the analyses of the individual components of metabolic syndrome, high triglycerides and low HDL cholesterol showed statistically significant dose-dependent associations. When the analyses were confined to current smokers, there was a positive dose-dependent association between current smoking amount and abdominal obesity (P = 0.002 for trend, not shown in Table 1).


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  		Table 1— Adjusted ORs of metabolic syndrome and its components according to current smoking amounts

 
Total pack-years of cigarettes smoked during a subject’s lifetime also showed significant dose-dependent associations with metabolic syndrome (P = 0.040 for trend, not shown in Table 1). Similar to the results of current smoking amounts, high triglycerides and low HDL cholesterol had a significant dose-dependent association with total pack-years. We could also find significant dose-dependent associations across the quartiles of total pack-years after exclusion of never smokers (P = 0.003 for trend, not shown in Table 1).


   CONCLUSIONS
TOP
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
REFERENCES
 
Of the components of metabolic syndrome, high triglycerides, low HDL cholesterol, and abdominal obesity are thought to be the main contributors to the association. In contrast to our expectations, we could not find associations of smoking with high fasting glucose and high blood pressure. There have been inconsistent epidemiologic findings from previous studies on this issue. However, recent well-established evidence supports the associations of smoking with hypertension (15,16) and type 2 diabetes (17,18). We suppose that the cross-sectional design of this study limited its ability to detect these associations.

When the analyses were restricted to smokers, we found that an increased amount of smoking tended to be positively associated with abdominal obesity. This finding is somewhat contrary to the general concept that smokers have lower anthropometric indexes than never- smokers (19). However, results from other recent studies showed that increased smoking amounts can contribute to abdominal obesity (20–22); this is consistent with our findings. Although a precise mechanism explaining the association remains to be elucidated, we did find that increased smoking amounts are associated with abdominal obesity and can aggravate metabolic syndrome in smokers.

The strengths of this study were that the study subjects were a representative population-based sample of Koreans and that the analyses were conducted with adjustments for various possible confounders. However, our study has some limitations. First, we could not demonstrate this association for women because of their lower smoking rate. Second, the cross-sectional design of this study prohibited us from concluding causal relationships and may have included some biases.

In conclusion, these population-based data support the hypothesis that cigarette smoking is independently associated with metabolic syndrome. However, further studies are needed to elucidate the underlying mechanisms and the causal effects of smoking on metabolic syndrome.


   Acknowledgments
 
We thank the Korea Institute for Health and Social Affairs (KIHASA) for providing the 1998 Korea National Health and Nutrition Examination Survey data.


   Footnotes
 
A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received for publication April 25, 2005. Accepted for publication April 25, 2005.


   REFERENCES
TOP
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 REFERENCES
 

  1. Ford ES, Giles WH, Dietz WH: Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey. JAMA 287:356–359, 2002[Abstract/Free Full Text]
  2. Yoon YS, Oh SW, Baik HW, Park HS, Kim WY: Alcohol consumption and the metabolic syndrome in Korean adults: the 1998 Korean National Health and Nutrition Examination Survey. Am J Clin Nutr 80:217–224, 2004[Abstract/Free Full Text]
  3. Hanson RL, Imperatore G, Bennett PH, Knowler WC: Components of the "metabolic syndrome" and the incidence of type 2 diabetes. Diabetes 51:3120–3127, 2002[Abstract/Free Full Text]
  4. Isomaa B, Almgren P, Tuomi T, Forsen B, Lahti K, Nissen M, Taskinen MR, Groop L: Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care 24:683–689, 2001[Abstract/Free Full Text]
  5. Lakka H-M, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, Tuomilehto J, Salonen JT: The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. JAMA 288:2909–2916, 2002
  6. Carnethon MR, Loria CM, Hill JO, Sidney S, Savage PJ, Liu K: Risk factors for the metabolic syndrome: the Coronary Artery Risk Development in Young Adults (CARDIA) study, 1985–2001. Diabetes Care 27:2707–2715, 2004[Abstract/Free Full Text]
  7. Yoo S, Nicklas T, Baranowski T, Zakeri IF, Yang SJ, Srinivasan SR, Berenson GS: Comparison of dietary intakes associated with metabolic syndrome risk factors in young adults: the Bogalusa Heart Study. Am J Clin Nutr 80:841–848, 2004[Abstract/Free Full Text]
  8. Kannel WB: Update on the role of cigarette smoking in coronary artery disease. Am Heart J 101:319–328, 1981[Medline]
  9. Kong C, Nimmo L, Elatrozy T, Anyaoku V, Hughes C, Robinson S, Richmond W, Elkeles RS: Smoking is associated with increased hepatic lipase activity, insulin resistance, dyslipidaemia and early atherosclerosis in type 2 diabetes. Atherosclerosis 156:373–378, 2001[Medline]
  10. Heitzer T, Yla-Herttuala S, Luoma J, Kurz S, Munzel T, Just H, Olschewski M, Drexler H: Cigarette smoking potentiates endothelial dysfunction of forearm resistance vessels in patients with hypercholesterolemia: role of oxidized LDL. Circulation 9:1346–1353, 1996
  11. Facchini FS, Hollenbeck CB, Jeppesen J, Chen YD, Reaven GM: Insulin resistance and cigarette smoking. Lancet 339:1128–1130, 1992[Medline]
  12. Ronnemaa T, Ronnemaa EM, Puukka P, Pyorala K, Laakso M: Smoking is independently associated with high plasma insulin levels in nondiabetic men. Diabetes Care 19:1229–1232, 1996[Abstract]
  13. National Cholesterol Education Program, National Heart, Lung and Blood Institute, National Institutes of Health: National Cholesterol Education Program Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III): Executive Summary. Bethesda, MD, National Institutes of Health, 2001. (National Institutes of Health publication no. 01-3670)
  14. World Health Organization Western Pacific Region, International Association for the Study of Obesity, International Obesity Task Force: The Asia-Pacific Perspective: Redefining Obesity and its Treatment. Sydney: Health Communications Australia, 2000
  15. Elliott JM, Simpson FO: Cigarettes and accelerated hypertension. N Z Med J 91:447–449, 1980[Medline]
  16. Dyer AR, Stamler J, Shekelle RB, Schoenberger JA, Stamler R, Shekelle S, Berkson DM, Paul O, Lepper MH, Lindberg HA: Pulse pressure. II. Factors associated with follow-up values in three Chicago epidemiologic studies. J Chronic Dis 35:275–282, 1982[Medline]
  17. Rimm EB, Chan J, Stampfer MJ, Colditz GA, Willett WC: Prospective study of cigarette smoking, alcohol use, and the risk of diabetes in men. BMJ 310:555–559, 1995[Abstract/Free Full Text]
  18. Feskens EJ, Kromhout D: Cardiovascular risk factors and the 25-year incidence of diabetes mellitus in middle-aged men: the Zutphen Study. Am J Epidemiol 130:1101–1108, 1989[Abstract/Free Full Text]
  19. Ferrara CM, Kumar M, Nicklas B, McCrone S, Goldberg AP: Weight gain and adipose tissue metabolism after smoking cessation in women. Int J Obes 25:1322–1326, 2001
  20. Bamia C, Trichopoulou A, Lenas D, Trichopoulos D: Tobacco smoking in relation to body fat mass and distribution in a general population sample. Int J Obes Relat Metab Disord 28:1091–1096, 2004[Medline]
  21. Shimokata H, Muller DC, Andres R: Studies in the distribution of body fat. III. Effects of cigarette smoking. JAMA 261:1169–1173, 1989[Abstract]
  22. Barrett-Connor E, Khaw K: Cigarette smoking and increased central adiposity. Ann Intern Med 111:783–787, 1989

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