Original Article

Obesity (2006) 14, 1654–1661; doi: 10.1038/oby.2006.190

Impaired Lung Function Is Associated with Obesity and Metabolic Syndrome in Adults*

Wen-Yuan Lin*,†,‡, Chien-An Yao*, Hao-Chien Wang§, and Kuo-Chin Huang*

  1. *Department of Family Medicine, National Taiwan University Hospital, Taipei, Taiwan;
  2. §Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan;
  3. †Department of Family Medicine, China Medical University Hospital, Taichung, China;
  4. ‡Department of Family Medicine, College of Medicine, China Medical University, Taichung, China;
  5. Division of Chest, Department of Internal Medicine, Far Eastern Memorial Hospital, Taipei County, Taiwan.

Correspondence: Kuo-Chin Huang Department of Family Medicine, National Taiwan University Hospital, 7 Chung-Shan South Road, Taipei, Taiwan 100. E-mail: chin3@ha.mc.ntu.edu.tw

*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 12 December 2005; Accepted 19 June 2006.

Top

Abstract

Objective: Impaired lung function is associated with obesity and insulin resistance. In this study, we investigated the relationship between metabolic syndrome and impaired lung function in adults.

Research Methods and Procedures: A total of 46,514 subjects 20 years and over (21,669 men and 24,845 women, mean age = 37.3 plusminus 11.2 and 37.0 plusminus 11.3 years, respectively) were recruited from four nationwide MJ Health Screening Centers in Taiwan from 1998 to 2000. Metabolic syndrome was defined using the National Cholesterol Education Panel (NCEP) metabolic syndrome criteria or America Heart Association/National Heart Lung Blood Institute (AHA/NHLBI) criteria. The relationship between metabolic syndrome and lung function test was examined using multivariate logistic regression analysis.

Results: The prevalence of impaired lung function was 11.1% in men and 14.0% in women. The prevalence of metabolic syndrome was 5.8% using NCEP criteria and 12.8% using AHA/NHLBI criteria. In multivariate logistic regression analysis with adjustment for age, gender, BMI, smoking, alcohol drinking, and physical activity, restrictive lung impairment was independently associated with increased risk of having metabolic syndrome (p < 0.01, odds ratios = 1.221 using NCEP criteria and 1.150 using AHA/NHLBI criteria).

Discussion: Obesity and metabolic syndrome were associated with impaired lung function in adults in Taiwan. Our results imply that obesity and insulin resistance may be the common pathways underlying lung function impairment and metabolic syndrome. Moreover, lung function test may be applied as an additional evaluation for metabolic syndrome in a clinical setting.

Keywords:

metabolic syndrome, spirometry, restrictive, obstructive, lifestyle

Top

Introduction

Increased lung function impairment has been found in connection with cardiovascular and all-cause mortalities (1, 2, 3, 4, 5). Decreased forced expiratory volume in 1 second (FEV1),1 for example, is an independent predictor for mortalities (2, 4, 5). The presence of obstructive or restrictive lung diseases as assessed by spirometry is associated with a higher risk of death (3). In addition, lung function impairment is also associated with insulin resistance (6, 7), type 2 diabetes (7, 8), and cardiovascular diseases (9, 10). Therefore, lung function test may be commonly used as a tool in general health assessment.

The metabolic syndrome, a constellation of impaired glucose metabolism, dyslipidemia, hypertension, and central obesity, is associated with subsequent development of type 2 diabetes (11, 12). It also increases the risk of cardiovascular diseases and mortality (12, 13, 14, 15). The metabolic syndrome is a common metabolic disorder that may result from the increasing prevalence of obesity. Depending on the criteria used, the prevalence of metabolic syndrome in the United States and Europe is approx20% to 30% in adults (16, 17, 18), whereas in Asians, the prevalence is approx10% to 20% (18, 19, 20, 21). Therefore, metabolic syndrome has become one of the major public health challenges worldwide.

It has been well known that a common mechanism, such as insulin resistance and/or obesity, underlies metabolic syndrome (22, 23, 24, 25, 26). The purpose of this study was to examine the relationship between lung function impairment and metabolic syndrome in a large adult population.

Top

Research Methods and Procedures

Subjects and Measurements

The data were collected from four nationwide MJ Health Screening Centers in Taiwan from 1998 to 2000. The details of MJ centers have been described elsewhere (21). To avoid possible factors affecting the results of the lung function test, subjects with any history of or medication for major systemic diseases such as diabetes, hypertension, asthma, chronic lung diseases, or autoimmune diseases were excluded. A total of 46,941 healthy adults out of 225,513 subjects were recruited for this study. Among them, there were 427 subjects who did not have complete laboratory data. Therefore, 46,514 subjects were available for our final analysis. Ethics approval for patient recruitment and analysis of the data were obtained from the MJ Research Foundation Review Committee in Taiwan.

The anthropometric characteristics, blood pressure, plasma glucose, and lipid levels, were measured and described by Huang et al. (27). Metabolic syndrome was defined clinically, based on the presence of three or more of the following National Cholesterol Education Panel (NCEP) metabolic syndrome criteria (28): central obesity [ (waist circumference (WC) > 102 cm in men and >88 cm in women)] , a high triglyceride level (greater than or equal to1.695 mM), a low high-density lipoprotein-cholesterol (HDL-C) level (<1.036 mM for men and <1.295 mM for women), high blood pressure (greater than or equal to130/85 mm Hg), and a high fasting plasma glucose concentration (greater than or equal to6.1 mM). Furthermore, the America Heart Association/National Heart Lung Blood Institute (AHA/NHLBI) criteria using a lower WC cut-off (WC greater than or equal to 90 cm in men and greater than or equal to 80 cm in women) and a lower fasting glucose level (greater than or equal to5.55 mM) were also applied for comparison (29).

Lung function test was performed in every participant by an experienced technician using an automated flow-sensing spirometer (Microspiro HI-500, Tokyo, Japan) based on American Thoracic Society recommendations (30), with all subjects seated and using a dry rolling-seal spirometer calibrated by using 1 or 3 liters of precision syringe daily. If at all possible, at least three and up to a maximum of eight forced expiratory maneuvers were performed in an effort to meet the American Thoracic Society standards. Values used in the study were the forced vital capacity (FVC), FEV1, and FEV1-to-FVC ratio. The highest FVC and FEV1 value of the three or more tests with acceptable curves was used in the analysis. Obstructive lung impairment was defined as an FEV1-to-FVC ratio < 70% and an FVC > 80% of the predicted value. Restrictive lung impairment was defined as an FVC < 80% of the predicted value and an FEV1-to-FVC ratio > 70% . Mixed lung impairment was defined as a FEV1-to-FVC ratio < 70% and FVC < 80% of the predicted value. The other was defined as normal lung function (30, 31).

Smoking, alcohol drinking, and physical activity histories for each subject were obtained from a questionnaire. Current, former, and never smokers were defined as those who reported the current use, any prior use, and no use of cigarettes, respectively, at the time of survey. Current and never alcohol drinkers were defined as those who reported drinking alcohol at least 1 time/wk and <1 time/wk, respectively. Physical activity was divided into three levels. None/mild physical activity was defined as those who exercised <1 h/wk. Moderate physical activity was defined as those who exercised between 1 and 4 h/wk. Vigorous physical activity was defined as those who exercised >5 h/wk.

Statistical Analyses

The data are presented as the means and standard deviation unless indicated otherwise. The frequency of metabolic syndrome and its components was calculated for participants according to the results of a lung function test. The Wald chi2 test was used to evaluate the statistical significance and odds ratios (ORs) of the prevalence rates of the metabolic syndrome. Multiple logistic regression analysis was used to estimate the ORs of the metabolic syndrome by age, gender, BMI, types of lung function impairment, smoking, alcohol drinking, and physical activity histories. These statistical analyses were performed using the SPSS/PC statistical program (version 11.0 for Windows; SPSS, Inc., Chicago, IL).

Top

Results

The means of age, weight, height, BMI, and WC were higher in men than in women (Table 1). The prevalence of metabolic syndrome was 5.8% using NCEP criteria and 12.8% using AHA/NHLBI criteria. Men had a higher prevalence of the metabolic syndrome, central obesity using AHA/NHLBI criteria, high blood pressure, high fasting glucose, high triglycerides, current smoking and alcohol drinking histories, and moderate to vigorous physical activity than women. However, the prevalences of lung function impairment, central obesity using NCEP criteria, and low HDL-C were lower in men (11.1% , 1.0% , and 33.1% ) than in women (14.0% , 2.5% , and 34.1% ).


The crude ORs of having the metabolic syndrome and its individual components were significantly higher in subjects with lung function impairment than in those with normal lung function (OR > 1, p < 0.05 in each analysis; Table 2). The crude ORs of the metabolic syndrome were 2.29 (1.90 in men and 3.12 in women) using NCEP criteria and 2.10 (1.82 in men and 2.82 in women) using AHA/NHLBI criteria. However, the association between lung function impairment and metabolic syndrome was attenuated when adjusted for age, smoking, and other variables such as BMI, alcohol drinking, and physical activity. The prevalence of lung function impairment increased in the underweight, overweight, and obese subjects compared with the subjects with normal weight (Figure 1A). The prevalence of lung function impairment increased with age in each gender (Figure 1B).

Figure 1.
Figure 1 - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

(A) Relationship between the prevalence of lung function impairment and BMI groups. BMI was divided into four groups using World Health Organization Asia-Pacific criteria (from left to right, bars: BMI < 18.5, 18.5 less than or equal to BMI < 23, 23 less than or equal to BMI < 25, and BMI greater than or equal to 25 kg/m2) in Group 1 and World Health Organization criteria (from left to right, bars: BMI < 18.5, 18.5 less than or equal to BMI < 25, 25 less than or equal to BMI < 30, and BMI greater than or equal to 30 kg/m2) (test for trends, p < 0.001). (B) Age groups stratified by gender (test for trends, p < 0.001).

Full figure and legend (38K)


Using a multivariate logistic regression analysis with the metabolic syndrome as the outcome variable (using NCEP criteria in Model 1 and using AHA/NHLBI criteria in Model 2), we found that age, gender, BMI, types of lung function impairment, and physical activity were independent variables associated with metabolic syndrome in these subjects (Table 3). With increasing age and BMI, the ORs of having metabolic syndrome increased significantly. Compared with the subjects with normal lung function, the subjects with restrictive lung impairment had higher ORs of having the metabolic syndrome in Model 1 (1.221, p < 0.01) and Model 2 (1.150, p < 0.01). The ORs of having the metabolic syndrome were significantly higher in the current than in the never alcohol drinkers in Model 2 (1.249, p < 0.001) and also higher in the current than in the never smokers in Model 2 (1.105, p < 0.05). Moreover, subjects with moderate and vigorous physical activities had lower ORs of having the metabolic syndrome than subjects with mild or no physical activity.


Top

Discussion

In the present study, we found that obesity was related to lung function impairment in a previously healthy population in Taiwan. This was consistent with other studies (32, 33, 34, 35, 36). We also demonstrated that, for the first time, to our knowledge, the prevalence of metabolic syndrome was independently associated with restrictive lung impairment after adjustment for age, gender, BMI, smoking, alcohol drinking, and physical activity either using the NCEP or AHA/NHLBI criteria.

It has been well known that a common mechanism, such as insulin resistance and/or obesity, underlies the metabolic syndrome (22, 23, 24, 25, 26). Obesity has been shown to be inversely related to lung function (32, 33, 34, 35, 36). Fasting serum insulin levels are negatively correlated with FVC and FEV1 (6). Furthermore, insulin resistance assessed by HOMA and prevalence of type 2 diabetes are inversely associated with FVC and FEV1 (7). In addition, it has been shown in 3 prospective studies ((8, 9, 37) that subjects with impaired lung function have an increased risk for developing insulin resistance and type 2 diabetes. Taken together, similarly, obesity and insulin resistance may also play an important role in lung function impairment. Consistently, we found that metabolic syndrome was associated with lung function impairment independently of BMI (see Table 2). Furthermore, restrictive lung impairment was also associated with metabolic syndrome when adjusted for BMI (p < 0.001) and other variables (see Table 3). Therefore, the positive correlation between lung function impairment and metabolic syndrome could be explained by obesity and insulin resistance. These findings also suggest that a lung function test may be applied as an additional evaluation for metabolic syndrome in a clinical setting.

Obese subjects are prone to having reduced FEV1, FVC, and total lung capacity in lung function tests, and they usually present with restrictive lung patterns (36, 38, 39, 40). The possible mechanisms for the abnormal lung function tests in obese patients are reduced chest wall compliance and increased peripheral airway resistance. In addition to the above mechanical factors, adipocytokines could also play an essential role directly or indirectly. For example, serum leptin levels are elevated in obese subjects (41). Previously, we and other groups (42, 43, 44) have reported that plasma leptin levels are independently associated with insulin resistance after adjustment for possible confounders in non-diabetic subjects. Interestingly, Sin et al. (45) have found that serum leptin levels are elevated in adults of normal weight with impaired lung function. Therefore, leptin may also play a role in the pathogenesis of impaired lung function. This deserves further research in the future.

Subjects with metabolic syndrome are at increased risk for type 2 diabetes, cardiovascular diseases, and mortality (11, 12, 13, 14, 15). In addition to obesity and insulin resistance, systemic inflammation may also play an important role. Rutter et al. (46) have found, for example, that elevated CRP levels are related to metabolic syndrome. Furthermore, measurement of CRP levels adds prognostic information on the subsequent risk of cardiovascular events related to metabolic syndrome (47). On the other hand, increased CRP levels are strongly and independently associated with lung function impairment (48, 49). Taken together, inflammation may also be an element in the link between lung function impairment and metabolic syndrome.

The prevalence of lung function impairment increased with age in our present study (Figure 1), which was comparable with the other studies (6, 36, 50, 51). Insulin resistance can be induced by smoking (52). Smoking is a known risk factor for metabolic syndrome (53). Similarly, our study showed that the prevalence of metabolic syndrome was higher in the current smokers than in non-smokers (Table 3). However, we did not have a complete smoking history including pack-years of smoking in the study. Therefore, by comparing restrictive lung function impairment vs. normal lung function, the observed small increase in OR (22.1% in Model 1 and 15.0% in Model 2, Table 3) of having metabolic syndrome could be due to residual confounding by smoking. In addition, moderate to vigorous physical activities have been noted to protect against the development of type 2 diabetes, cardiovascular diseases, and metabolic syndrome (54, 55, 56, 57, 58). Similarly, our study showed that the prevalence of metabolic syndrome was lower in subjects with moderate to vigorous physical activities (Table 3). However, the odds of having metabolic syndrome were higher in the current alcohol drinkers than in non-alcohol drinkers in the present study. This finding was different from the observation of Rosell et al. (59).

In summary, we found that obesity and metabolic syndrome were related to lung function impairment in adults. Subjects with lung function impairment were associated with a higher risk of having metabolic syndrome and its individual components, as compared with subjects without lung function impairment. Therefore, a lung function test may be applied as an additional evaluation for metabolic syndrome in a clinical setting. Although our study was limited by the cross-sectional design, and there was potential bias by the subjects, our results suggested that lung function impairment may be regarded as the pulmonary manifestation of metabolic syndrome. The interplay between lung function and the metabolic syndrome in humans merits further study.

Top

Notes

1 Nonstandard abbreviations: FEV1, forced expiratory volume in 1 second; NCEP, National Cholesterol Education Panel; WC, waist circumference; HDL-C, high-density lipoprotein-cholesterol; AHA/NHLBI, America Heart Association/National Heart Lung Blood Institute; FVC, forced vital capacity; OR, odds ratio.

Top

References

  1. Lange, P, Nyboe, J, Jensen, G, Schnohr, P, Appleyard, M. (1991) Ventilatory function impairment and risk of cardiovascular death and of fatal or non-fatal myocardial infarction. Eur Respir J. 4: 1080–1087.
  2. Schunemann, HJ, Dorn, J, Grant, BJB, Winkelstein, W, Jr, Trevisan, M (2000) Pulmonary function is a long-term predictor of mortality in the general population: 29-year follow-up of the Buffalo Health Study. Chest. 118: 656–664. | Article | PubMed | ChemPort |
  3. Mannino, DM, Buist, AS, Petty, TL, Enright, PL, Redd, SC. (2003) Lung function and mortality in the United States: data from the First National Health and Nutrition Examination Survey follow up study. Thorax. 58: 388–393.
  4. Sin, DD, Wu, LL, Man, SFP. (2005) The relationship between reduced lung function and cardiovascular mortality: a population-based study and a systematic review of the literature. Chest. 127: 1952–1959.
  5. Stavem, K, Aaser, E, Sandvik, L, et al (2005) Lung function, smoking and mortality in a 26-year follow-up of healthy middle-aged males. Eur Respir J. 25: 618–625.
  6. Lazarus, R, Sparrow, D, Weiss, ST. (1998) Baseline ventilatory function predicts the development of higher levels of fasting insulin and fasting insulin resistance index: the Normative Aging Study. Eur Respir J. 12: 641–645.
  7. Lawlor, DA, Ebrahim, S, Smith, GD. (2004) Associations of measures of lung function with insulin resistance and Type 2 diabetes: findings from the British Womens Heart and Health Study. Diabetologia. 47: 195–203.
  8. Yeh, HC, Punjabi, NM, Wang, NY, Pankow, JS, Duncan, BB, Brancati, FL. (2005) Vital capacity as a predictor of incident type 2 diabetes: The Atherosclerosis Risk in Communities study. Diabetes Care. 28: 1472–1479.
  9. Engstrom, G, Hedblad, B, Nilsson, P, Wollmer, P, Berglund, G, Janzon, L. (2003) Lung function, insulin resistance and incidence of cardiovascular disease: a longitudinal cohort study. J Intern Med. 253: 574–581.
  10. Schroeder, EB, Welch, VL, Couper, D, et al (2003) Lung function and incident coronary heart disease: The Atherosclerosis Risk in Communities Study. Am J Epidemiol. 158: 1171–1181. | Article | PubMed |
  11. Hanson, RL, Imperatore, G, Bennett, PH, Knowler, WC. (2002) Components of the "metabolic syndrome" and incidence of type 2 diabetes. Diabetes. 51: 3120–3127. | Article | PubMed | ISI | ChemPort |
  12. Klein, BE, Klein, R, Lee, KE. (2002) Components of the metabolic syndrome and risk of cardiovascular disease and diabetes in beaver dam. Diabetes Care. 25: 1790–1794. | Article | PubMed | ISI |
  13. Pyorala, M, Miettinen, H, Halonen, P, Laakso, M, Pyorala, K. (2000) Insulin resistance syndrome predicts the risk of coronary heart disease and stroke in healthy middle-aged men: the 22-year follow-up results of the Helsinki Policemen Study. Arterioscler Thromb Vasc Biol. 20: 538–544. | PubMed | ISI | ChemPort |
  14. Isomaa, B, Almgren, P, Tuomi, T, et al (2001) Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care. 24: 683–689. | Article | PubMed | ISI | ChemPort |
  15. Lakka, HM, Laaksonen, DE, Lakka, TA, et al (2002) The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. JAMA. 288: 2709–2716. | Article | PubMed | ISI |
  16. Ford, ES, Giles, WH, Dietz, WH. (2002) Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey. JAMA. 287: 356–359. | Article | PubMed | ISI |
  17. Panagiotakos, DB, Pitsavos, C, Chrysohoou, C, et al (2004) Impact of lifestyle habits on the prevalence of the metabolic syndrome among Greek adults from the ATTICA study. Am Heart J. 147: 106–112. | Article | PubMed | ISI |
  18. Eckel, RH, Grundy, SM, Zimmet, PZ. (2005) The metabolic syndrome. Lancet. 365: 1415–1428. | Article | PubMed | ISI | ChemPort |
  19. Park, HS, Oh, SW, Cho, SI, Choi, WH, Kim, YS. (2004) The metabolic syndrome and associated lifestyle factors among South Korean adults. Int J Epidemiol. 33: 328–336. | Article | PubMed | ISI |
  20. Tan, CE, Ma, S, Wai, D, Chew, SK, Tai, ES. (2004) Can we apply the National Cholesterol Education Program Adult Treatment Panel definition of the metabolic syndrome to Asians? Diabetes Care. 27: 1182–1186. | Article | PubMed | ISI |
  21. Shen, YH, Yang, WS, Lee, TH, Lee, LT, Chen, CY, Huang, KC. (2005) Bright liver and alanine aminotransferase are associated with metabolic syndrome in adults. Obes Res. 13: 1238–1245. | PubMed | ChemPort |
  22. Alberti, KG, Zimmet, PZ. (1998) Definition, diagnosis and classification of diabetes mellitus and its complications: I. Diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabetic Med. 15: 539–553. | Article | PubMed | ISI | ChemPort |
  23. Balkau, B, Charles, MA. (1999) Comment on the provisional report from the WHO consultation: European Group for the Study of Insulin Resistance (EGIR). Diabetic Med. 16: 442–443. | PubMed |
  24. Maison, P, Byrne, CD, Hales, CN, Day, NE, Wareham, NJ. (2001) Do different dimensions of the metabolic syndrome change together over time? Evidence supporting obesity as the central feature. Diabetes Care. 24: 1758–1763. | PubMed | ISI | ChemPort |
  25. Reaven, GM. (2002) Metabolic syndrome: pathophysiology and implications for management of cardiovascular disease. Circulation. 206: 286–288. | Article |
  26. Cheal, KL, Abbasi, F, Lamendola, C, McLaughlin, T, Reaven, GM, Ford, ES. (2004) Relationship to insulin resistance of the adult treatment panel III diagnostic criteria for identification of the metabolic syndrome. Diabetes. 53: 1195–1200. | Article | PubMed | ISI | ChemPort |
  27. Huang, KC, Lin, WY, Lee, LT, et al (2002) Four anthropometric indices and cardiovascular risk factors in Taiwan. Int J Obes Relat Metab Disord. 26: 1060–1068. | Article | PubMed |
  28. National Cholesterol Education Program (2001) Executive summary of the third report of the National Cholesterol Education Program (NCEP) Expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA. 285: 2486–2497. | Article | PubMed | ISI |
  29. Grundy, SM, Cleeman, JI, Daniels, SR, et al (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute scientific statement. Circulation. 112: 2735–2752. | Article | PubMed | ISI |
  30. American Thoracic Society (1995) American Thoracic Society: standardization of spirometry, 1994 update. Am J Respir Crit Care Med. 152: 1107–1136. | PubMed | ISI |
  31. Evans, SE, Scanlon, PD. (2003) Current practice in pulmonary function testing. Mayo Clin Proc. 78: 758–763.
  32. Kannel, WB, Cupples, LA, Ramaswami, R, Stokes, J, 3rd, Kreger, BE, Higgins, M (1991) Regional obesity and risk of cardiovascular disease; the Framingham Study. J Clin Epidemiol. 44: 183–190. | Article | PubMed | ISI | ChemPort |
  33. Chinn, DJ, Cotes, JE, Reed, JW. (1996) Longitudinal effects of change in body mass on measurements of ventilatory capacity. Thorax. 51: 699–704.
  34. Lazarus, R, Gore, CJ, Booth, M, Owen, N. (1998) Effects of body composition and fat distribution on ventilatory function in adults. Am J Clin Nutr. 68: 35–41. | PubMed | ChemPort |
  35. Carey, IM, Cook, DG, Strachan, DP. (1999) The effects of adiposity and weight change on forced expiratory volume decline in a longitudinal study of adults. Int J Obes Relat Metab Disord. 23: 979–985. | Article | PubMed | ChemPort |
  36. Canoy, D, Luben, R, Welch, A, et al (2004) Abdominal obesity and respiratory function in men and women in the EPIC-Norfolk Study, United Kingdom. Am J Epidemiol. 159: 1140–1149. | Article | PubMed | ISI | ChemPort |
  37. Ford, ES, Mannino, DM. (2004) Prospective association between lung function and the incidence of diabetes: findings from the National Health and Nutrition Examination Survey Epidemiologic Follow-Up Study. Diabetes Care. 27: 2966–2970.
  38. Collins, LC, Hoberty, PD, Walker, JF, Fletcher, EC, Peiris, AN. (1995) The effect of body fat distribution on pulmonary function tests. Chest. 107: 1298–1302. | Article | PubMed | ChemPort |
  39. Sahebjami, H, Gartside, PS. (1996) Pulmonary function in obese subjects with a normal FEV1/FVC ratio. Chest. 110: 1425–1429. | PubMed | ChemPort |
  40. Li, AM, Chan, D, Wong, E, Yin, J, Nelson, EAS, Fok, TF. (2003) The effects of obesity on pulmonary function. Arch Dis Child. 88: 361–363. | Article | PubMed | ChemPort |
  41. Considine, RV, Sinha, MK, Heiman, ML, et al (1996) Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med. 334: 292–295. | Article | PubMed | ISI | ChemPort |
  42. Donahue, RP, Prineas, RJ, Donahue, RD, et al (1999) Is fasting leptin associated with insulin resistance among nondiabetic individuals? The Miami Community Health Study. Diabetes Care. 22: 1092–1096. | PubMed |
  43. Zimmet, P, Boyko, EJ, Collier, GR, de Courten, M. (1999) Etiology of the metabolic syndrome: potential role of insulin resistance, leptin resistance, and other players. Ann N Y Acad Sci. 892: 25–44.
  44. Huang, KC, Lin, RC, Kormas, N, et al (2004) Plasma leptin is associated with insulin resistance independent of age, body mass index, fat mass, lipids, and pubertal development in nondiabetic adolescents. Int J Obes Relat Metab Disord. 28: 470–475. | Article |
  45. Sin, DD, Man, SFP. (2003) Impaired lung function and serum leptin in men and women with normal body weight: a population based study. Thorax. 58: 695–698.
  46. Rutter, MK, Meigs, JB, Sullivan, LM, D'Agostino, RB, Wilson, PWF. (2004) C-reactive protein, the metabolic syndrome, and prediction of cardiovascular events in the Framingham Offspring Study. Circulation. 110: 380–385. | Article | PubMed | ChemPort |
  47. Ridker, PM, Buring, JE, Cook, NR, Rifai, N. (2003) C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: an 8-year follow-up of 14719 initially healthy American women. Circulation. 107: 391–397. | Article | PubMed | ISI |
  48. Kony, S, Zureik, M, Driss, F, Neukirch, C, Leynaert, B, Neukirch, F. (2004) Association of bronchial hyperresponsiveness and lung function with C-reactive protein (CRP): a population based study. Thorax. 59: 892–896.
  49. Gan, WQ, Man, SFP, Sin, DD. (2005) The interactions between cigarette smoking and reduced lung function on systemic inflammation. Chest. 127: 558–564.
  50. Hankison, JL, Odencrantz, JR, Fedan, KB. (1999) Spirometric reference values from a sample of the general U.S. population. Am J Respir Crit Care Med. 159: 179–187. | PubMed | ISI | ChemPort |
  51. Mannino, DM, Gagnon, RC, Petty, TL, Lydick, E. (2000) Obstructive lung disease and low lung function in adults in the United States: data from the National Health and Nutrition Examination Survey, 1988–1994. Arch Intern Med. 160: 1683–1689.
  52. Attvall, S, Fowelin, J, Lager, I, Von Schenck, H, Smith, U. (1993) Smoking induces insulin resistance: a potential link with the insulin resistance syndrome. J Intern Med. 233: 327–332.
  53. Park, YW, Zhu, S, Palaniappan, L, Heshka, S, Carnethon, MR, Heymsfield, SB. (2003) The metabolic syndrome: prevalence and associated risk factor findings in the US population from the Third National Health and Nutrition Examination Survey, 1988–1994. Arch Intern Med. 163: 427–436. | Article | PubMed | ISI |
  54. Lynch, J, Helmrich, SP, Lakka, TA, et al (1996) Moderately intense physical activities and high levels of cardiorespiratory fitness reduce the risk of non-insulin-dependent diabetes mellitus in middle-aged men. Arch Intern Med. 156: 1307–1314. | PubMed |
  55. Brunner, EJ, Marmot, MG, Nanchahal, K, et al (1997) Social inequality in coronary risk: central obesity and the metabolic syndrome: evidence from the Whitehall II study. Diabetologia. 40: 1341–1349. | Article | PubMed | ISI | ChemPort |
  56. Laukkanen, JA, Lakka, TA, Rauramaa, R, et al (2001) Cardiovascular fitness as a predictor of mortality in men. Arch Intern Med. 161: 825–831. | PubMed |
  57. Laaksonen, DE, Lakka, HM, Salonen, JT, Niskanen, LK, Rauramaa, R, Lakka, TA. (2002) Low levels of leisure-time physical activity and cardiorespiratory fitness predict development of the metabolic syndrome. Diabetes Care. 25: 1612–1618.
  58. Lakka, TA, Laaksonen, DE, Lakka, HM, et al (2003) Sedentary lifestyle, poor cardiorespiratory fitness, and the metabolic syndrome. Med Sci Sports Exerc. 35: 1279–1286.
  59. Rosell, M, De Faire, U, Hellenius, ML. (2003) Low prevalence of the metabolic syndrome in wine drinkers–is it the alcohol beverage or the lifestyle? Eur J Clin Nutr. 57: 227–234. | Article | PubMed | ChemPort |
Top

Acknowledgments

We thank Dr. Steven Kaufman for kindly reviewing the manuscript. There was no funding/outside support for this study.

Extra navigation

.
ADVERTISEMENT