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Diabetes, Impaired Glucose Tolerance, and Metabolic Biomarkers in Individuals with Normal Glucose Tolerance are Inversely Associated with Lung Function: The Jackson Heart Study

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Abstract

The objectives of this study were to test the hypothesis that diabetes and impaired glucose tolerance (IGT), diabetes control and diabetes duration, and metabolic biomarkers in adults with normal glucose tolerance (NGT) are inversely associated with spirometry-measured lung function. We conducted a cross-sectional observational cohort study that included nonsmoking African American adults (n = 2,945; mean age = 52.5 ± 12.6 years; 69.2% female), who were free of cardiovascular disease, from the Jackson Heart Study. The interventions were diabetes, metabolic biomarkers and lung function. We measured the associations of glycemia with forced expiratory volume (FEV) in 1 s, FEV in 6 s, and vital capacity. Multivariable adjusted mean lung function values were lower among adults with diabetes and IGT (in women only, but not after adjustment for waist circumference) than adults with NGT. Among adults with diabetes, no associations were observed between lung function and diabetes control or duration. In women with NGT, lower lung function was consistently associated with higher glucose levels and less consistently with higher insulin levels and insulin resistance. Lower lung function was consistently associated with higher insulin levels and insulin resistance and less consistently associated with insulin and hemoglobin A1c in men with NGT. Overall, our findings generally support the hypothesis that diabetes, IGT, and increased levels of metabolic biomarkers in individuals with NGT are inversely associated with lung function in African Americans, independent of adiposity.

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References

  1. Rodriguez BL, Masaki K, Burchfiel C, Curb JD, Fong KO, Chyou PH, Marcus EB (1994) Pulmonary function decline and 17-year total mortality: the Honolulu Heart Program. Am J Epidemiol 140:398–408

    PubMed  CAS  Google Scholar 

  2. Bang KM, Gergen PJ, Kramer R, Cohen B (1993) The effect of pulmonary impairment on all-cause mortality in a national cohort. Chest 103:536–540

    Article  PubMed  CAS  Google Scholar 

  3. Hankinson JL, Odencrantz JR, Fedan KB (1999) Spirometric reference values from a sample of the general US population. Am J Respir Crit Care Med 159:179–187

    PubMed  CAS  Google Scholar 

  4. Menacker F, Martin JA (2008) Expanded health data from the new birth certificate, 2005. Natl Vital Stat Rep 56:1–24

    PubMed  Google Scholar 

  5. Yeh HC, Punjabi NM, Wang NY, Pankow JS, Duncan BB, Cox CE, Selvin E, Brancati FL (2008) Cross-sectional and prospective study of lung function in adults with type 2 diabetes: the Atherosclerosis Risk In Communities (ARIC) Study. Diabetes Care 31:741–746

    Article  PubMed  Google Scholar 

  6. McKeever TM, Weston PJ, Hubbard R, Fogarty A (2005) Lung function and glucose metabolism: an analysis of data from the third national health and nutrition examination survey. Am J Epidemiol 161:546–556

    Article  PubMed  Google Scholar 

  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 Women’s Heart and Health Study. Diabetologia 47:195–203

    Article  PubMed  CAS  Google Scholar 

  8. Lange P, Groth S, Mortensen J, Appleyard M, Nyboe J, Schnohr P, Schnohr P, Jensen G (1990) Diabetes mellitus and ventilatory capacity: a five year follow-up study. Eur Respir J 3:288–292

    PubMed  CAS  Google Scholar 

  9. Lange P, Groth S, Kastrup J, Mortensen J, Appleyard M, Nyboe J, Jensen G, Schnohr P (1989) Diabetes mellitus, plasma glucose and lung function in a cross-sectional population study. Eur Respir J 2:14–19

    PubMed  CAS  Google Scholar 

  10. Ford ES, Mannino DM, National Health Nutrition Examination Survey Epidemiologic Follow-up Study (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

    Article  PubMed  Google Scholar 

  11. Berclaz PY, Gao H, Tobian JA, Swanson DL, Webb DM, Crapo RO, Jensen RL (2009) The impact of diabetes and age on pulmonary function: data from the national health and nutrition examination survey. Diabetes Res Clin Pract 83:e1–e3

    Article  PubMed  Google Scholar 

  12. Davis WA, Knuiman M, Kendall P, Grange V, Davis TM, Fremantle Diabetes Study (2004) Glycemic exposure is associated with reduced pulmonary function in type 2 diabetes: the Fremantle diabetes study. Diabetes Care 27:752–757

    Article  PubMed  Google Scholar 

  13. Burchfiel CM, Curb JD, Sharp DS, Rodriguez BL, Arakaki R, Chyou PH, Yano K (1995) Distribution and correlates of insulin in elderly men. The Honolulu Heart Program. Arterioscler Thromb Vasc Biol 15:2213–2221

    Article  PubMed  CAS  Google Scholar 

  14. Walter RE, Belser A, Givelber RJ, O’Conner GT, Gottlieb DJ (2003) Association between glycemic state and lung function: the Framingham Heart Study. Am J Respir Crit Care Med 167:911–916

    Article  PubMed  Google Scholar 

  15. Sandler M, Bumm AE, Stemont RI (1987) Cross-section study of pulmonary function in patients with insulin-dependent diabetes mellitus. Am Rev Respir Dis 135:223–229

    PubMed  CAS  Google Scholar 

  16. Barrett-Connor E, Frette C (1996) NIDDM, impaired glucose tolerance, and pulmonary function in older adults. The Rancho Bernardo study. Diabetes Care 19:1441–1444

    Article  PubMed  CAS  Google Scholar 

  17. Taylor HA, Wilson JG, Jones DW, Sarpong DF, Srinivasan A, Garrison RJ, Nelson C, Wyatt SB (2005) Toward resolution of cardiovascular health disparities in African Americans: design and methods of the Jackson Heart Study. Ethn Dis 5(4 Suppl 6):S6-4–S6-17

    Google Scholar 

  18. Fuqua SR, Wyatt SB, Andrew ME, Sarpong DF, Henderson FR, Cunningham MF, Taylor HA Jr (2005) Recruiting African–American research participation in the Jackson Heart Study: methods, response rates, and sample description. Ethn Dis 15(4 Suppl 6):S6-18–S6-29

    Google Scholar 

  19. Wilson JG, Rotimi CN, Ekunwe L, Royal CD, Crump ME, Wyatt SB, Steffes MW, Adeyemo A, Zhou J, Taylor HA Jr, Jaquish C (2005) Study design for genetic analysis in the Jackson Heart Study. Ethn Dis 15(4 Suppl 6):S6-30–S6-37

    Google Scholar 

  20. Pauwels RA, Buist AS, Calverley PM, Jenkins CR, Hurd SS, GOLD Scientific Committee (2001) Global strategies for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: NHLBI / WHO global initiative for chronic obstructive lung disease (GOLD) workshop summary. Am J Respir Crit Care Med 163:1256–1276

    PubMed  CAS  Google Scholar 

  21. American Thoracic Society (1995) Standardization of spirometry: 1994 update. Am J Respir Crit Care Med 152:1107–1136

    Google Scholar 

  22. Carpenter MA, Crow R, Steffes M, Rock W, Heilbraun J, Evans G, Skelton T, Jensen R, Sarpong D (2004) Laboratory, reading center, and coordinating center data management methods in the Jackson Heart Study. Am J Med Sci 328:131–144

    Article  PubMed  Google Scholar 

  23. American Diabetes Association (2004) Diagnosis and classification of diabetes mellitus. Diabetes Care 27(suppl 1):s5–s10

    Google Scholar 

  24. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419

    Article  PubMed  CAS  Google Scholar 

  25. Prescott E, Lange P, Vestbo J (1999) Socioeconomic status, lung function and admission to hospital for COPD: results from the Copenhagen city heart study. Eur Respir J 13:1109–1114

    Article  PubMed  CAS  Google Scholar 

  26. Nystad W, Samuelsen SO, Nafstad P, Langhammer A (2006) Association between level of physical activity and lung function among Norwegian men and women: the HUNT study. Int J Tuberc Lung Dis 10:1399–1405

    PubMed  CAS  Google Scholar 

  27. Ochs-Balcom HM, Grant BJ, Muti P, Sempos CT, Freudenheim JL, Trevisan M, Cassano PA, Iacoviello L, Schunemann HJ (2006) Pulmonary function and abdominal adiposity in the general population. Chest 129:853–862

    Article  PubMed  Google Scholar 

  28. Smitherman TA, Dubbert PM, Grothe KB, Sung JH, Kendzor DE, Reis JP, Ainsworth BE, Newton RL Jr, Lesniak KT, Taylor HA Jr (2009) Validation of the Jackson Heart Study physical activity survey in African Americans. J Phys Act Health 6(Suppl 1):S124–S132

    PubMed  Google Scholar 

  29. Hickson DA, Wilhite RL, Petrini MF, White WB, Burchfiel C (2009) Asthma and asthma severity among African Americans in the Jackson Heart Study. J Asthma 46:421–428

    Article  PubMed  CAS  Google Scholar 

  30. Liu J, Fox CS, Hickson DA, May WD, Hairston KG, Carr JJ, Taylor HA (2010) Impact of Abdominal visceral and subcutaneous adipose tissue on cardiometabolic risk factors: the Jackson Heart Study. J Clin Endocrinol Metab 95(12):5419–5426

    Article  PubMed  CAS  Google Scholar 

  31. Krakoff J, Lindsay RS, Looker HC, Nelson RG, Hanson RL, Knowler WC (2003) Incidence of retinopathy and nephropathy in youth-onset compared with adult-onset type 2 diabetes. Diabetes Care 26:76–81

    Article  PubMed  Google Scholar 

  32. Vracko R, Thorning D, Huang TW (1979) Basal lamina of alveolar epithelium and capillaries: quantitative changes with aging and in diabetes mellitus. Am Rev Respir Dis 120:973–983

    PubMed  CAS  Google Scholar 

  33. Popov D, Simionescu M (2001) Structural and transport property alterations of the lung capillary endothelium in diabetes. Ital J Anat Embryol 106:405–412

    PubMed  CAS  Google Scholar 

  34. Bell D, Collier A, Matthews DM, Cooksey EJ, McHardy GJ, Clarke BF (1988) Are reduced lung volumes in IDDM due to defect in connective tissue? Diabetes 37:829–831

    Article  PubMed  CAS  Google Scholar 

  35. Sandler M (1990) Is the lung a target organ in diabetes mellitus? Arch Intern Med 150:1385–1388

    Article  PubMed  CAS  Google Scholar 

  36. Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY, Vasan RS, Murabito JM, Meigs JB, Cupples LA, D’Agostino RB Sr, O’Donnell CJ (2007) Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation 116:39–48

    Article  PubMed  Google Scholar 

  37. Blüher M (2009) Adipose tissue dysfunction in obesity. Exp Clin Endocrinol Diabetes 117:241–250

    Article  PubMed  Google Scholar 

  38. 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

    Article  PubMed  Google Scholar 

  39. Eisner MD (2002) Environmental tobacco smoke exposure and pulmonary function among adults in NHANES III: impact on the general population and adults with current asthma. Environ Health Perspect 110:765–770

    Article  PubMed  Google Scholar 

  40. Kan H, Heiss G, Rose KM, Whitsel E, Lurmann F, London SJ (2007) Traffic exposure and lung function in adults: the atherosclerosis risk in communities study. Thorax 62:873–879

    Article  PubMed  Google Scholar 

  41. Robinson JC, Wyatt SB, Hickson D, Gwinn D, Faruque F, Sims M, Sarpong D, Taylor HA (2010) Methods for retrospectively geocoding urban and rural epidemiology studies: the Jackson Heart Study. J Urban Health 87:136–150

    Article  PubMed  Google Scholar 

  42. Levitzky YS, Pencina MJ, D’Agostino RB, Meigs JB, Murabito JM, Vasan RS, Fox CS (2008) Impact of impaired fasting glucose on cardiovascular disease: the Framingham Heart Study. J Am Coll Cardiol 51:264–270

    Article  PubMed  CAS  Google Scholar 

  43. Ehrlich SF, Quesenberry CP Jr, Van Den Eeden SK, Shan J, Ferrara A (2010) Patients diagnosed with diabetes are at increased risk for asthma, chronic obstructive pulmonary disease, pulmonary fibrosis, and pneumonia but not lung cancer. Diabetes Care 33:55–60

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors sincerely thank the Jackson Heart Study participants, staff, and interns for their long-term commitment to the study. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the National Institutes of Health (NIH) or the National Institute for Occupational Safety and Health. This work was supported by the NIH: National Heart, Lung, and Blood Institute and the National Center on Minority Health and Health Disparities [Contracts N01-HC-95170, N01-HC-95171, and N01-HC-95172].

Conflict of interest

The authors have no conflicts of interest to disclose.

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Authors and Affiliations

  1. Jackson Heart Study, Jackson State University, 350 West Woodrow Wilson Avenue, Suite 701, Jackson, MS, 39213, USA

    DeMarc A. Hickson

  2. Department of Medicine, University of Mississippi Medical Center, Jackson, MS, 39216, USA

    DeMarc A. Hickson, Jiankang Liu & Marcy F. Petrini

  3. Health Effects Laboratory Division, National Institute for Occupational Safety and Health, Morgantown, WV, 26505, USA

    Cecil M. Burchfiel

  4. Jackson Heart Study, Tougaloo College, Tougaloo, MS, 39174, USA

    Kimystian Harrison & Wendy B. White

  5. Department of Epidemiology and Biostatistics, Jackson State University, Jackson, MS, 39213, USA

    Daniel F. Sarpong

Authors
  1. DeMarc A. Hickson
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  2. Cecil M. Burchfiel
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  3. Jiankang Liu
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  4. Marcy F. Petrini
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  7. Daniel F. Sarpong
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Correspondence to DeMarc A. Hickson.

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Hickson, D.A., Burchfiel, C.M., Liu, J. et al. Diabetes, Impaired Glucose Tolerance, and Metabolic Biomarkers in Individuals with Normal Glucose Tolerance are Inversely Associated with Lung Function: The Jackson Heart Study. Lung 189, 311–321 (2011). https://doi.org/10.1007/s00408-011-9296-1

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