Acta Diabetologica

, Volume 51, Issue 6, pp 933–940 | Cite as

Diabetes mellitus among outpatients with COPD attending a university hospital

  • Paola Rogliani
  • Luigino Calzetta
  • Andrea Segreti
  • Annapina Barrile
  • Mario Cazzola
Original Article


Type 2 diabetes mellitus is a common comorbidity of COPD, but there are still many doubts about the relation among diabetes and COPD. We retrospectively collected data from patients afferent to our Respiratory Diseases outpatient clinic at the Tor Vergata University Hospital between 2010 and 2012. The study population was analyzed by clusters of age, gender, body mass index (BMI), smoking status, lung function, concomitant pharmacologic therapies and comorbidities. The values of the association between variables were expressed as odds ratio. Data were adjusted for gender, age and possible confounding variables by Mantel–Haenszel method. We identified 493 patients with COPD. Ninety-two (18.7 %) patients were affected by type 2 diabetes mellitus, with no significant gender differences. The prevalence distribution was similar among the different age clusters, but the association was stronger in patients younger than 65 years. The association was present only in obese subjects in whom it was significant only in patients with moderate-to-severe COPD, but not mild COPD. The presence of cardiovascular diseases was significantly associated with diabetes mellitus in patients with COPD. There was a slight association of inhaled corticosteroid (ICS) use with the presence of diabetes mellitus in COPD, but the combination of an ICS with a β2-agonist apparently reduced this association. The association with type 2 diabetes mellitus was greater in patients with COPD respect to general population, and correlated with the increase in BMI and the presence of other comorbidities, suggesting that both diseases may be targets of systemic inflammation.


Diabetes mellitus COPD Comorbidities Systemic inflammation 


  1. 1.
    Mannino DM, Thorn D, Swensen A, Holguin F (2008) Prevalence and outcomes of diabetes, hypertension and cardiovascular disease in COPD. Eur Respir J 32(4):962–969PubMedCrossRefGoogle Scholar
  2. 2.
    Barr RG, Celli BR, Mannino DM, Petty T, Rennard SI, Sciurba FC, Stoller JK, Thomashow BM, Turino GM (2009) Comorbidities, patient knowledge, and disease management in a national sample of patients with COPD. Am J Med 122(4):348–355. doi:10.1016/j.amjmed.2008.09.042 PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Feary JR, Rodrigues LC, Smith CJ, Hubbard RB, Gibson JE (2010) Prevalence of major comorbidities in subjects with COPD and incidence of myocardial infarction and stroke: a comprehensive analysis using data from primary care. Thorax 65(11):956–962PubMedCrossRefGoogle Scholar
  4. 4.
    Cazzola M, Bettoncelli G, Sessa E, Cricelli C, Biscione G (2010) Prevalence of comorbidities in patients with chronic obstructive pulmonary disease. Respiration 80(2):112–119. doi:10.1159/000281880 PubMedCrossRefGoogle Scholar
  5. 5.
    Lee CT, Mao IC, Lin CH, Lin SH, Hsieh MC (2013) Chronic obstructive pulmonary disease: a risk factor for type 2 diabetes: a nationwide population-based study. Eur J Clin Invest 43(11):1113–1119. doi:10.1111/eci.12147 PubMedGoogle Scholar
  6. 6.
    Joo H, Park J, Lee SD, Oh YM (2012) Comorbidities of chronic obstructive pulmonary disease in Koreans: a population-based study. J Korean Med Sci 27(8):901–906. doi:10.3346/jkms.2012.27.8.901 PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Cavailles A, Brinchault-Rabin G, Dixmier A, Goupil F, Gut-Gobert C, Marchand-Adam S, Meurice JC, Morel H, Person-Tacnet C, Leroyer C, Diot P (2013) Comorbidities of COPD. Eur Respir Rev 22(130):454–475. doi:10.1183/09059180.00008612 PubMedCrossRefGoogle Scholar
  8. 8.
    ISTAT Annuario statistico italiano 2009. Capitolo 3: Sanità e Salute.
  9. 9.
    Schmidt CO, Kohlmann T (2008) When to use the odds ratio or the relative risk? Int J Public Health 53(3):165–167PubMedCrossRefGoogle Scholar
  10. 10.
    Zhang J, Yu KF (1998) What’s the relative risk? a method of correcting the odds ratio in cohort studies of common outcomes. J Am Med Assoc 280(19):1690–1691CrossRefGoogle Scholar
  11. 11.
    Wells CE, Baker EH (2013) Metabolic syndrome and European Respiratory Monograph 59: COPD and Comorbidity 117–134Google Scholar
  12. 12.
    Franssen FM, O’Donnell DE, Goossens GH, Blaak EE, Schols AM (2008) Obesity and the lung: 5.Obesity and COPD. Thorax 63(12):1110–1117. doi:10.1136/thx.2007.086827 PubMedCrossRefGoogle Scholar
  13. 13.
    Cazzola M, Calzetta L, Lauro D, Bettoncelli G, Cricelli C, Di Daniele N, Rogliani P (2013) Asthma and COPD in an Italian adult population: role of BMI considering the smoking habit. Respir Med 107(9):1417–1422. doi:10.1016/j.rmed.2013.04.021 PubMedCrossRefGoogle Scholar
  14. 14.
    Mancuso P (2010) Obesity and lung inflammation. J Appl Physiol 108(3):722–728. doi:10.1152/japplphysiol.00781.2009 PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    van den Borst B, Gosker HR, Wesseling G, de Jager W, Hellwig VA, Snepvangers FJ, Schols AM (2011) Low-grade adipose tissue inflammation in patients with mild-to-moderate chronic obstructive pulmonary disease. Am J Clin Nutr 94(6):1504–1512. doi:10.3945/ajcn.111.023911 PubMedCrossRefGoogle Scholar
  16. 16.
    Rana JS, Mittleman MA, Sheikh J, Hu FB, Manson JE, Colditz GA, Speizer FE, Barr RG, Camargo CA Jr (2004) Chronic obstructive pulmonary disease, asthma, and risk of type 2 diabetes in women. Diabetes Care 27(10):2478–2484PubMedCrossRefGoogle Scholar
  17. 17.
    Walter RE, Beiser A, Givelber RJ, O’Connor GT, Gottlieb DJ (2003) Association between glycemic state and lung function: the Framingham Heart Study. Am J Respir Crit Care Med 167(6):911–916. doi:10.1164/rccm.2203022167/6/911 PubMedCrossRefGoogle Scholar
  18. 18.
    Rimm EB, Manson JE, Stampfer MJ, Colditz GA, Willett WC, Rosner B, Hennekens CH, Speizer FE (1993) Cigarette smoking and the risk of diabetes in women. Am J Public Health 83(2):211–214PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Rosen P, Nawroth PP, King G, Moller W, Tritschler HJ, Packer L (2001) The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCO-MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab Res Rev 17(3):189–212PubMedCrossRefGoogle Scholar
  20. 20.
    Laghi F, Adiguzel N, Tobin MJ (2009) Endocrinological derangements in COPD. Eur Respir J 34(4):975–996. doi:10.1183/09031936.00103708 PubMedCrossRefGoogle Scholar
  21. 21.
    Bolton CE, Evans M, Ionescu AA, Edwards SM, Morris RH, Dunseath G, Luzio SD, Owens DR, Shale DJ (2007) Insulin resistance and inflammation: a further systemic complication of COPD. COPD 4(2):121–126. doi:10.1080/15412550701341053 PubMedCrossRefGoogle Scholar
  22. 22.
    Buist AS, McBurnie MA, Vollmer WM, Gillespie S, Burney P, Mannino DM, Menezes AM, Sullivan SD, Lee TA, Weiss KB, Jensen RL, Marks GB, Gulsvik A, Nizankowska-Mogilnicka E, Group BCR (2007) International variation in the prevalence of COPD (the BOLD Study): a population-based prevalence study. Lancet 370(9589):741–750. doi:10.1016/S0140-6736(07)61377-4 PubMedCrossRefGoogle Scholar
  23. 23.
    Manson JE, Ajani UA, Liu S, Nathan DM, Hennekens CH (2000) A prospective study of cigarette smoking and the incidence of diabetes mellitus among US male physicians. Am J Med 109(7):538–542PubMedCrossRefGoogle Scholar
  24. 24.
    Chung KF, Adcock IM (2008) Multifaceted mechanisms in COPD: inflammation, immunity, and tissue repair and destruction. Eur Respir J 31(6):1334–1356. doi:10.1183/09031936.00018908 PubMedCrossRefGoogle Scholar
  25. 25.
    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(6):546–556. doi:10.1093/aje/kwi076 PubMedCrossRefGoogle Scholar
  26. 26.
    Sandler M (1990) Is the lung a ‘target organ’ in diabetes mellitus? Arch Intern Med 150(7):1385–1388PubMedCrossRefGoogle Scholar
  27. 27.
    Weynand B, Jonckheere A, Frans A, Rahier J (1999) Diabetes mellitus induces a thickening of the pulmonary basal lamina. Respiration 66(1):14–19PubMedCrossRefGoogle Scholar
  28. 28.
    Fine MJ, Smith MA, Carson CA, Mutha SS, Sankey SS, Weissfeld LA, Kapoor WN (1996) Prognosis and outcomes of patients with community-acquired pneumonia: a meta-analysis. J Am Med Assoc 275(2):134–141CrossRefGoogle Scholar
  29. 29.
    Pogson ZE, McKeever TM, Fogarty A (2008) The association between serum osmolality and lung function among adults. Eur Respir J 32(1):98–104. doi:10.1183/09031936.00144207 PubMedCrossRefGoogle Scholar
  30. 30.
    Cazzola M, Calzetta L, Rogliani P, Lauro D, Novelli L, Page CP, Kanabar V, Matera MG (2012) High glucose enhances responsiveness of human airways smooth muscle via the Rho/ROCK pathway. Am J Respir Cell Mol Biol 47(4):509–516. doi:10.1165/rcmb.2011-0449OC PubMedCrossRefGoogle Scholar
  31. 31.
    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(3):641–645PubMedCrossRefGoogle Scholar
  32. 32.
    Engstrom G, Janzon L (2002) Risk of developing diabetes is inversely related to lung function: a population-based cohort study. Diabet Med 19(2):167–170PubMedCrossRefGoogle Scholar
  33. 33.
    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(6):1472–1479PubMedCrossRefGoogle Scholar
  34. 34.
    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(4):741–746. doi:10.2337/dc07-1464 PubMedCentralPubMedCrossRefGoogle Scholar
  35. 35.
    Fabbri LM, Rabe KF (2007) From COPD to chronic systemic inflammatory syndrome? Lancet 370(9589):797–799PubMedCrossRefGoogle Scholar
  36. 36.
    Barnes PJ (2010) Chronic obstructive pulmonary disease: effects beyond the lungs. PLoS Med 7(3):e1000220. doi:10.1371/journal.pmed.1000220 PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Bousquet J, Anto JM, Sterk PJ, Adcock IM, Chung KF, Roca J, Agusti A, Brightling C, Cambon-Thomsen A, Cesario A, Abdelhak S, Antonarakis SE, Avignon A, Ballabio A, Baraldi E, Baranov A, Bieber T, Bockaert J, Brahmachari S, Brambilla C, Bringer J, Dauzat M, Ernberg I, Fabbri L, Froguel P, Galas D, Gojobori T, Hunter P, Jorgensen C, Kauffmann F, Kourilsky P, Kowalski ML, Lancet D, Pen CL, Mallet J, Mayosi B, Mercier J, Metspalu A, Nadeau JH, Ninot G, Noble D, Ozturk M, Palkonen S, Prefaut C, Rabe K, Renard E, Roberts RG, Samolinski B, Schunemann HJ, Simon HU, Soares MB, Superti-Furga G, Tegner J, Verjovski-Almeida S, Wellstead P, Wolkenhauer O, Wouters E, Balling R, Brookes AJ, Charron D, Pison C, Chen Z, Hood L, Auffray C (2011) Systems medicine and integrated care to combat chronic noncommunicable diseases. Genome Med 3(7):43PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Slatore CG, Bryson CL, Au DH (2009) The association of inhaled corticosteroid use with serum glucose concentration in a large cohort. Am J Med 122(5):472–478. doi:10.1016/j.amjmed.2008.09.048 PubMedCrossRefGoogle Scholar
  39. 39.
    Faul JL, Wilson SR, Chu JW, Canfield J, Kuschner WG (2009) The effect of an inhaled corticosteroid on glucose control in type 2 diabetes. Clin Med Res 7(1–2):14–20. doi:10.3121/cmr.2009.824 PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    O’Byrne PM, Rennard S, Gerstein H, Radner F, Peterson S, Lindberg B, Carlsson LG, Sin DD (2012) Risk of new onset diabetes mellitus in patients with asthma or COPD taking inhaled corticosteroids. Respir Med 106(11):1487–1493. doi:10.1016/j.rmed.2012.07.011 PubMedCrossRefGoogle Scholar
  41. 41.
    Kesten S, Jara M, Wentworth C, Lanes S (2006) Pooled clinical trial analysis of tiotropium safety. Chest 130(6):1695–1703. doi:10.1378/chest.130.6.1695 PubMedCrossRefGoogle Scholar
  42. 42.
    Philipson LH (2002) beta-Agonists and metabolism. J Allergy Clin Immunol 110(6 Suppl):S313–S317PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Italia 2014

Authors and Affiliations

  • Paola Rogliani
    • 1
  • Luigino Calzetta
    • 2
  • Andrea Segreti
    • 1
  • Annapina Barrile
    • 1
  • Mario Cazzola
    • 1
  1. 1.Department of System MedicineUniversity of Rome Tor VergataRomeItaly
  2. 2.Department of Pulmonary RehabilitationIRCCS, San Raffaele Pisana HospitalRomeItaly

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