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Erschienen in: Endocrine 1/2018

06.03.2018 | Mini Review

Physiopathological relationship between chronic obstructive pulmonary disease and insulin resistance

verfasst von: Felipe Vilaça Cavallari Machado, Fabio Pitta, Nidia Aparecida Hernandes, Gisele Lopes Bertolini

Erschienen in: Endocrine | Ausgabe 1/2018

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Abstract

Purpose

Chronic obstructive pulmonary disease (COPD) is characterized by persistent and progressive airflow obstruction that is associated with an abnormal chronic inflammatory response in the airways and lungs to noxious particles. COPD often leads to physical inactivity and deconditioning that added to inappropriate/excessive inflammatory responses leads to systemic consequences. Studies have shown that metabolic syndrome and manifested diabetes are more frequent in COPD than in healthy subjects; a possible explanation is that different pathophysiological aspects of COPD can lead to insulin resistance. Thus, this mini-review aims to present the main studies suggesting a pathophysiological relationship between COPD and insulin resistance.

Methods

A review of literature was conducted using PubMed and Web of Science databases with the aim of searching for studies supporting a relationship between COPD and insulin resistance.

Results

A physiopathological relationship between COPD and insulin resistance was found, supported in part due to common risk factors presented by these two conditions, such as smoking and physical inactivity. Also, systemic effects (worsening of physical inactivity and sedentary behavior, inflammation and oxidative stress, body composition abnormalities) and the corticosteroid treatment of patients with COPD may play a role.

Conclusion

Patients with COPD should be screened for abnormalities in insulin sensitivity in order to reduce morbidity and improve health status in this population.
Literatur
1.
Zurück zum Zitat Global Strategy for the Diagnosis, Management and Prevention of COPD, Global Initiative for Chronic Obstructive Lung Disease (GOLD) (2017). http://goldcopd.org. Accessed 21 Aug 2017 Global Strategy for the Diagnosis, Management and Prevention of COPD, Global Initiative for Chronic Obstructive Lung Disease (GOLD) (2017). http://​goldcopd.​org. Accessed 21 Aug 2017
2.
Zurück zum Zitat P.J. Miranda, R.A. DeFronzo, R.M. Califf, J.R. Guyton, Metabolic syndrome: definition, pathophysiology, and mechanisms. Am. Heart J. 149, 33–45 (2005)CrossRefPubMed P.J. Miranda, R.A. DeFronzo, R.M. Califf, J.R. Guyton, Metabolic syndrome: definition, pathophysiology, and mechanisms. Am. Heart J. 149, 33–45 (2005)CrossRefPubMed
3.
Zurück zum Zitat C.E. Bolton, M. Evans, A.A. Ionescu, S.M. Edwards, R.H.K. Morris, G. Dunseath et al., Insulin resistance and inflammation - a further systemic complication of COPD. COPD 4, 121–126 (2007)CrossRefPubMed C.E. Bolton, M. Evans, A.A. Ionescu, S.M. Edwards, R.H.K. Morris, G. Dunseath et al., Insulin resistance and inflammation - a further systemic complication of COPD. COPD 4, 121–126 (2007)CrossRefPubMed
4.
Zurück zum Zitat M. Minas, K. Kostikas, A.I. Papaioannou, P. Mystridou, E. Karetsi, P. Georgoulias et al., The association of metabolic syndrome with adipose tissue hormones and insulin resistance in patients with COPD without co-morbidities. COPD 8, 414–420 (2011)CrossRefPubMed M. Minas, K. Kostikas, A.I. Papaioannou, P. Mystridou, E. Karetsi, P. Georgoulias et al., The association of metabolic syndrome with adipose tissue hormones and insulin resistance in patients with COPD without co-morbidities. COPD 8, 414–420 (2011)CrossRefPubMed
5.
Zurück zum Zitat S. Gläser, S. Krüger, M. Merkel, P. Bramlage, F.J.F. Herth, Chronic obstructive pulmonary disease and diabetes mellitus: a systematic review of the literature. Respiration 89, 253–264 (2015)CrossRefPubMed S. Gläser, S. Krüger, M. Merkel, P. Bramlage, F.J.F. Herth, Chronic obstructive pulmonary disease and diabetes mellitus: a systematic review of the literature. Respiration 89, 253–264 (2015)CrossRefPubMed
6.
Zurück zum Zitat P.J. Barnes, Inflammatory mechanisms in patients with chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 138, 16–27 (2016)CrossRefPubMed P.J. Barnes, Inflammatory mechanisms in patients with chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 138, 16–27 (2016)CrossRefPubMed
8.
Zurück zum Zitat L. Lavie, P. Lavie, Molecular mechanisms of cardiovascular disease in OSAHS: the oxidative stress link. Eur. Respir. J. 33, 1467–1484 (2009)CrossRefPubMed L. Lavie, P. Lavie, Molecular mechanisms of cardiovascular disease in OSAHS: the oxidative stress link. Eur. Respir. J. 33, 1467–1484 (2009)CrossRefPubMed
9.
Zurück zum Zitat K.N. Keane, V.F. Cruzat, R. Carlessi, P.I.H. Bittencourt, P. Newsholme, Molecular events linking oxidative stress and inflammation to insulin resistance and ß-cell disfunction. Oxid. Med. Cell. Longev. 2015, 181643 (2015)CrossRefPubMedPubMedCentral K.N. Keane, V.F. Cruzat, R. Carlessi, P.I.H. Bittencourt, P. Newsholme, Molecular events linking oxidative stress and inflammation to insulin resistance and ß-cell disfunction. Oxid. Med. Cell. Longev. 2015, 181643 (2015)CrossRefPubMedPubMedCentral
10.
11.
Zurück zum Zitat J. Spranger, A. Kroke, M. Möhlig, K. Hoffmann, M.M. Bergmann, M. Ristow et al., Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into cancer and nutrition (EPIC)-Postdam study. Diabetes 52, 812–817 (2003)CrossRefPubMed J. Spranger, A. Kroke, M. Möhlig, K. Hoffmann, M.M. Bergmann, M. Ristow et al., Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into cancer and nutrition (EPIC)-Postdam study. Diabetes 52, 812–817 (2003)CrossRefPubMed
12.
Zurück zum Zitat H. Watz, B. Waschki, A. Kirsten, K.C. Müller, G. Kretschmar, T. Meyer et al., The metabolic syndrome in patients with chronic bronchitis and COPD: frequency and associated consequences for systemic inflammation and physical activity. Chest 136, 1039–1046 (2009)CrossRefPubMed H. Watz, B. Waschki, A. Kirsten, K.C. Müller, G. Kretschmar, T. Meyer et al., The metabolic syndrome in patients with chronic bronchitis and COPD: frequency and associated consequences for systemic inflammation and physical activity. Chest 136, 1039–1046 (2009)CrossRefPubMed
13.
Zurück zum Zitat H. Watz, B. Waschki, T. Meyer, H. Magnussen, Systemic manifestations and comorbidities of COPD. Eur. Respir. J. 33, 1165–1185 (2009)CrossRef H. Watz, B. Waschki, T. Meyer, H. Magnussen, Systemic manifestations and comorbidities of COPD. Eur. Respir. J. 33, 1165–1185 (2009)CrossRef
14.
Zurück zum Zitat F. Pitta, T. Troosters, M.A. Spruit, V.S. Probst, M. Decramer, R. Gosselink, Characteristics of physical activities in daily life in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 171, 972–977 (2005)CrossRefPubMed F. Pitta, T. Troosters, M.A. Spruit, V.S. Probst, M. Decramer, R. Gosselink, Characteristics of physical activities in daily life in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 171, 972–977 (2005)CrossRefPubMed
15.
Zurück zum Zitat N.A. Hernandes, D.C. Teixeira, V.S. Probst, A.F. Brunetto, E.M. Ramos, F. Pitta, Profile of the level of physical activity in the daily lives of patients with COPD in Brazil. J. Bras. Pneumol. 35, 949–956 (2009)CrossRefPubMed N.A. Hernandes, D.C. Teixeira, V.S. Probst, A.F. Brunetto, E.M. Ramos, F. Pitta, Profile of the level of physical activity in the daily lives of patients with COPD in Brazil. J. Bras. Pneumol. 35, 949–956 (2009)CrossRefPubMed
16.
Zurück zum Zitat S.N.W. Vorrink, H.S.M. Kort, T. Troosters, J.W.J. Lammers, Level of daily physical activity in individuals with COPD compared with healthy controls. Respir. Res. 12, 33 (2011)CrossRefPubMedPubMedCentral S.N.W. Vorrink, H.S.M. Kort, T. Troosters, J.W.J. Lammers, Level of daily physical activity in individuals with COPD compared with healthy controls. Respir. Res. 12, 33 (2011)CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat N.M. Hamburg, C.J. Mcmackin, A.L. Huang, S.M. Shenouda, E. Michael, E. Schulz et al., Physical inactivity rapidly induces insulin resistance and microvascular dysfunction in healthy volunteers. Arter. Thromb. Vasc. Biol. 27, 2650–2656 (2008)CrossRef N.M. Hamburg, C.J. Mcmackin, A.L. Huang, S.M. Shenouda, E. Michael, E. Schulz et al., Physical inactivity rapidly induces insulin resistance and microvascular dysfunction in healthy volunteers. Arter. Thromb. Vasc. Biol. 27, 2650–2656 (2008)CrossRef
18.
Zurück zum Zitat C.A. Stuart, R.E. Shangraw, M.J. Prince, E.J. Peters, R.R. Wolfe, Bed-rest induced insulin resistance occurs primarily in muscle. Metabolism 37, 802–806 (1988)CrossRefPubMed C.A. Stuart, R.E. Shangraw, M.J. Prince, E.J. Peters, R.R. Wolfe, Bed-rest induced insulin resistance occurs primarily in muscle. Metabolism 37, 802–806 (1988)CrossRefPubMed
19.
Zurück zum Zitat P.J. Arciero, D.L. Smith, J. Calles-escandon, Effects of short-term inactivity on glucose tolerance, energy expenditure, and blood flow in trained subjects. J. Appl. Physiol. 84, 1365–1373 (1998)CrossRefPubMed P.J. Arciero, D.L. Smith, J. Calles-escandon, Effects of short-term inactivity on glucose tolerance, energy expenditure, and blood flow in trained subjects. J. Appl. Physiol. 84, 1365–1373 (1998)CrossRefPubMed
20.
Zurück zum Zitat J. Smorawiński, H. Kaciuba-Uściłko, K. Nazar, P. Kubala, E. Kamińska, A.W. Ziemba et al., Effects of three-day bed rest on metabolic, hormonal and circulatory responses to an oral glucose load in endurance or strength trained athletes and untrained subjects. J. Physiol. Pharmacol. 51, 279–289 (2000)PubMed J. Smorawiński, H. Kaciuba-Uściłko, K. Nazar, P. Kubala, E. Kamińska, A.W. Ziemba et al., Effects of three-day bed rest on metabolic, hormonal and circulatory responses to an oral glucose load in endurance or strength trained athletes and untrained subjects. J. Physiol. Pharmacol. 51, 279–289 (2000)PubMed
21.
Zurück zum Zitat A.A.M. Castro, C. Kümpel, R.C. Rangueri, M.D. Oliveira, R.A. Dornelles, E.R. Brito et al., Daily activities are sufficient to induce dynamic pulmonary hyperinflation and dyspnea in chronic obstructive pulmonary disease patients. Clinics 67, 319–325 (2012)CrossRefPubMedPubMedCentral A.A.M. Castro, C. Kümpel, R.C. Rangueri, M.D. Oliveira, R.A. Dornelles, E.R. Brito et al., Daily activities are sufficient to induce dynamic pulmonary hyperinflation and dyspnea in chronic obstructive pulmonary disease patients. Clinics 67, 319–325 (2012)CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat M. Velloso, N.H. do Nascimento, M.R. Gazzotti, J.R. Jardim, Evaluation of effects of shoulder girdle training on strength and performance of activities of daily living in patients with chronic obstructive pulmonary disease. Int. J. Chron. Obstruct. Pulmon. Dis. 8, 187–192 (2013)PubMedPubMedCentral M. Velloso, N.H. do Nascimento, M.R. Gazzotti, J.R. Jardim, Evaluation of effects of shoulder girdle training on strength and performance of activities of daily living in patients with chronic obstructive pulmonary disease. Int. J. Chron. Obstruct. Pulmon. Dis. 8, 187–192 (2013)PubMedPubMedCentral
23.
Zurück zum Zitat N.C. Lipovec, R.J.H.C.G. Beijers, B. van den Borst, W. Doehner, M. Lainscak, A.M.W.J. Schols, The prevalence of metabolic syndrome in chronic obstructive pulmonary disease: a systematic review. COPD 13, 399–406 (2016)CrossRef N.C. Lipovec, R.J.H.C.G. Beijers, B. van den Borst, W. Doehner, M. Lainscak, A.M.W.J. Schols, The prevalence of metabolic syndrome in chronic obstructive pulmonary disease: a systematic review. COPD 13, 399–406 (2016)CrossRef
24.
Zurück zum Zitat S.K. Park, J.L. Larson, The relationship between physical activity and metabolic syndrome in people with chronic obstructive pulmonary disease. J. Cardiovasc. Nurs. 29, 499–507 (2014)CrossRefPubMedPubMedCentral S.K. Park, J.L. Larson, The relationship between physical activity and metabolic syndrome in people with chronic obstructive pulmonary disease. J. Cardiovasc. Nurs. 29, 499–507 (2014)CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat M.A. Spruit, S.J. Singh, C. Garvey, R. Zu Wallack, L. Nici, C. Rochester et al., An official american thoracic society/european respiratory society statement: key concepts and advances in pulmonary rehabilitation. Am. J. Respir. Crit. Care Med. 188, e13–e64 (2013)CrossRefPubMed M.A. Spruit, S.J. Singh, C. Garvey, R. Zu Wallack, L. Nici, C. Rochester et al., An official american thoracic society/european respiratory society statement: key concepts and advances in pulmonary rehabilitation. Am. J. Respir. Crit. Care Med. 188, e13–e64 (2013)CrossRefPubMed
26.
Zurück zum Zitat P. Joppa, R. Tkacova, F.M.E. Franssen, C. Hanson, S.I. Rennard, E.K. Silverman et al., Sarcopenic obesity, functional outcomes, and systemic inflammation in patients with chronic obstructive pulmonary disease. J. Am. Med. Dir. Assoc. 17, 712–718 (2016)CrossRefPubMed P. Joppa, R. Tkacova, F.M.E. Franssen, C. Hanson, S.I. Rennard, E.K. Silverman et al., Sarcopenic obesity, functional outcomes, and systemic inflammation in patients with chronic obstructive pulmonary disease. J. Am. Med. Dir. Assoc. 17, 712–718 (2016)CrossRefPubMed
27.
Zurück zum Zitat G.H. Goossens, The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol. Behav. 94, 206–218 (2008)CrossRefPubMed G.H. Goossens, The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol. Behav. 94, 206–218 (2008)CrossRefPubMed
28.
Zurück zum Zitat A.R. Saltiel, C.R. Kahn, Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414, 799–806 (2001)CrossRefPubMed A.R. Saltiel, C.R. Kahn, Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414, 799–806 (2001)CrossRefPubMed
29.
Zurück zum Zitat R.J.H.C.G. Beijers, C. van de Bool, B. van den Borst, F.M.E. Franssen, E.F.M. Wouters, A.M.W.J. Schols, Normal weight but low muscle massa and abdominally obese: implications for the cardiometabolic risk profile in chronic obstructive pulmonary disease. J. Am. Med. Dir. Assoc. 18, 533–538 (2017)CrossRefPubMed R.J.H.C.G. Beijers, C. van de Bool, B. van den Borst, F.M.E. Franssen, E.F.M. Wouters, A.M.W.J. Schols, Normal weight but low muscle massa and abdominally obese: implications for the cardiometabolic risk profile in chronic obstructive pulmonary disease. J. Am. Med. Dir. Assoc. 18, 533–538 (2017)CrossRefPubMed
30.
Zurück zum Zitat C.E. Wells, M.I. Polkey, E.H. Baker, Insulin resistance is associated with skeletal muscle weakness in COPD. Respirology 21, 689–696 (2016)CrossRefPubMed C.E. Wells, M.I. Polkey, E.H. Baker, Insulin resistance is associated with skeletal muscle weakness in COPD. Respirology 21, 689–696 (2016)CrossRefPubMed
31.
Zurück zum Zitat V.V.A. Lira, C.R.C. Benton, Z. Yan, A. Bonen, PGC-1α regulation by exercise training and its influences on muscle function and insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 299, E145–E161 (2010)CrossRefPubMedPubMedCentral V.V.A. Lira, C.R.C. Benton, Z. Yan, A. Bonen, PGC-1α regulation by exercise training and its influences on muscle function and insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 299, E145–E161 (2010)CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat F. Maltais, M. Decramer, R. Casaburi, E. Barreiro, Y. Burelle, R. Debigaré et al., An official American thoraic society/European respiratory society statement: update on lim muscle dysfunction in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 189, 15–62 (2014)CrossRef F. Maltais, M. Decramer, R. Casaburi, E. Barreiro, Y. Burelle, R. Debigaré et al., An official American thoraic society/European respiratory society statement: update on lim muscle dysfunction in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 189, 15–62 (2014)CrossRef
33.
Zurück zum Zitat H.J. Green, M.E. Burnett, C.L. D’Arsigny, D.E. O’Donnell, J. Ouyang, K.A. Webb, Altered metabolic and transporter characteristics of vastus lateralis in chronic obstructive pulmonary disease. J. Appl. Physiol. 105, 879–886 (2008)CrossRefPubMed H.J. Green, M.E. Burnett, C.L. D’Arsigny, D.E. O’Donnell, J. Ouyang, K.A. Webb, Altered metabolic and transporter characteristics of vastus lateralis in chronic obstructive pulmonary disease. J. Appl. Physiol. 105, 879–886 (2008)CrossRefPubMed
34.
Zurück zum Zitat B.K. Pedersen, M.A. Febbraio, Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat. Rev. Endocrinol. 8, 457–465 (2012)CrossRefPubMed B.K. Pedersen, M.A. Febbraio, Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat. Rev. Endocrinol. 8, 457–465 (2012)CrossRefPubMed
35.
Zurück zum Zitat K.H. Park, L. Zaichenko, M. Brinkoetter, B. Thakkar, A. Sahin-Efe, K.E. Joung et al., Circulating irisin in relation to insulin resistance and the metabolic syndrome. J. Clin. Endocrinol. Metab. 98, 4899–4907 (2013)CrossRefPubMed K.H. Park, L. Zaichenko, M. Brinkoetter, B. Thakkar, A. Sahin-Efe, K.E. Joung et al., Circulating irisin in relation to insulin resistance and the metabolic syndrome. J. Clin. Endocrinol. Metab. 98, 4899–4907 (2013)CrossRefPubMed
36.
Zurück zum Zitat N. Ijiri, H. Kanazawa, K. Asai, T. Watanabe, K. Hirata, Irisin, a newly discovered myokine, is a novel biomaker associated with physical activity in patients with chronic obstructive pulmonary disease. Respirology 20, 612–617 (2015)CrossRefPubMed N. Ijiri, H. Kanazawa, K. Asai, T. Watanabe, K. Hirata, Irisin, a newly discovered myokine, is a novel biomaker associated with physical activity in patients with chronic obstructive pulmonary disease. Respirology 20, 612–617 (2015)CrossRefPubMed
37.
Zurück zum Zitat E.B. Geer, J. Islam, C. Buettner, Mechanisms of glucocorticoid-induced insulin resistance. Endocrinol. Metab. Clin. North Am. 43, 75–102 (2014)CrossRefPubMedPubMedCentral E.B. Geer, J. Islam, C. Buettner, Mechanisms of glucocorticoid-induced insulin resistance. Endocrinol. Metab. Clin. North Am. 43, 75–102 (2014)CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat H. Schäcke, W.D. Döcke, K. Asadullah, Mechanisms involved in the side effects of glucocorticoids. Pharmacol. Ther. 96, 23–43 (2002)CrossRefPubMed H. Schäcke, W.D. Döcke, K. Asadullah, Mechanisms involved in the side effects of glucocorticoids. Pharmacol. Ther. 96, 23–43 (2002)CrossRefPubMed
39.
Zurück zum Zitat D. Blackburn, J. Hux, M. Mamdani, Quantification of the risk of corticosteroid-induced diabetes mellitus among the elderly. J. Gen. Intern. Med. 17, 717–720 (2002)CrossRefPubMedPubMedCentral D. Blackburn, J. Hux, M. Mamdani, Quantification of the risk of corticosteroid-induced diabetes mellitus among the elderly. J. Gen. Intern. Med. 17, 717–720 (2002)CrossRefPubMedPubMedCentral
40.
Zurück zum Zitat D.E. Niewoehner, M.L. Erbland, R.H. Deupree, D. Collins, N.J. Gross, R.W. Light et al., Effects of systemic glucocoricoids on exacerbations of chronic obstructive pulmonary disease. N. Engl. J. Med. 340, 1941–1947 (1999)CrossRefPubMed D.E. Niewoehner, M.L. Erbland, R.H. Deupree, D. Collins, N.J. Gross, R.W. Light et al., Effects of systemic glucocoricoids on exacerbations of chronic obstructive pulmonary disease. N. Engl. J. Med. 340, 1941–1947 (1999)CrossRefPubMed
41.
Zurück zum Zitat S. Suissa, A. Kezouh, P. Ernst, Inhaled corticosteroids and the risk of diabetes onset and progression. Am. J. Med. 123, 1001–1006 (2010)CrossRefPubMed S. Suissa, A. Kezouh, P. Ernst, Inhaled corticosteroids and the risk of diabetes onset and progression. Am. J. Med. 123, 1001–1006 (2010)CrossRefPubMed
42.
Zurück zum Zitat P.M. O’Byrne, S. Rennard, H. Gerstein, F. Radner, S. Peterson, B. Lindberg et al., Risk of new onset diabetes mellitus in patients with asthma or COPD taking inhaled corticosteroids. Respir. Med. 106, 1487–1493 (2012)CrossRefPubMed P.M. O’Byrne, S. Rennard, H. Gerstein, F. Radner, S. Peterson, B. Lindberg et al., Risk of new onset diabetes mellitus in patients with asthma or COPD taking inhaled corticosteroids. Respir. Med. 106, 1487–1493 (2012)CrossRefPubMed
43.
Zurück zum Zitat N. Dendukuri, L. Blais, J. LeLorier, Inhlaed corticosteroids and the risk of diabetes among the elderly. Br. J. Clin. Pharmacol. 54, 59–64 (2002)CrossRefPubMedPubMedCentral N. Dendukuri, L. Blais, J. LeLorier, Inhlaed corticosteroids and the risk of diabetes among the elderly. Br. J. Clin. Pharmacol. 54, 59–64 (2002)CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat F.S. Facchini, C.B. Hollenbeck, J. Jeppesen, Y.D. Chen, G.M. Reaven, Insulin resistance and cigarette smoking. Lancet 339, 1128–1130 (1992)CrossRefPubMed F.S. Facchini, C.B. Hollenbeck, J. Jeppesen, Y.D. Chen, G.M. Reaven, Insulin resistance and cigarette smoking. Lancet 339, 1128–1130 (1992)CrossRefPubMed
45.
Zurück zum Zitat A.C. Frati, F. Iniestra, C.R. Ariza, Acute effect of cigarette smoking on glucose tolerance and other cardiovascular risk factors. Diabetes Care 19, 112–118 (1996)CrossRefPubMed A.C. Frati, F. Iniestra, C.R. Ariza, Acute effect of cigarette smoking on glucose tolerance and other cardiovascular risk factors. Diabetes Care 19, 112–118 (1996)CrossRefPubMed
46.
Zurück zum Zitat H. Cena, A. Tesone, R. Niniano, I. Cerveri, C. Roggi, G. Turconi, Prevalence rate of metabolic syndrome in a group of light and heavy smokers. Diabetol. Metab. Syndr. 5, 1–7 (2013)CrossRef H. Cena, A. Tesone, R. Niniano, I. Cerveri, C. Roggi, G. Turconi, Prevalence rate of metabolic syndrome in a group of light and heavy smokers. Diabetol. Metab. Syndr. 5, 1–7 (2013)CrossRef
47.
Zurück zum Zitat J.E. Manson, U.A. Ajani, S. Liu, D.M. Nathan, C.H. Hennekens, A prospective study of cigarette smoking and the incidence of diabetes mellitus among US male physicians. Am. J. Med. 109, 538–542 (2000)CrossRefPubMed J.E. Manson, U.A. Ajani, S. Liu, D.M. Nathan, C.H. Hennekens, A prospective study of cigarette smoking and the incidence of diabetes mellitus among US male physicians. Am. J. Med. 109, 538–542 (2000)CrossRefPubMed
48.
Zurück zum Zitat C. Willi, P. Bodenmann, W.A. Ghali, P.D. Faris, J. Cornuz, Active smoking and the risk of type 2 diabetes: a systematic review and meta-analysis. JAMA 298, 2654–2664 (2007)CrossRefPubMed C. Willi, P. Bodenmann, W.A. Ghali, P.D. Faris, J. Cornuz, Active smoking and the risk of type 2 diabetes: a systematic review and meta-analysis. JAMA 298, 2654–2664 (2007)CrossRefPubMed
49.
50.
Zurück zum Zitat B.C. Bergman, L. Perreault, D. Hunerdosse, A. Kerege, M. Playdon, A.M. Samek et al., Novel and reversible mechanisms of smoking-induced insulin resistance in humans. Diabetes 61, 3156–3166 (2012)CrossRefPubMedPubMedCentral B.C. Bergman, L. Perreault, D. Hunerdosse, A. Kerege, M. Playdon, A.M. Samek et al., Novel and reversible mechanisms of smoking-induced insulin resistance in humans. Diabetes 61, 3156–3166 (2012)CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat T. Wada, M. Urashima, T. Fukumoto, Risk of metabolic syndrome persists twenty years after the cessarion of smoking. Intern. Med. 46, 1079–1082 (2007)CrossRefPubMed T. Wada, M. Urashima, T. Fukumoto, Risk of metabolic syndrome persists twenty years after the cessarion of smoking. Intern. Med. 46, 1079–1082 (2007)CrossRefPubMed
52.
Zurück zum Zitat G. Piazzolla, A. Castrovilli, V. Liotino, M.R. Vulpi, M. Fanelli, A. Mazzocca et al., Metabolic syndome and chronic obstructive pulmonary disease (COPD): the interplay among smoking, insulin resistance and vitamin D. PLoS ONE 12, e0186708 (2017)CrossRefPubMedPubMedCentral G. Piazzolla, A. Castrovilli, V. Liotino, M.R. Vulpi, M. Fanelli, A. Mazzocca et al., Metabolic syndome and chronic obstructive pulmonary disease (COPD): the interplay among smoking, insulin resistance and vitamin D. PLoS ONE 12, e0186708 (2017)CrossRefPubMedPubMedCentral
53.
Zurück zum Zitat R.J. Dennis, D. Maldonado, M.X. Rojas, P. Aschner, M. Róndon, L. Charry et al., Inadequate glucose control in type 2 diabetes is associated with impaired lung function and systemic inflammation: a cross-sectional study. BMC Pulm. Med. 10, 38 (2010)CrossRefPubMedPubMedCentral R.J. Dennis, D. Maldonado, M.X. Rojas, P. Aschner, M. Róndon, L. Charry et al., Inadequate glucose control in type 2 diabetes is associated with impaired lung function and systemic inflammation: a cross-sectional study. BMC Pulm. Med. 10, 38 (2010)CrossRefPubMedPubMedCentral
54.
Zurück zum Zitat D.A. Lawlor, S. Ebrahim, G.D. Smith, 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 (2004)CrossRefPubMed D.A. Lawlor, S. Ebrahim, G.D. Smith, 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 (2004)CrossRefPubMed
55.
Zurück zum Zitat S. Singh, M. Bodas, N.K. Bhatraju, B. Pattnaik, A. Gheware, P.K. Parameswaran et al., Hyperinsulinemia adversely affects lung structure and function. Am. J. Physiol. Lung Cell Mol. Physiol. 310, L837–L845 (2016)CrossRefPubMedPubMedCentral S. Singh, M. Bodas, N.K. Bhatraju, B. Pattnaik, A. Gheware, P.K. Parameswaran et al., Hyperinsulinemia adversely affects lung structure and function. Am. J. Physiol. Lung Cell Mol. Physiol. 310, L837–L845 (2016)CrossRefPubMedPubMedCentral
Metadaten
Titel
Physiopathological relationship between chronic obstructive pulmonary disease and insulin resistance
verfasst von
Felipe Vilaça Cavallari Machado
Fabio Pitta
Nidia Aparecida Hernandes
Gisele Lopes Bertolini
Publikationsdatum
06.03.2018
Verlag
Springer US
Erschienen in
Endocrine / Ausgabe 1/2018
Print ISSN: 1355-008X
Elektronische ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-018-1554-z

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