Skip to main content

Advertisement

SpringerLink
Log in

Impact of diabetes on cardiopulmonary function: the added value of a combined cardiopulmonary and echocardiography stress test

  • Published:
Heart Failure Reviews Aims and scope Submit manuscript

Abstract

Type 2 diabetes mellitus (T2DM) represents a major health issue worldwide, as patients with T2DM show an excess risk of death for cardiovascular causes, twice as high as the general population. Among the many complications of T2DM, heart failure (HF) deserves special consideration as one of the leading causes of morbidity and reduced life expectancy. T2DM has been associated with different phenotypes of HF, including HF with reduced and preserved ejection fraction. Cardiopulmonary exercise testing (CPET) can evaluate the metabolic and ventilatory alterations related to myocardial dysfunction and/or peripheral impairment, representing a unique tool for the clinician to study the whole HF spectrum. While CPET allows for a thorough evaluation of functional capacity, it cannot directly differentiate central and peripheral determinants of effort intolerance. Combining CPET with imaging techniques could provide even higher accuracy and further insights into the progression of the disease since signs of left ventricular systolic and diastolic dysfunction can be detected during exercise, even in asymptomatic diabetic individuals. This review aims to dissect the alterations in cardiopulmonary function characterising patients with T2DM and HF to improve patient risk stratification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

AVO2diff:

Arterio-venous oxygen difference

BMI:

Body mass index

CAD:

Coronary artery disease

CMR:

Cardiac magnetic resonance

CO:

Cardiac output

CPET:

Cardiopulmonary exercise testing

EAT:

Epicardial adipose tissue

EF:

Ejection fraction

ESE:

Exercise stress echocardiography

HF:

Heart failure

HFpEF:

Heart failure with preserved ejection fraction

HFrEF:

Heart failure with reduced ejection fraction

HR:

Heart rate

LV:

Left ventricle

LVEF:

Left ventricle ejection fraction

SGLT2i:

Sodium-glucose cotransporter-2 inhibitors

SV:

Stroke volume

T2DM:

Type 2 diabetes mellitus

V/Q:

Ventilation/perfusion

VCO2 :

Carbon dioxide production

VO2 :

Oxygen consumption

References

  1. Zheng Y, Ley SH, Hu FB (2018) Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol 14:88–98. https://doi.org/10.1038/nrendo.2017.151

    Article  PubMed  Google Scholar 

  2. Saeedi P, Petersohn I, Salpea P et al (2019) Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res Clin Pract 157:107843. https://doi.org/10.1016/j.diabres.2019.107843

  3. Kannel B, Castelli P (1974) Role of diabetes in congestive heart failure : the Framingham study 34:29–34

    CAS  Google Scholar 

  4. Bozkurt B, Coats AJS, Tsutsui H et al (2021) Universal definition and classification of heart failure: a report of the Heart Failure Society of America, Heart Failure Association of the European Society of Cardiology, Japanese Heart Failure Society and Writing Committee of the Universal Definition o. Eur J Heart Fail ejhf.2115. https://doi.org/10.1002/ejhf.2115

  5. Nesti L, Pugliese NR, Sciuto P, Natali A (2020) Type 2 diabetes and reduced exercise tolerance: a review of the literature through an integrated physiology approach. Cardiovasc Diabetol 19:134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Pugliese NR, De Biase N, Balletti A et al (2021) Characterisation of haemodynamic and metabolic abnormalities in the heart failure spectrum: the role of combined cardiopulmonary and exercise echocardiography stress test. Minerva Cardiol Angiol. https://doi.org/10.23736/S2724-5683.21.05743-4

  7. Pugliese NR, De Biase N, Conte L et al (2021) Cardiac reserve and exercise capacity: insights from combined cardiopulmonary and exercise echocardiography stress testing. J Am Soc Echocardiogr 34:38–50. https://doi.org/10.1016/j.echo.2020.08.015

    Article  PubMed  Google Scholar 

  8. Nesti L, Pugliese NR, Sciuto P et al (2021) Mechanisms of reduced peak oxygen consumption in subjects with uncomplicated type 2 diabetes. Cardiovasc Diabetol 20:124. https://doi.org/10.1186/s12933-021-01314-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Fabiani I, Pugliese NR, La Carrubba S et al (2019) Interactive role of diastolic dysfunction and ventricular remodeling in asymptomatic subjects at increased risk of heart failure. Int J Cardiovasc Imaging 35:1231–1240. https://doi.org/10.1007/s10554-019-01560-6

    Article  PubMed  Google Scholar 

  10. Pugliese NR, De Biase N, Gargani L et al (2020) Predicting the transition to and progression of heart failure with preserved ejection fraction: a weighted risk score using bio-humoural, cardiopulmonary, and echocardiographic stress testing. Eur J Prev Cardiol. https://doi.org/10.1093/eurjpc/zwaa129

    Article  PubMed  Google Scholar 

  11. Beckman JA, Creager MA, Libby P (2002) Diabetes and atherosclerosis epidemiology, pathophysiology, and management. J Am Med Assoc 287:2570–2581

    Article  CAS  Google Scholar 

  12. Zhi YF, Prins JB, Marwick TH (2004) Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev 25:543–567. https://doi.org/10.1210/er.2003-0012

    Article  CAS  Google Scholar 

  13. McDonagh TA, Metra M, Adamo M et al (2021) 2021 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure developed by the Task Force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC) with the special contribution. Eur Heart J. https://doi.org/10.1093/EURHEARTJ/EHAB368

    Article  PubMed  PubMed Central  Google Scholar 

  14. Khan SS, Butler J, Gheorghiade M (2014) Management of comorbid diabetes mellitus and worsening heart failure. JAMA - J Am Med Assoc 311:2379–2380. https://doi.org/10.1001/jama.2014.4115

    Article  CAS  Google Scholar 

  15. Rubler S, Dlugash J, Yuceoglu YZ et al (1972) New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 30:595–602. https://doi.org/10.1016/0002-9149(72)90595-4

    Article  CAS  PubMed  Google Scholar 

  16. Camici PG, Tscho C, Carli MF Di et al (2020) Coronary microvascular dysfunction in hypertrophy and heart failure. 806–816. https://doi.org/10.1093/cvr/cvaa023

  17. Paulus WJ, Dal Canto E (2018) Distinct myocardial targets for diabetes therapy in heart failure with preserved or reduced ejection fraction. JACC Hear Fail 6:1–7. https://doi.org/10.1016/j.jchf.2017.07.012

    Article  Google Scholar 

  18. Shah SJ, Lam CSP, Svedlund S et al (2018) Prevalence and correlates of coronary microvascular dysfunction in heart failure with preserved ejection fraction: PROMIS-HFpEF. Eur Heart J 39:3439–3450. https://doi.org/10.1093/eurheartj/ehy531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Tromp J, Lim SL, Tay WT et al (2019) Microvascular disease in patients with diabetes with heart failure and reduced ejection versus preserved ejection fraction. Diabetes Care 42:1792–1799. https://doi.org/10.2337/dc18-2515

    Article  PubMed  Google Scholar 

  20. Lindman BR, Dávila-Román VG, Mann DL et al (2014) Cardiovascular phenotype in HFpEF patients with or without diabetes: a RELAX trial ancillary study. J Am Coll Cardiol 64:541–549. https://doi.org/10.1016/j.jacc.2014.05.030

    Article  PubMed  PubMed Central  Google Scholar 

  21. Meagher P, Adam M, Civitarese R et al (2018) Heart failure with preserved ejection fraction in diabetes: mechanisms and management. Canadian Cardiovascular Society

  22. Van Linthout S, Tschöpe C (2017) Inflammation – cause or consequence of heart failure or both? Curr Heart Fail Rep 14:251–265. https://doi.org/10.1007/s11897-017-0337-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Franssen C, Chen S, Unger A et al (2016) Myocardial microvascular inflammatory endothelial activation in heart failure with preserved ejection fraction. JACC Hear Fail 4:312–324. https://doi.org/10.1016/j.jchf.2015.10.007

    Article  Google Scholar 

  24. Adamo L, Rocha-Resende C, Lin CY et al (2020) Myocardial B cells are a subset of circulating lymphocytes with delayed transit through the heart JCI Insight 5.https://doi.org/10.1172/jci.insight.134700

  25. Hulsmans M, Clauss S, Xiao L et al (2017) Macrophages facilitate electrical conduction in the heart. Cell 169:510-522.e20. https://doi.org/10.1016/j.cell.2017.03.050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hotamisligil GS (2017) Foundations of immunometabolism and implications for metabolic health and disease. Immunity 47:406–420. https://doi.org/10.1016/j.immuni.2017.08.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Schiattarella GG, Rodolico D, Hill JA (2021) Metabolic inflammation in heart failure with preserved ejection fraction. Cardiovasc Res 117:423–434. https://doi.org/10.1093/cvr/cvaa217

    Article  CAS  PubMed  Google Scholar 

  28. Kleber FX (2004) The predictive value of cardiorespiratory fitness. Eur Heart J 25:1374–1375. https://doi.org/10.1016/j.ehj.2004.06.021

    Article  PubMed  Google Scholar 

  29. Arena R, Myers J, Abella J et al (2007) Development of a ventilatory classification system in patients with heart failure. Circulation 115:2410–2417. https://doi.org/10.1161/CIRCULATIONAHA.107.686576

    Article  PubMed  Google Scholar 

  30. Regensteiner JG, Bauer TA, Reusch JEB et al (2009) Cardiac dysfunction during exercise in uncomplicated type 2 diabetes. Med Sci Sports Exerc 41:977–984. https://doi.org/10.1249/MSS.0b013e3181942051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Eckstein ML, Farinha JB, McCarthy O et al (2021) Differences in physiological responses to cardiopulmonary exercise testing in adults with and without type 1 diabetes: a pooled analysis. Diabetes Care 44:240–247. https://doi.org/10.2337/dc20-1496

    Article  PubMed  Google Scholar 

  32. Pandey A, Patel KV, Bahnson JL et al (2020) Association of intensive lifestyle intervention, fitness, and body mass index with risk of heart failure in overweight or obese adults with type 2 diabetes mellitus: an analysis from the Look AHEAD trial. Circulation 141:1295–1306. https://doi.org/10.1161/CIRCULATIONAHA.119.044865

    Article  PubMed  PubMed Central  Google Scholar 

  33. Abe T, Yokota T, Fukushima A et al (2020) Type 2 diabetes is an independent predictor of lowered peak aerobic capacity in heart failure patients with non - reduced or reduced left ventricular ejection fraction. Cardiovasc Diabetol 1–10.https://doi.org/10.1186/s12933-020-01114-4

  34. Uribe-Heredia G, Arroyo-Espliguero R, Viana-Llamas MC et al (2020) Type 2 diabetes mellitus, glycated hemoglobin levels, and cardiopulmonary exercise capacity in patients with ischemic heart disease. J Cardiopulm Rehabil Prev 40:167–173. https://doi.org/10.1097/HCR.0000000000000451

    Article  PubMed  Google Scholar 

  35. Gürdal A, Kasikcioglu E, Yakal S, Bugra Z (2015) Impact of diabetes and diastolic dysfunction on exercise capacity in normotensive patients without coronary artery disease. Diabetes Vasc Dis Res 12:181–188. https://doi.org/10.1177/1479164114565631

    Article  CAS  Google Scholar 

  36. Lau ACW, Lo MKW, Leung GTC et al (2004) Altered exercise gas exchange as related to microalbuminuria in type 2 diabetic patients. Chest 125:1292–1298. https://doi.org/10.1378/chest.125.4.1292

    Article  PubMed  Google Scholar 

  37. Roberts TJ, Burns AT, MacIsaac RJ et al (2018) Exercise capacity in diabetes mellitus is predicted by activity status and cardiac size rather than cardiac function: a case control study Cardiovasc Diabetol 17. https://doi.org/10.1186/s12933-018-0688-x

  38. Gulsin GS, Henson J, Brady EM et al (2020) Cardiovascular determinants of aerobic exercise capacity in adults with type 2 diabetes. 43:2248–2256. https://doi.org/10.2337/dc20-0706

  39. Fang ZY, Sharman J, Prins JB, Marwick TH (2005) Determinants of exercise capacity in patients with type 2 diabetes. Diabetes Care 28:1643–1648. https://doi.org/10.2337/diacare.28.7.1643

    Article  PubMed  Google Scholar 

  40. Bayes-Genis A, Bisbal F, Núñez J et al (2020) Transitioning from preclinical to clinical heart failure with preserved ejection fraction: a mechanistic approach. J Clin Med 9:1110. https://doi.org/10.3390/jcm9041110

    Article  PubMed  PubMed Central  Google Scholar 

  41. Pugliese NR, Paneni F, Mazzola M et al (2021) Impact of epicardial adipose tissue on cardiovascular hemodynamics, metabolic profile, and prognosis in heart failure. Eur J Heart Fail ejhf.2337. https://doi.org/10.1002/EJHF.2337

  42. Iacobellis G (2015) Local and systemic effects of the multifaceted epicardial adipose tissue depot. Nat Rev Endocrinol 11:363–371

    Article  CAS  PubMed  Google Scholar 

  43. Iacobellis G, Willens HJ (2009) Echocardiographic epicardial fat: a review of research and clinical applications. J Am Soc Echocardiogr 22:1311–1319

    Article  PubMed  Google Scholar 

  44. Song DK, Hong YS, Lee H et al (2015) Increased epicardial adipose tissue thickness in type 2 diabetes mellitus and obesity. Diabetes Metab J 39:405–413. https://doi.org/10.4093/dmj.2015.39.5.405

    Article  PubMed  PubMed Central  Google Scholar 

  45. Philouze C, Obert P, Nottin S et al (2018) Dobutamine stress echocardiography unmasks early left ventricular dysfunction in asymptomatic patients with uncomplicated type 2 diabetes: a comprehensive two-dimensional speckle-tracking imaging study. J Am Soc Echocardiogr Off Publ Am Soc Echocardiogr 31:587–597. https://doi.org/10.1016/j.echo.2017.12.006

    Article  Google Scholar 

  46. Sugita Y, Ito K, Sakurai S et al (2020) Epicardial adipose tissue is tightly associated with exercise intolerance in patients with type 2 diabetes mellitus with asymptomatic left ventricular structural and functional abnormalities. J Diabetes Complications 34:107552. https://doi.org/10.1016/j.jdiacomp.2020.107552

    Article  PubMed  Google Scholar 

  47. Fabiani I, Pugliese NR, Galeotti GG et al (2019) The added value of exercise stress echocardiography in patients with heart failure. Am J Cardiol 123:1470–1477. https://doi.org/10.1016/j.amjcard.2019.02.008

    Article  PubMed  Google Scholar 

  48. Pugliese NR, Fabiani I, Mandoli GE et al (2019) Echo-derived peak cardiac power output-to-left ventricular mass with cardiopulmonary exercise testing predicts outcome in patients with heart failure and depressed systolic function. Eur Heart J Cardiovasc Imaging 20:700–708. https://doi.org/10.1093/ehjci/jey172

    Article  PubMed  Google Scholar 

  49. Pugliese NR, Mazzola M, Fabiani I et al (2020) Haemodynamic and metabolic phenotyping of hypertensive patients with and without heart failure by combining cardiopulmonary and echocardiographic stress test. Eur J Heart Fail 22:1–11. https://doi.org/10.1002/ejhf.1739

    Article  CAS  Google Scholar 

  50. Pugliese NR, Fabiani I, Santini C et al (2019) Value of combined cardiopulmonary and echocardiography stress test to characterize the haemodynamic and metabolic responses of patients with heart failure and mid-range ejection fraction. Eur Heart J Cardiovasc Imaging 20:828–836. https://doi.org/10.1093/ehjci/jez014

    Article  PubMed  Google Scholar 

  51. Roberts TJ, Barros-Murphy JF, Burns AT et al (2020) Reduced exercise capacity in diabetes mellitus is not associated with impaired deformation or twist. J Am Soc Echocardiogr 33:481–489. https://doi.org/10.1016/j.echo.2019.11.012

    Article  PubMed  Google Scholar 

  52. Massie B, Conway M, Yonge R et al (1987) Skeletal muscle metabolism in patients with congestive heart failure: relation to clinical severity and blood flow. Circulation 76:1009–1019. https://doi.org/10.1161/01.CIR.76.5.1009

    Article  CAS  PubMed  Google Scholar 

  53. Okita K, Nishijima H, Yonezawa K et al (1998) Skeletal muscle metabolism in maximal bicycle and treadmill exercise distinguished by using in vivo metabolic freeze method and phosphorus-31 magnetic resonance spectroscopy in normal men. Am J Cardiol 81:106–109. https://doi.org/10.1016/S0002-9149(97)00857-6

    Article  CAS  PubMed  Google Scholar 

  54. Oberbach A, Bossenz Y, Lehmann S et al (2006) Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 29:895–900. https://doi.org/10.2337/diacare.29.04.06.dc05-1854

    Article  CAS  PubMed  Google Scholar 

  55. Shimiaie J, Sherez J, Aviram G et al (2015) Determinants of effort intolerance in patients with heart failure: combined echocardiography and cardiopulmonary stress protocol. JACC Hear Fail 3:803–814. https://doi.org/10.1016/j.jchf.2015.05.010

    Article  Google Scholar 

  56. Kobayashi Y, Christle JW, Contrepois K et al (2021) Peripheral oxygen extraction and exercise limitation in asymptomatic patients with diabetes mellitus. Am J Cardiol. https://doi.org/10.1016/j.amjcard.2021.03.011

    Article  PubMed  PubMed Central  Google Scholar 

  57. Lewis GD, Shah RV, Pappagianopolas PP et al (2008) Determinants of ventilatory efficiency in heart failure: the role of right ventricular performance and pulmonary vascular tone. Circ Heart Fail 1:227–233. https://doi.org/10.1161/CIRCHEARTFAILURE.108.785501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Scali MC, Cortigiani L, Simionuc A et al (2017) Exercise-induced B-lines identify worse functional and prognostic stage in heart failure patients with depressed left ventricular ejection fraction. Eur J Heart Fail 19:1468–1478. https://doi.org/10.1002/ejhf.776

    Article  CAS  PubMed  Google Scholar 

  59. Gargani L, Pugliese NR, Frassi F et al (2021) Prognostic value of lung ultrasound in patients hospitalized for heart disease irrespective of symptoms and ejection fraction. ESC Hear Fail ehf2.13206. https://doi.org/10.1002/ehf2.13206

  60. Pugliese NR, Fabiani I, Conte L et al (2020) Persistent congestion, renal dysfunction and inflammatory cytokines in acute heart failure: a prognosis study. J Cardiovasc Med 21:494–502. https://doi.org/10.2459/JCM.0000000000000974

    Article  CAS  Google Scholar 

  61. Scali MC, Zagatina A, Ciampi Q et al (2020) Lung ultrasound and pulmonary congestion during stress echocardiography. JACC Cardiovasc Imaging 13:2085–2095. https://doi.org/10.1016/j.jcmg.2020.04.020

    Article  PubMed  Google Scholar 

  62. Picano E, Scali MC, Ciampi Q, Lichtenstein D (2018) Lung ultrasound for the cardiologist. JACC Cardiovasc Imaging 11:1692–1705. https://doi.org/10.1016/j.jcmg.2018.06.023

    Article  PubMed  Google Scholar 

  63. Fowler MJ (2008) Microvascular and macrovascular complications of diabetes. Clin Diabetes 26:77 LP – 82. https://doi.org/10.2337/diaclin.26.2.77

  64. Boulé NG, Haddad E, Kenny GP et al (2001) Effects of exercise on glycemic control and body mass in type 2 diabetes mellitus: a meta-analysis of controlled clinical trials. J Am Med Assoc 286:1218–1227. https://doi.org/10.1001/jama.286.10.1218

    Article  Google Scholar 

  65. Gulsin GS, Swarbrick DJ, Athithan L et al (2020) Effects of low-energy diet or exercise on cardiovascular function in working-age adults with type 2 diabetes : a prospective , randomized , open- label , blinded end point trial. 1–11. https://doi.org/10.2337/dc20-0129

  66. Gulsin GS, Athithan L, McCann GP (2019) Diabetic cardiomyopathy: prevalence, determinants and potential treatments. Ther Adv Endocrinol Metab 10:1–21

    Article  Google Scholar 

  67. Colberg SR, Sigal RJ, Yardley JE et al (2016) Physical activity/exercise and diabetes: a position statement of the American Diabetes Association. Diabetes Care 39:2065–2079. https://doi.org/10.2337/dc16-1728

    Article  PubMed  PubMed Central  Google Scholar 

  68. Verma S, Mazer CD, Yan AT et al (2019) Effect of empagliflozin on left ventricular mass in patients with type 2 diabetes mellitus and coronary artery disease: the EMPA-HEART CardioLink-6 randomized clinical trial. Circulation 140:1693–1702. https://doi.org/10.1161/CIRCULATIONAHA.119.042375

    Article  PubMed  Google Scholar 

  69. Drucker DJ (2007) Dipeptidyl peptidase-4 inhibition and the treatment of type 2 diabetes: preclinical biology and mechanisms of action. Diabetes Care 30:1335–1343. https://doi.org/10.2337/dc07-0228

    Article  CAS  PubMed  Google Scholar 

  70. Fujimoto N, Moriwaki K, Takeuchi T et al (2020) Effects of sitagliptin on exercise capacity and hemodynamics in patients with type 2 diabetes mellitus and coronary artery disease. Heart Vessels 35:605–613. https://doi.org/10.1007/s00380-019-01526-7

    Article  PubMed  Google Scholar 

  71. Shigeta T, Aoyama M, Bando YK et al (2012) Dipeptidyl peptidase-4 modulates left ventricular dysfunction in chronic heart failure via angiogenesis-dependent and -independent actions. Circulation 126:1838–1851. https://doi.org/10.1161/CIRCULATIONAHA.112.096479

    Article  CAS  PubMed  Google Scholar 

  72. Marwick TH, Hordern MD, Miller T et al (2009) Exercise training for type 2 diabetes mellitus: impact on cardiovascular risk: a scientific statement from the American Heart Association. Circulation 119:3244–3262. https://doi.org/10.1161/CIRCULATIONAHA.109.192521

    Article  PubMed  Google Scholar 

  73. Cosentino F, Grant PJ, Aboyans V et al (2020) 2019 ESC Guidelines on diabetes, pre-diabetes, and cardiovascular diseases developed in collaboration with the EASD. Eur Heart J 41:255–323. https://doi.org/10.1093/eurheartj/ehz486

    Article  PubMed  Google Scholar 

  74. Rena G, Hardie DG, Pearson ER (2017) The mechanisms of action of metformin. Diabetologia 60:1577–1585. https://doi.org/10.1007/s00125-017-4342-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Wong AKF, Symon R, Alzadjali MA et al (2012) The effect of metformin on insulin resistance and exercise parameters in patients with heart failure. Eur J Heart Fail 14:1303–1310. https://doi.org/10.1093/eurjhf/hfs106

    Article  CAS  PubMed  Google Scholar 

  76. Cadeddu C, Nocco S, Cugusi L et al (2014) Effects of metformin and exercise training, alone or in association, on cardio-pulmonary performance and quality of life in insulin resistance patients. Cardiovasc Diabetol 13:93. https://doi.org/10.1186/1475-2840-13-93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Cowie MR, Fisher M (2020) SGLT2 inhibitors: mechanisms of cardiovascular benefit beyond glycaemic control. Nat Rev Cardiol 17:761–772. https://doi.org/10.1038/s41569-020-0406-8

    Article  CAS  PubMed  Google Scholar 

  78. Bluemke DA, Kronmal RA, Lima JAC et al (2008) The relationship of left ventricular mass and geometry to incident cardiovascular events. The MESA (Multi-Ethnic Study of Atherosclerosis) study. J Am Coll Cardiol. https://doi.org/10.1016/j.jacc.2008.09.014

  79. Pugliese NR, Fabiani I, La Carrubba S et al (2017) Classification and prognostic evaluation of left ventricular remodeling in patients with asymptomatic heart failure. Am J Cardiol 119:71–77. https://doi.org/10.1016/j.amjcard.2016.09.018

    Article  PubMed  Google Scholar 

  80. Dini FL, Galeotti GG, Terlizzese G et al (2019) Left ventricular mass and thickness: why does it matter? Heart Fail Clin 15:159–166. https://doi.org/10.1016/j.hfc.2018.12.013

    Article  PubMed  Google Scholar 

  81. Oldgren J, Laurila S, Åkerblom A et al (2021) Effects of 6 weeks of treatment with dapagliflozin, a sodium-glucose co-transporter-2 inhibitor, on myocardial function and metabolism in patients with type 2 diabetes: a randomized, placebo-controlled, exploratory study Diabetes, Obes Metab 1–13 https://doi.org/10.1111/dom.14363

  82. Carbone S, Canada JM, Billingsley HE et al (1918). Effects of empagliflozin on cardiorespiratory fitness and significant interaction of loop diuretics Running title. https://doi.org/10.1111/dom.13309

    Article  Google Scholar 

  83. Nassif ME, Qintar M, Windsor SL et al (2021) Empagliflozin effects on pulmonary artery pressure in patients with heart failure: results from EMpagliflozin Evaluation By MeasuRing ImpAct on HemodynamiCs in PatiEnts with Heart Failure (EMBRACE-HF) trial Circulation 1673–1686. https://doi.org/10.1161/circulationaha.120.052503

  84. Aroda VR (2018) A review of GLP-1 receptor agonists: evolution and advancement, through the lens of randomised controlled trials. Diabetes Obes Metab 20(Suppl 1):22–33. https://doi.org/10.1111/dom.13162

    Article  CAS  PubMed  Google Scholar 

  85. Wägner AM, Miranda-Calderín G, Ugarte-Lopetegui MA et al (2019) Effect of liraglutide on physical performance in type 2 diabetes: results of a randomized, double-blind, controlled trial (LIPER2). Diabetes Metab 45:268–275. https://doi.org/10.1016/j.diabet.2018.08.010

    Article  CAS  PubMed  Google Scholar 

  86. Lepore JJ, Olson E, Demopoulos L et al (2016) Effects of the novel long-acting GLP-1 agonist, albiglutide, on cardiac function, cardiac metabolism, and exercise capacity in patients with chronic heart failure and reduced ejection fraction. JACC Heart Fail 4:559–566. https://doi.org/10.1016/j.jchf.2016.01.008

    Article  PubMed  Google Scholar 

  87. Seferović PM, Coats AJS, Ponikowski P et al (2020) European Society of Cardiology/Heart Failure Association position paper on the role and safety of new glucose-lowering drugs in patients with heart failure. Eur J Heart Fail 22:196–213. https://doi.org/10.1002/ejhf.1673

    Article  PubMed  Google Scholar 

  88. Li L, Li S, Deng K et al (2016) Dipeptidyl peptidase-4 inhibitors and risk of heart failure in type 2 diabetes: systematic review and meta-analysis of randomised and observational studies. BMJ 352.https://doi.org/10.1136/bmj.i610

  89. Fabiani I, Pugliese NR, Conte L et al (2017) Incremental prognostic value of a complex left ventricular remodeling classification in asymptomatic for heart failure hypertensive patients. J Am Soc Hypertens 11:412–419. https://doi.org/10.1016/j.jash.2017.05.005

    Article  PubMed  Google Scholar 

  90. Carbone S, Canada JM, Billingsley HE et al (2018) Effects of empagliflozin on cardiorespiratory fitness and significant interaction of loop diuretics. Diabetes, Obes Metab 20:2014–2018. https://doi.org/10.1111/dom.13309

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Clinical and Experimental Medicine, University of Pisa, Via Roma, 67, 56126, Pisa, Italy

    Nicola Riccardo Pugliese, Alessandra Pieroni, Nicolò De Biase, Valerio Di Fiore & Lorenzo Nesti

  2. Centro Cardiologico Monzino, IRCCS, Milan, Italy

    Piergiuseppe Agostoni

  3. Centro Medico Sant’Agostino, Milan, Italy

    Frank Lloyd Dini

  4. Department of Clinical Sciences and Community Medicine, University of Milan, Milan, Italy

    Frank Lloyd Dini

Authors
  1. Nicola Riccardo Pugliese
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alessandra Pieroni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicolò De Biase
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Valerio Di Fiore
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lorenzo Nesti
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Piergiuseppe Agostoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Frank Lloyd Dini
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Nicola Riccardo Pugliese, Alessandra Pieroni, Nicolò De Biase and Valerio Di Fiore. The first draft of the manuscript was written by Nicola Riccardo Pugliese, Alessandra Pieroni and Nicolò De Biase. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Ethics declarations

All authors take responsibility for all aspects of the reliability and freedom from bias of the data presented and their discussed interpretation.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pugliese, N.R., Pieroni, A., De Biase, N. et al. Impact of diabetes on cardiopulmonary function: the added value of a combined cardiopulmonary and echocardiography stress test. Heart Fail Rev 28, 645–655 (2023). https://doi.org/10.1007/s10741-021-10194-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10741-021-10194-7

Keywords

Search

Navigation