Speckle-Tracking Analysis of the Right and Left Heart after Peak Exercise in Healthy Subjects with Type 1 Diabetes: An Explorative Analysis of the AppEx Trial
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Echocardiographic Examination
2.3. Statistical Analyses
3. Results
3.1. Baseline T1D Subjects’ Characteristics and Structural and Functional Echocardiographic Assessment at Resting Conditions
3.2. T1D Speckle-Tracking Analysis of the Left and Right Heart at Resting Conditions and Dynamic Functional Cardiac Remodeling Post Peak Exercise
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Boudina, S.; Abel, E.D. Diabetic Cardiomyopathy Revisited. Circulation 2007, 115, 3213–3223. [Google Scholar] [CrossRef] [PubMed]
- Morrish, N.J.; Wang, S.-L.; Stevens, L.K.; Fuller, J.H.; Keen, H. Mortality and Causes of Death in the WHO Multinational Study of Vascular Disease in Diabetes. Diabetologia 2001, 44, S14–S21. [Google Scholar] [CrossRef] [PubMed]
- Matteucci, E.; Giampietro, O. Epidemiology of Cardiovascular Disease in Patients with Type 1 Diabetes: European Perspective. Exp. Clin. Endocrinol. Diabetes 2014, 122, 208–214. [Google Scholar] [CrossRef] [PubMed]
- Theilade, S.; Rossing, P.; Jensen, J.S.; Jensen, M.T. Arterial-Ventricular Coupling in Type 1 Diabetes: Arterial Stiffness Is Associated with Impaired Global Longitudinal Strain in Type 1 Diabetes Patients—The Thousand & 1 Study. Acta Diabetol. 2018, 55, 21–29. [Google Scholar] [CrossRef] [PubMed]
- Gæde, P.; Lund-Andersen, H.; Parving, H.-H.; Pedersen, O. Effect of a Multifactorial Intervention on Mortality in Type 2 Diabetes. N. Engl. J. Med. 2008, 358, 580–591. [Google Scholar] [CrossRef]
- Black, J.A.; Sharp, S.J.; Wareham, N.J.; Sandbæk, A.; Rutten, G.E.H.M.; Lauritzen, T.; Khunti, K.; Davies, M.J.; Borch-Johnsen, K.; Griffin, S.J.; et al. Does Early Intensive Multifactorial Therapy Reduce Modelled Cardiovascular Risk in Individuals with Screen-detected Diabetes? Results from the ADDITION-Europe Cluster Randomized Trial. Diabet. Med. 2014, 31, 647–656. [Google Scholar] [CrossRef]
- Spector, K.S. Diabetic Cardiomyopathy. Clin. Cardiol. 1998, 21, 885–887. [Google Scholar] [CrossRef]
- Berg, T.J.; Snorgaard, O.; Faber, J.; Torjesen, P.A.; Hildebrandt, P.; Mehlsen, J.; Hanssen, K.F. Serum Levels of Advanced Glycation End Products Are Associated with Left Ventricular Diastolic Function in Patients with Type 1 Diabetes. Diabetes Care 1999, 22, 1186–1190. [Google Scholar] [CrossRef]
- Avendano, G.F.; Agarwal, R.K.; Bashey, R.I.; Lyons, M.M.; Soni, B.J.; Jyothirmayi, G.N.; Regan, T.J. Effects of Glucose Intolerance on Myocardial Function and Collagen-Linked Glycation. Diabetes 1999, 48, 1443–1447. [Google Scholar] [CrossRef]
- Persson, M.; Östling, G.; Smith, G.; Hamrefors, V.; Melander, O.; Hedblad, B.; Engström, G. Soluble Urokinase Plasminogen Activator Receptor. Stroke 2014, 45, 18–23. [Google Scholar] [CrossRef]
- Llauradó, G.; Ceperuelo-Mallafré, V.; Vilardell, C.; Simó, R.; Gil, P.; Cano, A.; Vendrell, J.; González-Clemente, J.-M. Advanced Glycation End Products Are Associated with Arterial Stiffness in Type 1 Diabetes. J. Endocrinol. 2014, 221, 405–413. [Google Scholar] [CrossRef] [PubMed]
- Forbes, J.M.; Cooper, M.E. Mechanisms of Diabetic Complications. Physiol. Rev. 2013, 93, 137–188. [Google Scholar] [CrossRef]
- Aso, Y.; Inukai, T.; Tayama, K.; Takemura, Y. Serum Concentrations of Advanced Glycation Endproducts Are Associated with the Development of Atherosclerosis as Well as Diabetic Microangiopathy in Patients with Type 2 Diabetes. Acta Diabetol. 2000, 37, 87–92. [Google Scholar] [CrossRef]
- Mochizuki, Y.; Tanaka, H.; Matsumoto, K.; Sano, H.; Shimoura, H.; Ooka, J.; Sawa, T.; Motoji, Y.; Ryo-Koriyama, K.; Hirota, Y.; et al. Impact of Left Ventricular Longitudinal Functional Mechanics on the Progression of Diastolic Function in Diabetes Mellitus. Int. J. Cardiovasc. Imaging 2017, 33, 1905–1914. [Google Scholar] [CrossRef] [PubMed]
- Jensen, M.T.; Sogaard, P.; Andersen, H.U.; Bech, J.; Fritz Hansen, T.; Biering-Sørensen, T.; Jørgensen, P.G.; Galatius, S.; Madsen, J.K.; Rossing, P.; et al. Global Longitudinal Strain Is Not Impaired in Type 1 Diabetes Patients Without Albuminuria. JACC Cardiovasc. Imaging 2015, 8, 400–410. [Google Scholar] [CrossRef] [PubMed]
- Van Berendoncks, A.M.; Van Gaal, L.; De Block, C.; Buys, D.; Salgado, R.; Vrints, C.; Shivalkar, B. Abnormal Longitudinal Peak Systolic Strain in Asymptomatic Patients with Type I Diabetes Mellitus. Echocardiography 2019, 36, 478–485. [Google Scholar] [CrossRef]
- Minciună, I.; Hilda Orășan, O.; Minciună, I.; Lazar, A.; Sitar-Tăut, A.V.; Oltean, M.; Tomoaia, R.; Puiu, M.; Sitar-Tăut, D.; Pop, D.; et al. Assessment of Subclinical Diabetic Cardiomyopathy by Speckle-tracking Imaging. Eur. J. Clin. Invest. 2021, 51, e13475. [Google Scholar] [CrossRef]
- Berceanu, M.; Mirea, O.; Donoiu, I.; Militaru, C.; Săftoiu, A.; Istrătoaie, O. Myocardial Function Assessed by Multi-Layered Two-Dimensional Speckle Tracking Analysis in Asymptomatic Young Subjects with Diabetes Mellitus Type 1. Cardiology 2020, 145, 80–87. [Google Scholar] [CrossRef]
- Cameli, M.; Mandoli, G.E.; Lisi, E.; Ibrahim, A.; Incampo, E.; Buccoliero, G.; Rizzo, C.; Devito, F.; Ciccone, M.M.; Mondillo, S. Left Atrial, Ventricular and Atrio-Ventricular Strain in Patients with Subclinical Heart Dysfunction. Int. J. Cardiovasc. Imaging 2019, 35, 249–258. [Google Scholar] [CrossRef]
- Tadic, M.; Cuspidi, C. Left Atrial Function in Diabetes: Does It Help? Acta Diabetol. 2021, 58, 131–137. [Google Scholar] [CrossRef]
- Ifuku, M.; Takahashi, K.; Hosono, Y.; Iso, T.; Ishikawa, A.; Haruna, H.; Takubo, N.; Komiya, K.; Kurita, M.; Ikeda, F.; et al. Left Atrial Dysfunction and Stiffness in Pediatric and Adult Patients with Type 1 Diabetes Mellitus Assessed with Speckle Tracking Echocardiography. Pediatr. Diabetes 2021, 22, 303–319. [Google Scholar] [CrossRef] [PubMed]
- Harriss, D.J.; MacSween, A.; Atkinson, G. Ethical Standards in Sport and Exercise Science Research: 2020 Update. Int. J. Sports Med. 2019, 40, 813–817. [Google Scholar] [CrossRef] [PubMed]
- Evangelista, A.; Flachskampf, F.; Lancellotti, P.; Badano, L.; Aguilar, R.; Monaghan, M.; Zamorano, J.; Nihoyannopoulos, P. European Association of Echocardiography Recommendations for Standardization of Performance, Digital Storage and Reporting of Echocardiographic Studies. Eur. J. Echocardiogr. 2008, 9, 438–448. [Google Scholar] [CrossRef] [PubMed]
- Zimmermann, P.; Eckstein, M.L.; Moser, O.; Schöffl, I.; Zimmermann, L.; Schöffl, V. Left Ventricular, Left Atrial and Right Ventricular Strain Modifications after Maximal Exercise in Elite Ski-Mountaineering Athletes: A Feasibility Speckle Tracking Study. Int. J. Environ. Res. Public Health 2022, 19, 13153. [Google Scholar] [CrossRef]
- Zimmermann, P.; Moser, O.; Eckstein, M.L.; Wüstenfeld, J.; Schöffl, V.; Zimmermann, L.; Braun, M.; Schöffl, I. Athlete’s Heart in Elite Biathlon, Nordic Cross—Country and Ski-Mountaineering Athletes: Cardiac Adaptions Determined Using Echocardiographic Data. J. Cardiovasc. Dev. Dis. 2021, 9, 8. [Google Scholar] [CrossRef]
- Lang, R.; Bierig, M.; Devereux, R.; Flachskampf, F.; Foster, E.; Pellikka, P.; Picard, M.; Roman, M.; Seward, J.; Shanewise, J. Recommendations for Chamber Quantification☆. Eur. J. Echocardiogr. 2006, 7, 79–108. [Google Scholar] [CrossRef]
- Lang, R.M.; Badano, L.P.; Mor-Avi, V.; Afilalo, J.; Armstrong, A.; Ernande, L.; Flachskampf, F.A.; Foster, E.; Goldstein, S.A.; Kuznetsova, T.; et al. Recommendations for Cardiac Chamber Quantification by Echocardiography in Adults: An Update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J. Am. Soc. Echocardiogr. 2015, 28, 1–39.e14. [Google Scholar] [CrossRef]
- Hagendorff, A.; Fehske, W.; Flachskampf, F.A.; Helfen, A.; Kreidel, F.; Kruck, S.; la Rosée, K.; Tiemann, K.; Voigt, J.-U.; von Bardeleben, R.S.; et al. Manual Zur Indikation Und Durchführung Der Echokardiographie—Update 2020 Der Deutschen Gesellschaft Für Kardiologie. Kardiologe 2020, 14, 396–431. [Google Scholar] [CrossRef]
- Galderisi, M.; Cosyns, B.; Edvardsen, T.; Cardim, N.; Delgado, V.; di Salvo, G.; Donal, E.; Sade, L.E.; Ernande, L.; Garbi, M.; et al. Standardization of Adult Transthoracic Echocardiography Reporting in Agreement with Recent Chamber Quantification, Diastolic Function, and Heart Valve Disease Recommendations: An Expert Consensus Document of the European Association of Cardiovascular Imaging. Eur. Heart J. Cardiovasc. Imaging 2017, 18, 1301–1310. [Google Scholar] [CrossRef]
- Badano, L.P.; Kolias, T.J.; Muraru, D.; Abraham, T.P.; Aurigemma, G.; Edvardsen, T.; D’Hooge, J.; Donal, E.; Fraser, A.G.; Marwick, T.; et al. Standardization of Left Atrial, Right Ventricular, and Right Atrial Deformation Imaging Using Two-Dimensional Speckle Tracking Echocardiography: A Consensus Document of the EACVI/ASE/Industry Task Force to Standardize Deformation Imaging. Eur. Heart J. Cardiovasc. Imaging 2018, 19, 591–600. [Google Scholar] [CrossRef]
- Weber, T.R.; da Silva, R.L.; Cossul, S.; Alves, M.S.L.; Lee, S.V.d.S.; Marques, J.L.B. The Use of Echocardiography in Type 1 Diabetes. Rev. Port. Cardiol. 2021, 40, 757–765. [Google Scholar] [CrossRef] [PubMed]
- Kapelios, C.J.; Bonou, M.; Barmpagianni, A.; Tentolouris, A.; Tsilingiris, D.; Eleftheriadou, I.; Skouloudi, M.; Kanellopoulos, P.N.; Lambadiari, V.; Masoura, C.; et al. Early Left Ventricular Systolic Dysfunction in Asymptomatic Patients with Type 1 Diabetes: A Single-Center, Pilot Study. J. Diabetes Complicat. 2021, 35, 107913. [Google Scholar] [CrossRef] [PubMed]
- Andreasen, C.R.; Andersen, A.; Hagelqvist, P.G.; Lauritsen, J.V.; Jørgensen, P.G.; Engberg, S.; Faber, J.; Hartmann, B.; Pedersen-Bjergaard, U.; Knop, F.K.; et al. Hypoglycaemia and Rebound Hyperglycaemia Increase Left Ventricular Systolic Function in Patients with Type 1 Diabetes. Diabetes Obes. Metab. 2022, 24, 2027–2037. [Google Scholar] [CrossRef] [PubMed]
- Sonaglioni, A.; Nicolosi, G.L.; Trevisan, R.; Lombardo, M.; Grasso, E.; Gensini, G.F.; Ambrosio, G. The Influence of Pectus Excavatum on Cardiac Kinetics and Function in Otherwise Healthy Individuals: A Systematic Review. Int. J. Cardiol. 2023, 381, 135–144. [Google Scholar] [CrossRef]
- Jensen, M.T.; Sogaard, P.; Gustafsson, I.; Bech, J.; Hansen, T.F.; Almdal, T.; Theilade, S.; Biering-Sørensen, T.; Jørgensen, P.G.; Galatius, S.; et al. Echocardiography Improves Prediction of Major Adverse Cardiovascular Events in a Population with Type 1 Diabetes and without Known Heart Disease: The Thousand & 1 Study. Diabetologia 2019, 62, 2354–2364. [Google Scholar] [CrossRef]
- Zairi, I.; Mzoughi, K.; Kamoun, S.; Moussa, F.B.; Rezgallah, R.; Maatoug, J.; Mazigh, S.; Kraiem, S. Impairment of Left and Right Ventricular Longitudinal Strain in Asymptomatic Children with Type 1 Diabetes. Indian Heart J. 2019, 71, 249–255. [Google Scholar] [CrossRef]
- Ahmed, T.A.; Ahmed, Y.A.; Arafa, A.I.; Salah, R.A. Detection of Occult Right Ventricular Dysfunction in Young Egyptians with Type 1 Diabetes Mellitus by Two-Dimensional Speckle Tracking Echocardiography. Indian Heart J. 2018, 70, 665–671. [Google Scholar] [CrossRef]
- Berceanu, M.; Mirea, O.; Târtea, G.C.; Donoiu, I.; Militaru, C.; Istrătoaie, O.; Săftoiu, A. The Significance of Right Ventricle in Young Subjects with Diabetes Mellitus Type 1. An Echocardiographyic Study. Curr. Health Sci. J. 2019, 45, 174–178. [Google Scholar] [CrossRef] [PubMed]
- Brand, A.; Frumkin, D.; Hübscher, A.; Dreger, H.; Stangl, K.; Baldenhofer, G.; Knebel, F. Phasic Left Atrial Strain Analysis to Discriminate Cardiac Amyloidosis in Patients with Unclear Thick Heart Pathology. Eur. Heart J. Cardiovasc. Imaging 2021, 22, 680–687. [Google Scholar] [CrossRef]
- Ersbøll, M.; Andersen, M.J.; Valeur, N.; Mogensen, U.M.; Waziri, H.; Møller, J.E.; Hassager, C.; Søgaard, P.; Køber, L. The Prognostic Value of Left Atrial Peak Reservoir Strain in Acute Myocardial Infarction Is Dependent on Left Ventricular Longitudinal Function and Left Atrial Size. Circ. Cardiovasc. Imaging 2013, 6, 26–33. [Google Scholar] [CrossRef]
- Miglioranza, M.H.; Badano, L.P.; Mihăilă, S.; Peluso, D.; Cucchini, U.; Soriani, N.; Iliceto, S.; Muraru, D. Physiologic Determinants of Left Atrial Longitudinal Strain: A Two-Dimensional Speckle-Tracking and Three-Dimensional Echocardiographic Study in Healthy Volunteers. J. Am. Soc. Echocardiogr. 2016, 29, 1023–1034.e3. [Google Scholar] [CrossRef] [PubMed]
- Santos, A.B.S.; Roca, G.Q.; Claggett, B.; Sweitzer, N.K.; Shah, S.J.; Anand, I.S.; Fang, J.C.; Zile, M.R.; Pitt, B.; Solomon, S.D.; et al. Prognostic Relevance of Left Atrial Dysfunction in Heart Failure With Preserved Ejection Fraction. Circ. Heart Fail. 2016, 9, e002763. [Google Scholar] [CrossRef] [PubMed]
T1D Male n = 5 | T1D Female n = 3 | |
---|---|---|
Age (years) | 47.0 ± 17.5 | 39.3 ± 14.4 |
Height (cm) | 179.2 ± 5.7 | 163.3 ± 6.4 |
Weight (kg) | 76.7 ± 10.4 | 61.8 ± 0.8 |
BMI (kg/m2) | 23.8 ± 2.6 | 23.2 ± 1.4 |
Duration of T1D (years) | 16.8 ± 10.1 | 12.0 ± 1.7 |
HbA1c (%) | 6.4 ± 0.3 | 7.8 ± 1.9 |
T1D Male n = 5 | T1D Female n = 3 | Reference Value Male | Reference Value Female | |
---|---|---|---|---|
LV edd (mm) | 48.00 ± 4.53 | 38.33 ± 2.52 | 42–58 | 38–52 |
LV Mass Index (g/m2) | 79.40 ± 24.03 | 58.33 ± 5.51 | 49–115 | 43–95 |
Relative Wall Thickness RWT | 0.37 ± 0.03 | 0.43 ± 0.04 | ||
IVSd (mm) | 9.40 ± 1.14 | 9.00 ± 0 | 6–10 | 6–9 |
LVPWd (mm) | 8.80 ± 0.84 | 8.33 ± 0.58 | 6–10 | 6–9 |
E/A | 1.62 ± 0.72 | 1.13 ± 0.06 | ||
E/E’ | 7.76 ± 1.30 | 6.56 ± 2.20 | ||
LAVI (mL/m2) | 27.40 ± 6.54 | 30.33 ± 6.66 | ||
LV − EFrest (%) | 59.40 ± 0.89 | 60.00 ± 5.00 | 52–72 | 54–72 |
LV − EFpost-stress (%) | 69.40 ± 1.76 | 70.00 ± 5.00 |
T1D Rest n = 8 | T1D Post Exercise n = 8 | p-Value | |
---|---|---|---|
RV FW long Def. | −23.85 ± 6.40 | −26.05 ± 6.92 | 0.5839 |
RV 4C long Def. | −20.58 ± 3.93 | −21.45 ± 4.77 | 0.7419 |
LV GLS mean | −18.05 ± 2.31 | −17.41 ± 3.24 | 0.5952 |
LV reservoir | 41.45 ± 9.15 | 40.53 ± 7.99 | 0.8379 |
LA conduit | −23.53 ± 8.28 | −16.15 ± 6.51 | 0.0624 |
LA contractile | −17.91 ± 5.89 | −26.11 ± 5.61 | 0.0003 * |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zimmermann, P.; Schierbauer, J.; Kopf, N.; Sourij, H.; Oliver, N.; Aberer, F.; Wachsmuth, N.B.; Moser, O. Speckle-Tracking Analysis of the Right and Left Heart after Peak Exercise in Healthy Subjects with Type 1 Diabetes: An Explorative Analysis of the AppEx Trial. J. Cardiovasc. Dev. Dis. 2023, 10, 467. https://doi.org/10.3390/jcdd10110467
Zimmermann P, Schierbauer J, Kopf N, Sourij H, Oliver N, Aberer F, Wachsmuth NB, Moser O. Speckle-Tracking Analysis of the Right and Left Heart after Peak Exercise in Healthy Subjects with Type 1 Diabetes: An Explorative Analysis of the AppEx Trial. Journal of Cardiovascular Development and Disease. 2023; 10(11):467. https://doi.org/10.3390/jcdd10110467
Chicago/Turabian StyleZimmermann, Paul, Janis Schierbauer, Niklas Kopf, Harald Sourij, Nick Oliver, Felix Aberer, Nadine B. Wachsmuth, and Othmar Moser. 2023. "Speckle-Tracking Analysis of the Right and Left Heart after Peak Exercise in Healthy Subjects with Type 1 Diabetes: An Explorative Analysis of the AppEx Trial" Journal of Cardiovascular Development and Disease 10, no. 11: 467. https://doi.org/10.3390/jcdd10110467
APA StyleZimmermann, P., Schierbauer, J., Kopf, N., Sourij, H., Oliver, N., Aberer, F., Wachsmuth, N. B., & Moser, O. (2023). Speckle-Tracking Analysis of the Right and Left Heart after Peak Exercise in Healthy Subjects with Type 1 Diabetes: An Explorative Analysis of the AppEx Trial. Journal of Cardiovascular Development and Disease, 10(11), 467. https://doi.org/10.3390/jcdd10110467