Abstract
Background
The incidence of preserved ejection fraction heart failure has significantly increased in persons with type 2 diabetes mellitus (T2DM). Left ventricular (LV) diastolic dysfunction is an early and important manifestation of preserved ejection fraction heart failure. The onset of heart failure in persons with diabetes is associated with diabetic neuropathy. However, the relationship among sudomotor function, which is an early manifestation of small fiber neuropathy, and LV diastolic function remains unclear. This study aimed to explore the association between sudomotor function and LV diastolic function in persons with T2DM.
Methods
In total, 699 persons with T2DM were enrolled and divided into three groups according to electrochemical skin conductance (ESC) assessed using the SUDOSCAN device: “no dysfunction” group (NSF), “moderate dysfunction” group (MDF), and “severe dysfunction” group (SDF). LV diastolic function was assessed using Doppler echocardiography. To evaluate the relationship between ESC and echocardiographic parameters, Pearson’s correlation analysis was performed. Additionally, logistic regression analysis was used to determine the association between LV diastolic function and ESC. A receiver operating characteristic (ROC) curve was constructed to evaluate the performance of sudomotor function indicators in detecting impaired cardiac diastolic function.
Results
There were 301 persons (43.06%) in the NSF group, 232 (33.19%) in the MDF group, and 166 (23.75%) in the SDF group. Compared to the NSF group, the MDF and SDF groups had higher A and E/e′ and lower e′ values (all p < 0.05). Pearson’s correlation analysis showed that A and E/e′ were negatively associated with foot ESC (FESC) and hand ESC (HESC), whereas e′ was positively associated with FESC and HESC (all p < 0.05). After adjusting for confounding factors, binary logistic regression analysis showed that ESC was independently associated with impaired LV diastolic function (p = 0.003). The area under the ROC curve values for FESC and HESC were 0.621 and 0.635, respectively (both p < 0.05).
Conclusions
Deteriorating sudomotor function was associated with reduced diastolic function indicators. ESC can be used as a biomarker for detecting LV diastolic impairment.
Similar content being viewed by others
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- T2DM:
-
Type 2 diabetes mellitus
- LVDD:
-
Left ventricular diastolic dysfunction
- LV:
-
Left ventricular
- ESC:
-
Electrochemical skin conductance
- NSF:
-
No dysfunction group
- MDF:
-
Moderate dysfunction group
- SDF:
-
Severe dysfunction group
- HESC:
-
Hand electrochemical skin conductance
- FESC:
-
Foot electrochemical skin conductance
- LVMI:
-
Left ventricular mass index
- SFN:
-
Small fiber neuropathy
- HRV:
-
Heart rate variability
- eGFR:
-
Estimated glomerular filtration rate
- LVEF:
-
Left ventricular ejection fraction
- HF:
-
Heart failure
- HFpEF:
-
Preserved ejection fraction heart failure
- WHR:
-
Waist-to-hip ratio
- BMI:
-
Body mass index
- DBP:
-
Diastolic blood pressure
- FC-P:
-
Fasting C-peptide
- PC-P:
-
Postprandial C-peptide
- LDL-C:
-
Low-density lipoprotein cholesterol
- ACR:
-
Creatinine ratio
- HbA1C :
-
Glycated hemoglobin
- Scr:
-
Serum creatinine
References
Roger VL, Weston SA, Redfield MM et al (2004) Trends in heart failure incidence and survival in a community-based population. JAMA 292(3):344–350
Gustafsson I, Brendorp B, Seibaek M et al (2004) Influence of diabetes and diabetes-gender interaction on the risk of death in patients hospitalized with congestive heart failure. J Am Coll Cardiol 43(5):771–777
Kane GC, Karon BL, Mahoney DW et al (2011) Progression of left ventricular diastolic dysfunction and risk of heart failure. JAMA 306(8):856–863
Marwick TH, Ritchie R, Shaw JE et al (2018) Implications of underlying mechanisms for the recognition and management of diabetic cardiomyopathy. J Am Coll Cardiol 71(3):339–351
Debono M, Cachia E (2007) The impact of cardiovascular autonomic neuropathy in diabetes: is it associated with left ventricular dysfunction? Auton Neurosci 132(1–2):1–7
Morimoto A, Kadoya M, Kakutani-Hatayama M et al (2020) Subclinical decrease in cardiac autonomic and diastolic function in patients with metabolic disorders: HSCAA study. Metabol Open 5:100025
Dinh W, Füth R, Lankisch M et al (2011) Cardiovascular autonomic neuropathy contributes to left ventricular diastolic dysfunction in subjects with Type 2 diabetes and impaired glucose tolerance undergoing coronary angiography. Diabet Med 28(3):311–318
Callaghan BC, Cheng HT, Stables CL et al (2012) Diabetic neuropathy: clinical manifestations and current treatments. Lancet Neurol 11(6):521–534
Breiner A, Lovblom LE, Perkins BA et al (2014) Does the prevailing hypothesis that small-fiber dysfunction precedes large-fiber dysfunction apply to type 1 diabetic patients? Diabetes Care 37(5):1418–1424
Caselli A, Spallone V, Marfia GA et al (2006) Validation of the nerve axon reflex for the assessment of small nerve fibre dysfunction. J Neurol Neurosurg Psychiatry 77(8):927–932
Casellini CM, Parson HK, Richardson MS et al (2013) Sudoscan, a noninvasive tool for detecting diabetic small fiber neuropathy and autonomic dysfunction. Diabetes Technol Ther 15(11):948–953
Vinik AI, Nevoret ML, Casellini C (2015) The new age of sudomotor function testing: a sensitive and specific biomarker for diagnosis, estimation of severity, monitoring progression, and regression in response to intervention. Front Endocrinol (Lausanne) 6:94
Alberti KG, Zimmet PZ (1998) Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 15(7):539–553
Nagueh SF, Smiseth OA, Appleton CP et al (2016) Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging 17(12):1321–1360
Lang RM, Badano LP, Mor-Avi V et al (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging 16(3):233–270
Didangelos T, Kantartzis K (2020) Diabetes and heart failure: is it hyperglycemia or hyperinsulinemia? Curr Vasc Pharmacol 18(2):148–157
Levy DM, Terenghi G, Gu XH et al (1992) Immunohistochemical measurements of nerves and neuropeptides in diabetic skin: relationship to tests of neurological function. Diabetologia 35(9):889–897
Lee KA, Kim YJ, Park TS et al (2020) The association between cardiac autonomic neuropathy and heart function in type 2 diabetic patients. Somatosens Mot Res 37(3):149–156
Vinik AI, Ziegler D (2007) Diabetic cardiovascular autonomic neuropathy. Circulation 115:387–397
Spallone V, Bellavere F, Scionti L et al (2011) Recommendations for the use of cardiovascular tests in diagnosing diabetic autonomic neuropathy. Nutr Metab Cardiovasc Dis 21(1):69–78
Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability standards of measurement, physiological interpretation, and clinical use. Eur Heart J 17(3):354–381
Mao F, Liu S, Qiao X et al (2017) Sudoscan is an effective screening method for asymptomatic diabetic neuropathy in Chinese type 2 diabetes mellitus patients. J Diabetes Investig 8(3):363–368
Smith AG, Lessard M, Reyna S et al (2014) The diagnostic utility of Sudoscan for distal symmetric peripheral neuropathy. J Diabetes Complications 28(4):511–516
Dyck PJ, Overland CJ, Low PA et al (2010) Signs and symptoms versus nerve conduction studies to diagnose diabetic sensorimotor polyneuropathy: Cl vs. NPhys trial. Muscle Nerve 42(2):157–164
Nagueh SF (2020) Left ventricular diastolic function: understanding pathophysiology, diagnosis, and prognosis with echocardiography. JACC Cardiovasc Imaging 13(1 Pt 2):228–244
Paulus WJ, Tschöpe C (2013) A novel paradigm for heart failure with preserved ejection fraction: comorbidities drive myocardial dysfunction and remodeling through coronary microvascular endothelial inflammation. J Am Coll Cardiol 62(4):263–271
Dunlay SM, Roger VL, Redfield MM (2017) Epidemiology of heart failure with preserved ejection fraction. Nat Rev Cardiol 14(10):591–602
Khan MS, Samman Tahhan A, Vaduganathan M et al (2020) Trends in prevalence of comorbidities in heart failure clinical trials. Eur J Heart Fail 22(6):1032–1042
Adams KF Jr, Fonarow GC, Emerman CL et al (2005) Characteristics and outcomes of patients hospitalized for heart failure in the United States: rationale, design, and preliminary observations from the first 100,000 cases in the Acute Decompensated Heart Failure National Registry (ADHERE). Am Heart J 149(2):209–216
Yancy CW, Lopatin M, Stevenson LW et al (2006) Clinical presentation, management, and in-hospital outcomes of patients admitted with acute decompensated heart failure with preserved systolic function: a report from the Acute Decompensated Heart Failure National Registry (ADHERE) Database. J Am Coll Cardiol 47(1):76–84
Zhang X, Wei X, Liang Y et al (2013) Differential changes of left ventricular myocardial deformation in diabetic patients with controlled and uncontrolled blood glucose: a three-dimensional speckle-tracking echocardiography-based study. J Am Soc Echocardiogr 26(5):499–506
Ceyhan K, Kadi H, Koç F et al (2012) Longitudinal left ventricular function in normotensive prediabetics: a tissue Doppler and strain/strain rate echocardiography study. J Am Soc Echocardiogr 25(3):349–356
Heidenreich PA, Bozkurt B, Aguilar D et al (2022) 2022 AHA/ACC/HFSA guideline for the management of heart failure: a report of the American College of Cardiology/American Heart Association Joint Committee on clinical practice guidelines. J Am Coll Cardiol 79(17):e263–e421
El Sayed NA, Aleppo G, Aroda VR et al (2023) 12. Retinopathy, neuropathy, and foot care: standards of care in diabetes-2023. Diabetes Care 46(Suppl 1):S203–S215
Acknowledgements
We sincerely thank all of the participants involved in this study.
Funding
This study was supported by Natural Science Foundation of Guangdong Province (No. 2018A030313915) and Medical Scientific Research Foundation of Guangdong Province of China (No. A2018286) from YXB: identified the case, drafted the initial manuscript, and reviewed and revised the manuscript.
Author information
Authors and Affiliations
Contributions
XC, WX, XS, XH and JP contributed to the conception and design of the work, data analysis, interpretation of the data, and manuscript writing; HD, JZ and CW collected and analyzed data; JW, JY, BY, ZX, and WX searched and interpreted the data and critically revised the manuscript; and XY contributed to the conception and design of the work, acquisition and interpretation of the data, and critical revision of the manuscript. All authors approved the final version of the manuscript for publication and they agreed to be accountable for all aspects of the work. XY were the guarantors of this work, and as such, had full access to all the data in the study and took responsibility for the integrity of the data and the accuracy of the data analysis. All authors reviewed the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Ethics approval and consent to participate
This study was approved by the Ethics Committee of The Third Affiliated Hospital of Sun Yat-Sen University [02-107-01] and each subject provided written informed consent before participating in the study.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chen, X., Shui, X., Xu, H. et al. Sudomotor dysfunction is associated with impaired left ventricular diastolic function in persons with type 2 diabetes: a cross-sectional study. J Endocrinol Invest 47, 973–982 (2024). https://doi.org/10.1007/s40618-023-02214-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40618-023-02214-0