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Sudomotor dysfunction is associated with impaired left ventricular diastolic function in persons with type 2 diabetes: a cross-sectional study

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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.

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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

  1. 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

    Article  CAS  PubMed  Google Scholar 

  2. 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

    Article  PubMed  Google Scholar 

  3. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. 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

    Article  PubMed  Google Scholar 

  6. 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

    Article  PubMed  PubMed Central  Google Scholar 

  7. 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

    Article  CAS  PubMed  Google Scholar 

  8. Callaghan BC, Cheng HT, Stables CL et al (2012) Diabetic neuropathy: clinical manifestations and current treatments. Lancet Neurol 11(6):521–534

    Article  PubMed  PubMed Central  Google Scholar 

  9. 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

    Article  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. 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

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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

    Article  PubMed  Google Scholar 

  13. 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

    Article  CAS  PubMed  Google Scholar 

  14. 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

    Article  PubMed  Google Scholar 

  15. 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

    Article  PubMed  Google Scholar 

  16. Didangelos T, Kantartzis K (2020) Diabetes and heart failure: is it hyperglycemia or hyperinsulinemia? Curr Vasc Pharmacol 18(2):148–157

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  PubMed  Google Scholar 

  19. Vinik AI, Ziegler D (2007) Diabetic cardiovascular autonomic neuropathy. Circulation 115:387–397

    Article  PubMed  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. 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

    Article  Google Scholar 

  22. 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

    Article  CAS  PubMed  Google Scholar 

  23. 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

    Article  PubMed  PubMed Central  Google Scholar 

  24. 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

    Article  PubMed  Google Scholar 

  25. Nagueh SF (2020) Left ventricular diastolic function: understanding pathophysiology, diagnosis, and prognosis with echocardiography. JACC Cardiovasc Imaging 13(1 Pt 2):228–244

    Article  PubMed  Google Scholar 

  26. 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

    Article  PubMed  Google Scholar 

  27. Dunlay SM, Roger VL, Redfield MM (2017) Epidemiology of heart failure with preserved ejection fraction. Nat Rev Cardiol 14(10):591–602

    Article  PubMed  Google Scholar 

  28. 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

    Article  PubMed  Google Scholar 

  29. 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

    Article  PubMed  Google Scholar 

  30. 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

    Article  PubMed  Google Scholar 

  31. 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

    Article  CAS  PubMed  Google Scholar 

  32. 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

    Article  PubMed  Google Scholar 

  33. 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

    Article  PubMed  Google Scholar 

  34. 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

    Google Scholar 

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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.

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Authors and Affiliations

Authors

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

Correspondence to Z. Xiong, W. Xu or X. Yang.

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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.

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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

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