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Cardiovascular autonomic responses during head-up tilt test in newly diagnosed type 2 diabetes

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Abstract

Background

Autonomic dysfunction is commonly observed in patients with long-standing type 2 diabetes. Previous studies have confirmed the value of both subjectively assessed symptoms and objective measurements of autonomic nervous system function in diagnosing cardiovascular autonomic neuropathy. However, the head-up tilt test (HUTT) has been rarely used to investigate cardiovascular autonomic responses in subjects with high risk of newly diagnosed type 2 diabetes (nT2D).

Objective

To evaluate autonomic cardiovascular responses through passive orthostatic challenge along the diabetes continuum.

Methods

The study population was stratified as normoglycemic (n = 16), prediabetes (n = 20), and nT2D (n = 20). The prevalence of orthostatic intolerance and autonomic cardiovascular responses was evaluated with the Task Force Monitor during a 30-min passive HUTT. Spectral indices of heart rate and blood pressure variability and baroreceptor effectiveness index (BEI) were calculated through the HUTT. BEI was obtained by the sequence method.

Results

There were no differences in the prevalence of orthostatic intolerance or in the indices of heart rate and blood pressure variability among the three groups of study. The BEI was attenuated in the nT2D group in supine rest and throughout HUTT compared with normoglycemic and prediabetes groups. The multivariable linear regression analysis showed that BEI was associated with fasting glucose (β =  − 0.52, p  < 0.001) and HbA1c (β =  − 0.57, p  < 0.001) independently of cardiovascular risk factors.

Conclusion

Cardiovascular autonomic neuropathy, expressed as blunted BEI, is the only abnormal autonomic nervous test detected in nT2D, and it was independently associated with fasting glucose and HbA1c values.

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Change history

  • 13 November 2021

    The tagging of author name has been corrected.

References

  1. Khan MAB, Hashim MJ, King JK et al (2020) Epidemiology of type 2 diabetes – Global Burden of Disease and Forecasted Trends. J Epidemiol Glob Health 10:107–111. https://doi.org/10.2991/jegh.k.191028.001

    Article  PubMed  PubMed Central  Google Scholar 

  2. American Diabetes Association (2018) Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2018. Diabetes Care 41:S13–S27. https://doi.org/10.2337/dc18-S002

    Article  Google Scholar 

  3. Spallone V (2019) Update on the impact, diagnosis and management of cardiovascular autonomic neuropathy in diabetes: what is defined, what is new, and what is unmet. Diabetes Metab J 43:3–30

    Article  Google Scholar 

  4. Vinik AI, Erbas T, Casellini CM (2013) Diabetic cardiac autonomic neuropathy, inflammation and cardiovascular disease. J Diabetes Investig 4:4–18. https://doi.org/10.1111/jdi.12042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Yagihashi S, Yamagishi S-I, Wada R (2007) Pathology and pathogenetic mechanisms of diabetic neuropathy: correlation with clinical signs and symptoms. Diabetes Res Clin Pract 77(Suppl 1):S184-189. https://doi.org/10.1016/j.diabres.2007.01.054

    Article  CAS  PubMed  Google Scholar 

  6. Maser RE, Mitchell BD, Vinik AI, Freeman R (2003) The association between cardiovascular autonomic neuropathy and mortality in individuals with diabetes: a meta-analysis. Diabetes Care 26:1895–1901. https://doi.org/10.2337/diacare.26.6.1895

    Article  PubMed  Google Scholar 

  7. Spallone V, Ziegler D, Freeman R et al (2011) Cardiovascular autonomic neuropathy in diabetes: clinical impact, assessment, diagnosis, and management. Diabetes Metab Res Rev 27:639–653. https://doi.org/10.1002/dmrr.1239

    Article  PubMed  Google Scholar 

  8. Pop-Busui R (2010) Cardiac autonomic neuropathy in diabetes: a clinical perspective. Diabetes Care 33:434–441. https://doi.org/10.2337/dc09-1294

    Article  PubMed  PubMed Central  Google Scholar 

  9. González-Hermosillo A, Sierra-Beltrán M, López-Peña U et al (2018) Cardiovascular and cerebral hemodynamics in asymptomatic healthy subjects with/without abnormal head-up tilt test versus recurrent fainters. J Clin Neurophysiol 35:77–83. https://doi.org/10.1097/WNP.0000000000000430

    Article  PubMed  Google Scholar 

  10. Parry SW, Norton M, Pairman J et al (2009) Impedance cardiography: a role in vasovagal syncope diagnosis? Age Ageing 38:718–723. https://doi.org/10.1093/ageing/afp167

    Article  PubMed  Google Scholar 

  11. Gerritsen J, Dekker JM, TenVoorde BJ et al (2000) Glucose tolerance and other determinants of cardiovascular autonomic function: the Hoorn Study. Diabetologia 43:561–570. https://doi.org/10.1007/s001250051344

    Article  CAS  PubMed  Google Scholar 

  12. Wu J-S, Yang Y-C, Lin T-S et al (2007) Epidemiological evidence of altered cardiac autonomic function in subjects with impaired glucose tolerance but not isolated impaired fasting glucose. J Clin Endocrinol Metab 92:3885–3889. https://doi.org/10.1210/jc.2006-2175

    Article  CAS  PubMed  Google Scholar 

  13. Wu J-S, Lu F-H, Yang Y-C et al (2014) Impaired baroreflex sensitivity in subjects with impaired glucose tolerance, but not isolated impaired fasting glucose. Acta Diabetol 51:535–541. https://doi.org/10.1007/s00592-013-0548-9

    Article  CAS  PubMed  Google Scholar 

  14. Wang S, Randall DC, Knapp CF et al (2012) Blood pressure regulation in diabetic patients with and without peripheral neuropathy. Am J Physiol Regul Integr Comp Physiol 302:R541-550. https://doi.org/10.1152/ajpregu.00174.2011

    Article  CAS  PubMed  Google Scholar 

  15. de Moura-Tonello SCG, Porta A, Marchi A et al (2017) Correction: cardiovascular variability analysis and baroreflex estimation in patients with type 2 diabetes in absence of any manifest neuropathy. PLoS ONE 12:e0174492. https://doi.org/10.1371/journal.pone.0174492

    Article  PubMed  PubMed Central  Google Scholar 

  16. Michel-Chávez A, Estañol B, Gien-López JA et al (2015) Heart rate and systolic blood pressure variability on recently diagnosed diabetics. Arq Bras Cardiol 105:276–284. https://doi.org/10.5935/abc.20150073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Jorge-Galarza E, Medina-Urrutia A, Posadas-Sánchez R et al (2016) Adipose tissue dysfunction increases fatty liver association with pre diabetes and newly diagnosed type 2 diabetes mellitus. Diabetol Metab Syndr 8:73. https://doi.org/10.1186/s13098-016-0189-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Baecke JA, Burema J, Frijters JE (1982) A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr 36:936–942

    Article  CAS  Google Scholar 

  19. DeLong DM, DeLong ER, Wood PD et al (1986) A comparison of methods for the estimation of plasma low- and very low-density lipoprotein cholesterol. The Lipid Research Clinics Prevalence Study. JAMA 256:2372–2377

    Article  CAS  Google Scholar 

  20. Levey AS, Stevens LA, Schmid CH et al (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150:604–612. https://doi.org/10.7326/0003-4819-150-9-200905050-00006

    Article  PubMed  PubMed Central  Google Scholar 

  21. Malik M, Bigger JT, Camm AJ et al (1996) Heart rate variability standards of measurement, physiological interpretation, and clinical use. Eur Heart J 17:354–381. https://doi.org/10.1093/oxfordjournals.eurheartj.a014868

    Article  Google Scholar 

  22. Bianchi AM, Mainardi LT, Meloni C et al (1997) Continuous monitoring of the sympatho-vagal balance through spectral analysis. IEEE Eng Med Biol Mag 16:64–73. https://doi.org/10.1109/51.620497

    Article  CAS  PubMed  Google Scholar 

  23. Iellamo F, Legramante JM, Pigozzi F et al (2002) Conversion from vagal to sympathetic predominance with strenuous training in high-performance world class athletes. Circulation 105:2719–2724. https://doi.org/10.1161/01.cir.0000018124.01299.ae

    Article  PubMed  Google Scholar 

  24. Malliani A, Pagani M, Lombardi F, Cerutti S (1991) Cardiovascular neural regulation explored in the frequency domain. Circulation 84:482–492. https://doi.org/10.1161/01.cir.84.2.482

    Article  CAS  PubMed  Google Scholar 

  25. Watso JC, Babcock MC, Migdal KU, Robinson AT (2017) The baroreflex effectiveness index as an early marker of autonomic dysfunction in heart failure. J Physiol (Lond) 595:5013–5014. https://doi.org/10.1113/JP274664

    Article  CAS  Google Scholar 

  26. Di Rienzo M, Parati G, Castiglioni P et al (2001) Baroreflex effectiveness index: an additional measure of baroreflex control of heart rate in daily life. Am J Physiol Regul Integr Comp Physiol 280:R744-751. https://doi.org/10.1152/ajpregu.2001.280.3.R744

    Article  PubMed  Google Scholar 

  27. Laitinen T, Vauhkonen IK, Niskanen LK et al (1999) Power spectral analysis of heart rate variability during hyperinsulinemia in nondiabetic offspring of type 2 diabetic patients: evidence for possible early autonomic dysfunction in insulin-resistant subjects. Diabetes 48:1295–1299. https://doi.org/10.2337/diabetes.48.6.1295

    Article  CAS  PubMed  Google Scholar 

  28. Carnethon MR, Jacobs DR, Sidney S et al (2003) Influence of autonomic nervous system dysfunction on the development of type 2 diabetes: the CARDIA study. Diabetes Care 26:3035–3041. https://doi.org/10.2337/diacare.26.11.3035

    Article  PubMed  Google Scholar 

  29. Abdul-Ghani MA, Tripathy D, DeFronzo RA (2006) Contributions of beta-cell dysfunction and insulin resistance to the pathogenesis of impaired glucose tolerance and impaired fasting glucose. Diabetes Care 29:1130–1139. https://doi.org/10.2337/diacare.2951130

    Article  CAS  PubMed  Google Scholar 

  30. Schumer MP, Joyner SA, Pfeifer MA. (1998) Cardiovascular autonomic neuropathy testing in patients with diabetes. Diabetes Spectr 11:223–227

    Google Scholar 

  31. Ziegler D, Dannehl K, Volksw D et al (1992) Prevalence of cardiovascular autonomic dysfunction assessed by spectral analysis and standard tests of heart-rate variation in newly diagnosed IDDM patients. Diabetes Care 15:908–911. https://doi.org/10.2337/diacare.15.7.908

    Article  CAS  PubMed  Google Scholar 

  32. Dimova R, Tankova T, Kirilov G et al (2020) Endothelial and autonomic dysfunction at early stages of glucose intolerance and in metabolic syndrome. Horm Metab Res 52:39–48. https://doi.org/10.1055/a-0972-1302

    Article  CAS  PubMed  Google Scholar 

  33. Hong L-Z, Hsieh P-S (2007) Hyperinsulinemia instead of insulin resistance induces baroreflex dysfunction in chronic insulin-infused rats. Am J Hypertens 20:451–458. https://doi.org/10.1016/j.amjhyper.2006.11.004

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was partially supported by Instituto Nacional de Cardiología Ignacio Chávez (Project No 16-977). We thank Betty Lou Chinn R.N. for grammatical review.

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Authors and Affiliations

  1. Endocrinology Department, National Institute of Cardiology “Ignacio Chávez”, Mexico City, Mexico

    Esteban Jorge-Galarza, Margarita Torres-Tamayo, María del Rocío Martínez-Alvarado, Berenice Peña-Aparicio, Carmen González-Salazar & Juan Reyes-Barrera

  2. Dysautonomic Clinic, National Institute of Cardiology “Ignacio Chávez”, Mexico City, Mexico

    Manuel Sierra-Beltrán, Erika Fajardo-Flores, Andrey Kostin & J. Antonio González-Hermosillo

  3. Mexico City, Mexico

    J. Antonio González-Hermosillo

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  1. Esteban Jorge-Galarza
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  2. Margarita Torres-Tamayo
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  5. Carmen González-Salazar
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Contributions

J.A.G.H., M.S.B., and M.T.T. conceptualization and methodology. J.A.G.H., M.T.T., and E.J.G researched data, contributed to discussion, wrote the manuscript, and provided critical review and revision. M.T.T., M.R.A. M., B.P.A., J.R.B., M.C.G.S., E.F.F., and A.K. researched the data, provided critical review, and contributed to the discussion. E.J.G and J.A.G.H are the guarantors of this work and, as such, had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Corresponding author

Correspondence to J. Antonio González-Hermosillo.

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The protocol was approved by the Ethics and Research Committees of the National Institute of Cardiology, based on the Declaration of Helsinki

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All subjects gave their informed consent to participate in this study.

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The authors declare no competing interests.

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Jorge-Galarza, E., Torres-Tamayo, M., Martínez-Alvarado, M. et al. Cardiovascular autonomic responses during head-up tilt test in newly diagnosed type 2 diabetes. Ir J Med Sci 191, 2077–2084 (2022). https://doi.org/10.1007/s11845-021-02825-7

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  • DOI: https://doi.org/10.1007/s11845-021-02825-7

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