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Impaired Autonomic Function Is Associated With Increased Mortality, Especially in Subjects With Diabetes, Hypertension, or a History of Cardiovascular Disease
Open accessAbstract
OBJECTIVE: Measures of baroreflex sensitivity, heart rate variability (HRV), and the classical Ewing test parameters are currently used for the diagnosis of diabetic autonomic neuropathy and for mortality risk stratification after myocardial infarction. However, the strengths of the associations of these measures of autonomic function with risk of mortality have never been compared in one study population. Furthermore, no evidence is available on the possible effect of glucose tolerance on these associations. RESEARCH DESIGN AND METHODS: The study population (n = 605) consisted of a glucose tolerance-stratified sample from a general population (50-75 years of age). Cardiac cycle duration and continuous finger arterial pressure were measured under two conditions: at rest and on metronome breathing. From these readings, seven parameters of autonomic function were assessed (one Ewing, five HRV, and one baroreflex sensitivity). RESULTS: During 9 years of follow-up, 101 individuals died, 43 from cardiovascular causes. Subjects with diabetes and low levels of the autonomic function parameters, indicating impaired autonomic function, had an approximately doubled risk of mortality. This association was consistent, though not statistically significant, for all parameters. The elevated risk was not observed in subjects without diabetes, hypertension, or prevalent cardiovascular disease. CONCLUSIONS: Impaired autonomic function is associated with all-cause and cardiovascular mortality. Moreover, the results of the present study suggest that cardiac autonomic dysfunction in patients already at risk (diabetes, hypertension, or history of cardiovascular disease) may be especially hazardous.
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“Furthermore, despite HRV being linked with the severity of T2DM [23], no studies have comprehensively assessed the role of the most common variables, such as age [24], gender [25], blood glucose control [26], or medications treating for T2DM, on HRV parameters [27,28].”
From Heart rate variability in type 2 diabetes mellitus: A systematic review and meta–analysis (2018) · cites this paper as [23]
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BackgroundErnst, G., Watne, L. O., Frihagen, F., Wyller, T. B., Dominik, A., & Rostrup, M. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.640970 · Cited by 10
“Recent studies had a follow-up of 9 and 15 years (36, 45, 46), as opposed to our study of only 6 months follow-up.”
ResultMorphological evidence of reinnervation of the baroreceptive regions in sinoaortic‐denervated rats
Cai, G., Li, L., Xie, H., Xu, J., Miao, C., & Su, D. (2003) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2003.03938.x · Cited by 10
Kamińska, A., Tafil‐Klawe, M., Śmietanowski, M., Bronisz, A., Ruprecht, Z., Klawe, J. J., & Junik, R. (2008) · PubMed · Cited by 10
Metabolic Memory in the Autonomic Neuropathy of Diabetes
Chaturvedi, N. (2009) · Circulation · doi:10.1161/circulationaha.109.867036 · Cited by 10
Autonomic Nervous System Activity for Risk Stratification of Emergency Patients With Pneumonia
Mizera, L., Boehm, K., Duckheim, M., Groga‐Bada, P., Gawaz, M., Zuern, C. S., & Eick, C. (2018) · Journal of Emergency Medicine · doi:10.1016/j.jemermed.2018.06.016 · Cited by 9
Fu, Y.-J., Wang, W., Cai, G., Wang, M., & Su, D. (2005) · Autonomic Neuroscience · doi:10.1016/j.autneu.2005.11.001 · Cited by 9
“(Su et al., 1986; La Rovere et al., 1988; Sleight, 1997; Mortara et al., 1997; Gerritsen et al., 2001).”
Cardiovascular Autonomic Neuropathy in Patients with Type 2 Diabetes Mellitus
Ko, S., Kwon, H., Lee, J.-M., Kim, S.-R., Cho, J.-H., Yoo, K., Park, Y., Lee, W.-C., Song, K., Yoon, K., et al. (2006) · The Journal of Korean Diabetes Association · doi:10.4093/jkda.2006.30.3.226 · Cited by 9
Osailan, A., Metsios, G. S., Rouse, P. C., Ntoumanis, N., Duda, J. L., Kitas, G. D., & Zanten, J. V. (2016) · BMC Cardiovascular Disorders · doi:10.1186/s12872-016-0264-9 · Cited by 10
“Autonomic dysfunction, an increased activity of the sympathetic tone and less parasympathetic tone at rest [10], has been associated with increased risk of CVD [11] and all-cause mortality [12].”
Diabetes, Obesity and Atrial Fibrillation: Epidemiology, Mechanisms and Interventions.
Asghar, O., Alam, U., Hayat, S., Aghamohammadzadeh, R., Heagerty, A. M., & Malik, R. A. (2013) · Europe PMC (PubMed Central) · doi:10.4022/jafib.869 · Cited by 9
Rivas, E., Newmire, D. E., & Ben‐Ezra, V. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.08.026 · Cited by 9
Jung, C., Cho, Y. Y., Choi, D., Kim, B., Jung, S.-H., Kim, C., & Mok, J. (2024) · Scientific Reports · doi:10.1038/s41598-024-74390-9 · Cited by 9
Zhou, Z., Huang, Y., Zhuang, X., Guo, Y., Xie, P., Xiong, Z., Liu, M., Zhang, W., Zhong, J., Li, Y., et al. (2025) · Journal of the American Heart Association · doi:10.1161/jaha.124.034626 · Cited by 9
“30 Strong and consistent associations between multiple definitions of CAN and an increased risk of death have been shown in a meta-analysis.”
Atala, Y. B., de Matos, M. R., Corrêa‐Giannella, M. L., Parisi, M. C. R., Zantut‐Wittmann, D. E., Castillo, A. R., & Santos‐Bezerra, D. P. (2021) · Current Diabetes Reviews · doi:10.2174/1573399817666210827130339 · Cited by 8
Molina, E., Gould, N. F., Lee, K., Krimins, R. A., Hardenbergh, D., & Timlin, H. (2022) · Lupus · doi:10.1177/09612033221122980 · Cited by 8
“Decreased HRV has been associated with increased all-cause and cardiovascular mortality in diabetes, cardiovascular disease and essential hypertension.(101) Stress, although not in solidarity, has been implicated in development of each of these disorders.”
BackgroundPost-acute exercise cardiovagal modulation in older male adults with and without type 2 diabetes
Marôco, J. L., Arrais, I., Silvestre, T., Pinto, M., Laranjo, S. M., Magalhães, J. P., Clara, S., Fernhall, B., & Melo, X. (2023) · European Journal of Applied Physiology · doi:10.1007/s00421-023-05357-3 · Cited by 8
“…prospective cohort studies suggesting that the incidence of cardiac autonomic dysfunction increases with age and may contribute to the pathogenesis of T2DM, but also that T2DM may cause imbalances in cardiovagal modulation (Gerritsen et al. 2001; Carnethon et al. 2003; Almeida-Santos et al. 2016).”
BackgroundMenard, C. E., Durston, M., Zherebitskaya, E., Smith, D. R., Freed, D. H., Glazner, G. W., Tian, G., Fernyhough, P., & Arora, R. C. (2014) · Acta Neuropathologica Communications · doi:10.1186/2051-5960-2-60 · Cited by 10
“Additionally, diabetes has been used as a prognostic indicator in HF patients [11,12], with the five-year mortality rate in patients with diabetic autonomic neuropathy having been reported to be as high as 53%, versus 15% with normal autonomic function [13-16].”
BackgroundHeart rate variability – clinical significance
Urbanik, D., Podgórski, M., & Mazur, G. J. (2018) · Family Medicine & Primary Care Review · doi:10.5114/fmpcr.2018.73710 · Cited by 8
Balikai, F. A., Javali, S. B., Shindhe, V. M., Deshpande, N., Benni, J. M., Shetty, D. P., Kapoor, N., & Jaalam, K. (2022) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2022.109988 · Cited by 8
Chen, L. Y., Ye, X., Cheng, J. L., Xue, Y., Li, D., & Shao, J. (2022) · Medicine · doi:10.1097/md.0000000000030263 · Cited by 9
“[28] Moreover, the autonomic imbalance characteristic of the hyperactive sympathetic system and the hypoactive parasympathetic system was significantly correlated with cardiovascular disease in diabetic patients.[29] Studies have already demonstrated the reduced HRV could be regarded as early indicators of cardiac aut…”
BackgroundJelinek, H. F. (2004) · Cited by 8
Sympathetic and baroreflex abnormalities in the uncomplicated prediabetic state
Dell’Oro, R., Trevano, F. Q., Gamba, P., Ciuffarella, C., Seravalle, G., Mancia, G., & Grassi, G. M. (2018) · Journal of Hypertension · doi:10.1097/hjh.0000000000001659 · Cited by 8
Cardiovascular fitness and type 2 diabetes
Mullooly, C. (2002) · Current Diabetes Reports · doi:10.1007/s11892-002-0109-z · Cited by 8
Nylén, E. (2024) · Reviews in Cardiovascular Medicine · doi:10.31083/j.rcm2507263 · Cited by 7
“More advanced DM2 is frequently associated with neuropathy and a serious facet involve cardiac autonomic dysfunction which worsens with age which is evident both at rest and following exercise [21].”
BackgroundYang, S., Liao, X., Lin, Y., Chen, J.-J., & Wu, H. (2024) · Journal of Applied Biomedicine · doi:10.1016/j.bbe.2024.08.002 · Cited by 7
Autonomic Nervous System and Neurocardiac Physiopathology
Kingma, J. G., Simard, D., & Rouleau, J. R. (2018) · InTech eBooks · doi:10.5772/intechopen.77087 · Cited by 8
“New findings support the concept that disorders within the ANS contribute to pathogenesis of organ injury, co-morbidities [203, 204] and even survival.”
BackgroundCardiac Noradrenergic Denervation in a Patient with Multiple Symmetric Lipomatosis
Fonseca, V. R., Freitas, C., Palmeira, M., Ferreira, C., & Victorino, R. M. M. (2012) · Cardiology · doi:10.1159/000336951 · Cited by 7
Badea, A. R., Nedelcu, L. D., Văleanu, M., & Zdrenghea, D. T. (2014) · Medicine and Pharmacy Reports · doi:10.15386/cjmed-313 · Cited by 7
“function were negatively associated with fasting glucose, insulin resistance and all components of the metabolic syndrome [3,5].”
BackgroundWagner, J. A., Feinn, R., Lampert, R. J., Bermúdez‐Millán, A., & Pérez‐Escamilla, R. (2019) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2019.109774 · Cited by 7
Perring, S., & Jones, E. L. (2003) · Physiological Measurement · doi:10.1088/0967-3334/24/3/310 · Cited by 7
“The Hoorn Study has shown that reduced autonomic function is associated with increased mortality, particularly when associated with other conditions (Gerritsen et al 2001).”
Background
Metadata
- Authors
- Gerritsen, J., Dekker, J. M., TenVoorde, B. J., Kostense, P. J., Heine, R. J., Bouter, L. M., Heethaar, R. M., & Stehouwer, C. D. A.
- Affiliations
- Vrije Universiteit Amsterdam (NL)
- Department of Epidemiology and Biostatistics, Vrije Universiteit, Amsterdam, the Netherlands
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2001-10-01
- Volume
- 24
- Issue
- 10
- Pages
- 1793-1798
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- OpenAlex
- W2141929799
- Cited by
- 456
- References
- 27
- Citations by year
- 2026: 10 · 2025: 8 · 2024: 14 · 2023: 15 · 2022: 14 · 2021: 20 · 2020: 17 · 2019: 17 · 2018: 17 · 2017: 17 · 2016: 22 · 2015: 24 · 2014: 21 · 2013: 32 · 2012: 29
- FWCI
- 10.29
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Diabetes Care (publishedVersion)
- PubMed (publishedVersion)
- VU Research Portal (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Diabetes Fonds
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Syncope and Autonomic Disorders
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Function and Risk Factors
- Keywords
- cardiovascular mortality, all-cause mortality, diabetic autonomic neuropathy, heart rate variability, baroreflex sensitivity, Ewing test, cardiac autonomic dysfunction, diabetes mellitus, hypertension, cardiovascular disease, glucose tolerance, risk stratification
- MeSH terms
- Aged, Autonomic Nervous System Diseases, Cardiovascular Diseases, Female, Heart Rate, Humans, Hypertension, Male, Middle Aged, Respiration, Risk Factors, Supination, Baroreflex, Diabetes Complications
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