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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HRV is linked with the severity of T2DM.
“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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“Indeed, impaired BRS has been found to be associated with high cardiovascular mortality risk in hypertensive patients [103].”
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Pal, G. K., Pal, P., Nanda, N., Amudharaj, D., & Adithan, C. (2012) · Future Cardiology · doi:10.2217/fca.12.80 · Cited by 84 · see citing works
Detection of Silent Myocardial Ischemia in Asymptomatic Diabetic Subjects
Wackers, F. J. T., Young, L. H., Inzucchi, S. E., Chyun, D. A., & for the DIAD Investigators (2005) · Diabetes Care · doi:10.2337/diacare.28.1.232 · Cited by 84 · see citing works
Cardiac Autonomic Neuropathy: Why Should Cardiologists Care about That?
Bissinger, A. (2017) · Journal of Diabetes Research · doi:10.1155/2017/5374176 · Cited by 86 · see citing works
“Studies on patients with DM have concluded that an impaired BRR is a strong independent risk factor for mortality [54].”
BackgroundGUIDELINES ON DIABETES, PRE-DIABETES, AND CARDIOVASCULAR DISEASES
Rydén, L., Standl, E., Bartnik, M., den Berghe, G. V., Betteridge, J. D., de Boer, M. J., Cosentino, F., Jönsson, B., Laakso, M., Malmberg, K., et al. (2007) · Rational Pharmacotherapy in Cardiology · doi:10.20996/1819-6446-2007-3-4-71-99 · Cited by 81 · see citing works
“Subjects with diabetes and low levels of autonomic function parameters (baroreflex sensitivity, heart rate variability, and classical Ewing tests) had an approximately doubled risk of mortality in the Hoorn Study.(262) In the Detection of Ischaemia in Asymptomatic Diabetics Study,(263) cardiac autonomic dysfunction, a…”
BackgroundNonlinear Methods to Assess Changes in Heart Rate Variability in Type 2 Diabetic Patients
Roy, B., & Ghatak, S. K. (2013) · Arquivos Brasileiros de Cardiologia · doi:10.5935/abc.20130181 · Cited by 82 · see citing works
Air Pollution and Cardiovascular Disease in the Multi-Ethnic Study of Atherosclerosis
Gill, E. A., Curl, C. L., Adar, S. D., Allen, R. W., Auchincloss, A. H., O’Neill, M. S., Park, S. K., Hee, V. C. V., Roux, A. V. D., & Kaufman, J. D. (2011) · Progress in Cardiovascular Diseases · doi:10.1016/j.pcad.2011.02.001 · Cited by 82 · see citing works
Air Pollution and Heart Rate Variability
Park, S. K., O’Neill, M. S., Vokonas, P., Sparrow, D., Wright, R. O., Coull, B. A., Nie, H., Hu, H., & Schwartz, J. D. (2008) · Epidemiology · doi:10.1097/ede.0b013e31815c408a · Cited by 81 · see citing works
Vascular dysfunction and autonomic neuropathy in Type 2 diabetes
Meyer, C., Milat, F., McGrath, B. P., Cameron, J. D., Kotsopoulos, D., & Teede, H. J. (2004) · Diabetic Medicine · doi:10.1111/j.1464-5491.2004.01241.x · Cited by 79 · see citing works
Liu, W., Ma, C., Liu, I.-J., Han, B., Chuang, H., & Chuang, K.-J. (2015) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2015.01.003 · Cited by 80 · see citing works
Saito, I., Hitsumoto, S., Maruyama, K., Nishida, W., Eguchi, E., Kato, T., Kawamura, R., Takata, Y., Onuma, H., Osawa, H., et al. (2015) · Journal of Epidemiology · doi:10.2188/jea.je20140254 · Cited by 77 · see citing works
Hallman, D., Jørgensen, M. B., & Holtermann, A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177042 · Cited by 80 · see citing works
Boer‐Martins, L., Figueiredo, V. N., Demacq, C., Martins, L. C., Consolim‐Colombo, F. M., Figueiredo, M. J. D. O., Cannavan, F. P. D. S., & Moreno, H. (2011) · Cardiovascular Diabetology · doi:10.1186/1475-2840-10-24 · Cited by 76 · see citing works
“Therefore, autonomic imbalance may be a final common pathway to increased morbidity and mortality from a host of conditions and diseases, including cardiovascular disease [4,5].”
BackgroundGuo, Q., Zang, P., Xu, S.-Y., Song, W., Zhang, Z., Liu, C., Guo, Z., Chen, J., Lu, B., Gu, P., et al. (2020) · Journal of Diabetes Research · doi:10.1155/2020/5817074 · Cited by 75 · see citing works
“Cardiovascular autonomic neuropathy (CAN) is one of the most shared complications of diabetes, with autonomic imbalance including sympathetic system hyperactivity and parasympathetic system hypoactivity [5].”
BackgroundHeart rate variability response to mental arithmetic stress in patients with schizophrenia
Castro, M. N., Vigo, D. E., Weidema, H., Fahrer, R. D., Chu, E. M.-Y., de Achával, D., Nogués, M. A., Leiguarda, R. C., Cardinali, D. P., & Guinjoan, S. M. (2007) · Schizophrenia Research · doi:10.1016/j.schres.2007.08.025 · Cited by 73 · see citing works
“…parasympathetic input to the heart have been repeatedly shown to increase the proclivity to malignant ventricular arrhythmias and myocardial ischaemia (Schwartz and Priori, 1990; Smith et al., 2005), ultimately resulting in increased incidence of cardiovascular deaths (Gerritsen et al., 2001).”
Ayad, F., Belhadj, M., Pariès, J., Attali, J. R., & Valensi, P. E. (2010) · Diabetic Medicine · doi:10.1111/j.1464-5491.2010.03027.x · Cited by 72 · see citing works
Fadul, N. A., Strasser, F., Palmer, J. L., Yusuf, S. W., Guo, Y., Li, Z., Allo, J. A., & Bruera, E. D. (2010) · Journal of Pain and Symptom Management · doi:10.1016/j.jpainsymman.2009.06.014 · Cited by 72 · see citing works
Min, K., Min, J., Paek, D., & Cho, S. (2008) · Pacing and Clinical Electrophysiology · doi:10.1111/j.1540-8159.2008.01045.x · Cited by 72 · see citing works
Authors Task Force Members, Rydén, L., Standl, E., Bartnik, M., den Berghe, G. V., Betteridge, J. D., de Boer, M., Cosentino, F., Jönsson, B., Laakso, M., et al. (2007) · European Heart Journal Supplements · doi:10.1093/eurheartj/ehl261 · Cited by 73 · see citing works
Impact of bariatric surgery–induced weight loss on heart rate variability
Nault, I., Nadreau, É., Paquet, C., Brassard, P., Marceau, P., Marceau, S., Biron, S., Hould, F. S., Lebel, S., Richard, D., et al. (2007) · Metabolism · doi:10.1016/j.metabol.2007.06.006 · Cited by 70 · see citing works
Chemla, D., Young, J., Badilini, F., Maison‐Blanche, P., Affres, H., Lecarpentier, Y., & Chanson, P. (2005) · International Journal of Cardiology · doi:10.1016/j.ijcard.2004.12.018 · Cited by 70 · see citing works
“It has been suggested that patients with decreased HRV may have a higher reproducibility of spectral indices than healthy subjects [18,29,33] although conflicting results have been published in diabetic subjects [9,17,30].”
ResultKenig, A., & Ilan, Y. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01542 · Cited by 68 · see citing works
“Endotoxin challenge was described to induce hyporesponsiveness of spontaneously beating atria to cholinergic stimulation but not in chronotropic response to chronotropic adrenergic stimulation (Gholami et al., 2012).”
BackgroundCrews, D. C., McClellan, W. M., Shoham, D. A., Gao, L., Warnock, D. G., Judd, S. E., Muntner, P., Miller, E. R., & Powe, N. R. (2012) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2012.05.010 · Cited by 68 · see citing works
“For example, low social class has been independently associated with little variation in heart rate [low heart rate variability (HRV)] 33, 34 ; and low HRV has been associated with hypertension 35 , diabetes 36 , incident cardiovascular disease 35 , progression to ESRD 37 and death 38 .”
Diabetic Autonomic Imbalance and Glycemic Variability
Fleischer, J. (2012) · Journal of Diabetes Science and Technology · doi:10.1177/193229681200600526 · Cited by 69 · see citing works
Autonomic Nerve Testing Predicts the Development of Complications
Maguire, A., Craig, M. E., Craighead, A., Chan, A. K. F., Cusumano, J. M., Hing, S. J., Silink, M., Howard, N. J., & Donaghue, K. C. (2006) · Diabetes Care · doi:10.2337/dc06-0793 · Cited by 67 · see citing works
Aldosterone Function in Diabetes Mellitus: Effects on Cardiovascular and Renal Disease
McFarlane, S. I., & Sowers, J. R. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021443 · Cited by 67 · see citing works
Diabetes mellitus and sudden cardiac death: what are the data?
Bergner, D. W., & Goldberger, J. J. (2010) · PubMed · Cited by 66 · see citing works
Heart rate variability is associated with psychosocial stress in distinct social domains
Lischke, A., Jacksteit, R., Mau‐Moeller, A., Pahnke, R., Hamm, A. O., & Weippert, M. (2018) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2018.01.005 · Cited by 67 · see citing works
“, [40,41]] or major depressive disorder [e.”
Lykke, J. A., Tarnow, L., Parving, H. ‐., & Hilsted, J. (2008) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.1080/00365510802018330 · Cited by 65 · see citing works
Logtenberg, S. J. J., Kleefstra, N., Houweling, S. T., Groenier, K. H., & Bilo, H. J. G. (2006) · Journal of Hypertension · doi:10.1097/hjh.0b013e32801040d5 · Cited by 63 · see citing works
“For example, reduced baroreflex sensitivity (BRS) is an indicator of increased risk for mortality and morbidity and is associated independently with both diabetes mellitus and hypertension [24,25].”
BackgroundMoran, A. E., Palmas, W., Field, L., Bhattarai, J., Schwartz, J. E., Weinstock, R. S., & Shea, S. (2004) · Diabetes Care · doi:10.2337/diacare.27.4.972 · Cited by 63 · see citing works
“Approximately 65% of people with diabetes die of cardiovascular disease (4), and cardiovascular disease is the leading cause of death among patients with type 2 diabetes who are diagnosed with cardiovascular autonomic neuropathy (3,5).”
BackgroundSpontaneous baroreflex sensitivity in (pre)adolescents
Dietrich, A., Riese, H., van Roon, A. M., van Engelen, K., Ormel, J., Neeleman, J., & Rosmalen, J. G. M. (2006) · Journal of Hypertension · doi:10.1097/01.hjh.0000200517.27356.47 · Cited by 62 · see citing works
Mohammed, J., Meeus, M., Derom, E., Silva, H. D., & Calders, P. (2015) · Respiratory Care · doi:10.4187/respcare.04174 · Cited by 62 · see citing works
Acupuncture and Heart Rate Variability: A Systems Level Approach to Understanding Mechanism
Anderson, B. J., Nielsen, A., McKee, D., Jeffres, A., & Kligler, B. (2012) · EXPLORE · doi:10.1016/j.explore.2011.12.002 · Cited by 61 · see citing works
Gerson, M. C., Caldwell, J. H., Ananthasubramaniam, K., Clements, I. P., Henzlova, M. J., Amanullah, A. M., & Jacobson, A. F. (2010) · Circulation Cardiovascular Imaging · doi:10.1161/circimaging.110.954784 · Cited by 61 · see citing works
Carandina, A., Rodrigues, G. D., Francesco, P. D., Filtz, A., Bellocchi, C., Furlan, L., Carugo, S., Montano, N., & Tobaldini, E. (2021) · Autonomic Neuroscience · doi:10.1016/j.autneu.2021.102893 · Cited by 61 · see citing works
Wang, W.-Z., Gao, L., Pan, Y.-X., Zucker, I. H., & Wang, W. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00590.2006 · Cited by 59 · see citing works
“Impairment of baroreflex function has been shown to be associated with progression of several diseases and a poor prognosis (10, 14, 23).”
BackgroundDiabetic cardiovascular autonomic neuropathy: clinical implications
Karayannis, G., Giamouzis, G., Cokkinos, D. V., Skoularigis, J. S., & Triposkiadis, F. K. (2012) · Expert Review of Cardiovascular Therapy · doi:10.1586/erc.12.53 · Cited by 58 · see citing works
Risk factors for autonomic and somatic nerve dysfunction in different stages of glucose tolerance
Dimova, R. B., Tankova, T. I., Guergueltcheva, V., Tournev, I., Chakarova, N. Y., Grozeva, G. G., & Dakovska, L. N. (2016) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2016.11.002 · Cited by 59 · see citing works
“It has been shown that lipid profile parameters are not independently related to autonomic tone, supported by Gerritsen et al. (2001) and Meyer et al. (2004) findings.”
ResultTheurl, F., Schreinlechner, M., Sappler, N., Toifl, M., Dolejsi, T., Hofer, F., Massmann, C., Steinbring, C., Komarek, S., Moelgg, K., et al. (2023) · European Heart Journal - Digital Health · doi:10.1093/ehjdh/ztad022 · Cited by 57 · see citing works
Wagner, J. A., Lampert, R. J., Tennen, H. A., & Feinn, R. (2013) · Stress and Health · doi:10.1002/smi.2542 · Cited by 59 · see citing works
Hazari, M. S., Haykal-Coates, N., Winsett, D. W., Costa, D. L., & Farraj, A. K. (2009) · Toxicological Sciences · doi:10.1093/toxsci/kfp214 · Cited by 56 · see citing works
“Thus, it may be likely that SH rats are more sensitive to the arrhythmogenic effects of aconitine than WKY rats because of inherent depressed BRS, which is known to be impaired in hypertensive states (Gerritsen et al., 2001; Mortara et al., 1997; Struyker-Boudier et al., 1982).”
BackgroundMadden, K. M., Lockhart, C., Potter, T. F., & Cuff, D. (2010) · Clinical Journal of Sport Medicine · doi:10.1097/jsm.0b013e3181ea8454 · Cited by 61 · see citing works
“In fact, lowered BRS was found to double mortality in patients who had other cardiovascular risk factors, such as diabetes or hypertension.(2) One potential therapy for low BRS is aerobic training.”
BackgroundResultInfluentialKenig, A., Kolben, Y., Asleh, R., Amir, O., & Ilan, Y. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.695547 · Cited by 53 · see citing works
“HRV alteration is associated with numerous disease states and correlates with cardiovascular and all-cause mortality, mainly in patients with established cardiovascular disease (79).”
BackgroundPoon, A. K., Whitsel, E. A., HEISS, G. M., Soliman, E. Z., Wagenknecht, L. E., Suzuki, T., & Loehr, L. R. (2020) · BMC Cardiovascular Disorders · doi:10.1186/s12872-020-01496-z · Cited by 53 · see citing works
Sympathetic and Parasympathetic Neuropathy Are Frequent in Both Type 1 and Type 2 Diabetic Patients
Freccero, C., Svensson, H., Bornmyr, S., Wollmer, P., & Sundkvist, G. (2004) · Diabetes Care · doi:10.2337/diacare.27.12.2936 · Cited by 53 · see citing works
Borchini, R., Veronesi, G., Bonzini, M., Gianfagna, F., Dashi, O., & Ferrario, M. (2018) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph15010113 · Cited by 53 · see citing works
Cardiovascular autonomic neuropathy: A silent killer with long reach
Ang, L., Dillon, B., Mizokami-Stout, K., & Pop-Busui, R. (2020) · Autonomic Neuroscience · doi:10.1016/j.autneu.2020.102646 · Cited by 53 · see citing works
- 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 › Surgery › 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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