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Dysregulation of the Autonomic Nervous System Predicts the Development of the Metabolic Syndrome

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Dysregulation of the Autonomic Nervous System Predicts the Development of the Metabolic Syndrome ORIGINAL ARTICLE Endocrine Research Dysregulation of the Autonomic Nervous System Predicts the Development of the Metabolic Syndrome Carmilla M. M. Licht, Eco J. C. de Geus, and Brenda W. J. H. Penninx Department of Psychiatry (C.M.M.L., B.W.J.H.P.), Vrije Universiteit (VU) University Medical Center Amsterdam, The Netherlands; Extramural Medicine Researchϩ Institute (C.M.M.L., E.J.C.d.G., B.W.J.H.P.) for Health and Care Research, VU University Medical Center, Amsterdam, The Netherlands; Department Downloaded from https://academic.oup.com/jcem/article/98/6/2484/2537184 by guest on 30 September 2021 of Biological Psychology (E.J.C.d.G.), VU University, Amsterdam, The Netherlands; Neuroscience Campus Amsterdam (E.J.C.d.G., B.W.J.H.P.), VU University Medical Center, Amsterdam, The Netherlands; Department of Psychiatry (B.W.J.H.P.), Leiden University Medical Center, Leiden, The Netherlands; and Department of Psychiatry (B.W.J.H.P.), University Medical Center Groningen, Groningen, The Netherlands Context: Stress is suggested to lead to metabolic dysregulations as clustered in the metabolic syndrome. Although dysregulation of the autonomic nervous system is found to associate with the metabolic syndrome and its dysregulations, no longitudinal study has been performed to date to examine the predictive value of this stress system in the development of the metabolic syndrome. Objective: We examined whether autonomic nervous system functioning predicts 2-year devel- opment of metabolic abnormalities that constitute the metabolic syndrome. Design: Data of the baseline and 2-year follow-up assessment of a prospective cohort: the Neth- erlands Study of Depression and Anxiety was used. Setting: Participants were recruited in the general community, primary care, and specialized men- tal health care organizations. Participants: A group of 1933 participants aged 18–65 years. Main outcome measures: The autonomic nervous system measures included heart rate (HR), re- spiratory sinus arrhythmia (RSA; high RSA reflecting high parasympathetic activity), pre-ejection period (PEP; high PEP reflecting low sympathetic activity), cardiac autonomic balance (CAB), and cardiac autonomic regulation (CAR). Metabolic syndrome was based on the updated Adult Treat- ment Panel III criteria and included high waist circumference, serum triglycerides, blood pressure, serum glucose, and low high-density lipoprotein (HDL) cholesterol. Results: Baseline short PEP, low CAB, high HR, and CAR were predictors of an increase in the number of components of the metabolic syndrome during follow-up. High HR and low CAB were predictors of a 2-year decrease in HDL cholesterol, and 2-year increase in diastolic and systolic blood pressure. Short PEP and high CAR also predicted a 2-year increase in systolic blood pressure, and short PEP additionally predicted 2-year increase in diastolic blood pressure. Finally, a low baseline RSA was predictive for subsequent decreases in HDL cholesterol. Conclusion: Increased sympathetic activity predicts an increase in metabolic abnormalities over time. These findings suggest that a dysregulation of the autonomic nervous system is an important predictor of cardiovascular diseases and diabetes through dysregulating lipid metabolism and blood pressure over time. (J Clin Endocrinol Metab 98: 2484–2493, 2013) ISSN Print 0021-972X ISSN Online 1945-7197 Abbreviations: ANS, autonomic nervous system; ATC, World Health Organization Ana- Printed in U.S.A. tomical Therapeutic Chemical classification; BP, blood pressure; CAB, cardiac autonomic Copyright © 2013 by The Endocrine Society balance; CAR, cardiac autonomic regulation; CI, confidence interval; ECG, electrocardio- Received August 16, 2012. Accepted March 26, 2013. gram; HDL, high-density lipoproteins; HR, heart rate; IBI, interbeat interval; LV, left ven- First Published Online April 3, 2013 tricle; NESDA, Netherlands Study of Depression and Anxiety study; OR, odds ratio; PEP, pre-ejection period; RSA, respiratory sinus arrhythmia. 2484 jcem.endojournals.org J Clin Endocrinol Metab, June 2013, 98(6):2484–2493 doi: 10.1210/jc.2012-3104 doi: 10.1210/jc.2012-3104 jcem.endojournals.org 2485 t has often been hypothesized that stress leads to the participating universities and all respondents provided written I metabolic syndrome (1–3). Dysregulation of one of the informed consent. Two years after baseline, a face-to-face fol- main stress systems—the autonomic nervous system— low-up assessment was conducted with a response of 2596 of the 2981 respondents (87%). Nonresponders were younger, more could lead to insulin resistance, altered lipid metabolism, often of non-northern European ancestry, and less educated and and increased blood pressure (BP) (4–8). Results of a large more often had major depressive disorder (23). cross-sectional study indeed indicated that dysregulation Of the total follow-up sample, 340 participants had no data of the autonomic nervous system (ANS) is associated with on metabolic abnormalities on 1 of the 2 time points and an several metabolic alterations. Increased heart rate (HR) additional 107 had missing data on all baseline ANS measures. Because of the known effects of antidepressants on the ANS (24) with decreased respiratory sinus arrhythmia (RSA), indic- and the metabolic syndrome (25), we excluded 131 subjects who ative of low parasympathetic activity, and decreased pre- changed antidepressant use during the follow-up period (ie, sub- ejection period (PEP), indicative of high sympathetic ac- jects who started, stopped, or switched to another antidepres- Downloaded from https://academic.oup.com/jcem/article/98/6/2484/2537184 by guest on 30 September 2021 tivity, were found to associate with high BP, serum sant) because in these individuals changes in metabolic syndrome triglycerides, serum glucose, and waist circumference and also could be due to changes in antidepressant medication. Use with the presence of the metabolic syndrome and the num- of antidepressants was considered present when taken for at least 1 month and 50% of the time. Using the World Health Orga- ber of its components (9). The metabolic syndrome con- nization Anatomical Therapeutic Chemical (ATC) classifica- sists of a cluster of these metabolic abnormalities and is tion, medications were classified. Tricyclic antidepressants (ATC thought to be one of the most important risk factors for code N06AA), serotonergic and noradrenergic working antide- cardiovascular diseases (10, 11) and diabetes (12). Our pressants (ATC code N06AF/N06AX), and selective serotonin findings were in line with most other cross-sectional stud- reuptake inhibitors (ATC code N06AB) were included. Simi- ␤ ies investigating the association between metabolic abnor- larly, because of the impact of -blockers on the ANS as well as on metabolic factors (26–31), subjects who stopped or started malities and ANS functioning (3, 13, 14). Elevated the use of a ␤-blocker (ATC code C07, used for at least a month sympathetic nervous system activity and diminished para- and daily or more than 50% of the time) were also excluded (n ϭ sympathetic nervous system activity were found in sub- 85). Subjects who consistently used ␤-blockers or antidepres- jects with metabolic syndrome (15–19). As far as we sants during the 2-year follow-up remained included. The pres- know, only one longitudinal study has been performed ent study sample therefore consisted of 1933 participants. that investigated the predictive value of metabolic syn- Outcome measures drome factors for changes in HR variability (20). How- ever, no longitudinal studies have been performed to Metabolic syndrome test the reverse causality. Therefore, it remains unclear The metabolic syndrome was defined according to the Amer- whether autonomic dysregulation, as a marker of biolog- ican Heart Association and National Heart, Lung, and Blood ical stress activation, leads to metabolic dysregulations Institute’s update of the US National Cholesterol Education Pro- gram–Adult Treatment Panel III criteria (32). The US National and the metabolic syndrome (21). Cholesterol Education Program–Adult Treatment Panel III To examine the relation between (multiple) measures of guidelines define metabolic syndrome as a presence of 3 or more ANS and metabolic components in a large cohort study, of the following criteria: 1) waist circumference Ն102 cm in men we explored whether and which baseline autonomic mea- and Ն88 cm in women; 2) triglycerides Ն1.7 mmol/L (150 mg/ sures predicted worsening of metabolic syndrome com- dL) or medication for hypertriglyceridemia; 3) high-density li- Ͻ ponents over a 2-year time period, while considering pos- poprotein (HDL) cholesterol 1.03 mmol/L (40 mg/dL) in men and Ͻ1.30 mmol/L (50 mg/dL) in women or medication for sible important covariates. reduced HDL cholesterol; 4) BP: systolic Ն130 and/or diastolic Ն85 mm Hg or antihypertensive medication; 5) fasting plasma glucose Ն5.6 mmol/L (100 mg/dL) or antidiabetic medication. Materials and Methods The number of metabolic syndrome components was used as an indicator of severity of metabolic abnormalities (25). Study sample Data are from the Netherlands Study of Depression and Anx- Metabolic syndrome components iety (NESDA), a large longitudinal cohort study among 2981 In addition to metabolic syndrome, associations with contin- adults (18–65 y), 95.2% of North-European ancestry (see [22]). uous levels of individual metabolic components were examined, Respondents were recruited from the community, in primary to investigate
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