Skip to main content
Log in

Symptoms of anxiety and mood disturbance alter cardiac and peripheral autonomic control in patients with metabolic syndrome

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Previous investigations show that metabolic syndrome (MetSyn) causes sympathetic hyperactivation. Symptoms of anxiety and mood disturbance (AMd) provoke sympatho-vagal imbalance. We hypothesized that AMd would alter even further the autonomic function in patients with MetSyn. Twenty-six never-treated patients with MetSyn (ATP-III) were allocated to two groups, according to the levels of anxiety and mood disturbance: (1) with AMd (MetSyn + AMd, n = 15), and (2) without AMd (MetSyn, n = 11). Ten healthy control subjects were also studied (C, n = 10). AMd was determined using quantitative questionnaires. Muscle sympathetic nerve activity (MSNA, microneurography), blood pressure (oscillometric beat-to-beat basis), and heart rate (ECG) were measured during a baseline 10-min period. Spectral analysis of RR interval and systolic arterial pressure were analyzed, and the power of low (LF) and high (HF) frequency bands were determined. Sympatho-vagal balance was obtained by LF/HF ratio. Spontaneous baroreflex sensitivity (BRS) was evaluated by calculation of α-index. MSNA was greater in patients with MetSyn + AMd compared with MetSyn and C. Patients with MetSyn + AMd showed higher LF and lower HF power compared with MetSyn and C. In addition, LF/HF balance was higher in MetSyn + AMd than in MetSyn and C groups. BRS was decreased in MetSyn + AMd compared with MetSyn and C groups. Anxiety and mood disturbance alter autonomic function in patients with MetSyn. This autonomic dysfunction may contribute to the increased cardiovascular risk observed in patients with mood alterations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

AMd:

Anxiety and mood disturbance

BMI:

Body mass index

BP:

Blood pressure

BRS:

Baroreflex sensitivity

HF:

High frequency

k 2 :

Coherence

LF:

Low frequency

LF/HF:

Sympatho-vagal balance

MetSyn:

Metabolic syndrome

MSN:

Muscle sympathetic nerve activity

n.u.:

Normalized unit

pNN50:

Percent of successive RR interval differences >50 ms

POM:

Profile of mood states

rMSSD:

Root mean squares successive differences of RR intervals

RRI:

RR interval

SAP:

Systolic arterial pressure

SDNN:

Standard deviation of RR intervals

STAI:

State and trait anxiety inventory

TMD:

Total mood disturbance

VLF:

Very low frequency

φ:

Phase shift

References

  • Andrade L, Gorenstein C, Vieira Filho AH, Tung TC, Artes R (2001) Psychometric properties of the Portuguese version of the state-trait anxiety inventory applied to college students: factor analysis and relation to the beck depression inventory. Braz J Med Biol Res 34:367–374

    Article  PubMed  CAS  Google Scholar 

  • Bao AM, Meynen G, Swaab DF (2008) The stress system in depression and neurodegeneration: focus on the human hypothalamus. Brain Res Rev 57:531–553

    Article  PubMed  CAS  Google Scholar 

  • Bardwell WA, Moore P, Ancoli-Israel S, Dimsdale JE (2003) Fatigue in obstructive sleep apnea: driven by depressive symptoms instead of apnea severity? Am J Psychiatry 160:350–355

    Article  PubMed  Google Scholar 

  • Brunner EJ, Hemingway H, Walker BR, Page M, Clarke P, Juneja M, Shipley MJ, Kumari M, Andrew R, Seckl JR, Papadopoulos A, Checkley S, Rumley A, Lowe GD, Stansfeld SA, Marmot MG (2002) Adrenocortical, autonomic, and inflammatory causes of the metabolic syndrome: nested case-control study. Circulation 106:2659–2665

    Article  PubMed  CAS  Google Scholar 

  • Contoreggi C, Herning RI, Na P, Gold PW, Chrousos G, Negro PJ, Better W, Cadet JL (2003) Stress hormone responses to corticotropin-releasing hormone in substance abusers without severe comorbid psychiatric disease. Biol Psychiatry 54:873–878

    Article  PubMed  CAS  Google Scholar 

  • Fuchs E, Flugge G (2003) Chronic social stress: effects on limbic brain structures. Physiol Behav 79:417–427

    Article  PubMed  CAS  Google Scholar 

  • Gami AS, Witt BJ, Howard DE, Erwin PJ, Gami LA, Somers VK, Montori VM (2007) Metabolic syndrome and risk of incident cardiovascular events and death: a systematic review and meta-analysis of longitudinal studies. J Am Coll Cardiol 49:403–414

    Article  PubMed  CAS  Google Scholar 

  • Gianaros PJ, Sheu LK, Matthews KA, Jennings JR, Manuck SB, Hariri AR (2008) Individual differences in stressor-evoked blood pressure reactivity vary with activation, volume, and functional connectivity of the amygdala. J Neurosci 28:990–999

    Article  PubMed  CAS  Google Scholar 

  • Grassi G, Seravalle G, Dell’Oro R, Turri C, Pasqualinotto L, Colombo M, Mancia G (2001) Participation of the hypothalamus–hypophysis axis in the sympathetic activation of human obesity. Hypertension 38:1316–1320

    Article  PubMed  CAS  Google Scholar 

  • Grassi G, Dell’Oro R, Quarti-Trevano F, Scopelliti F, Seravalle G, Paleari F, Gamba PL, Mancia G (2005) Neuroadrenergic and reflex abnormalities in patients with metabolic syndrome. Diabetologia 48:1359–1365

    Article  PubMed  CAS  Google Scholar 

  • Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC Jr, Spertus JA, Costa F (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 112:2735–2752

    Article  PubMed  Google Scholar 

  • Huggett RJ, Burns J, Mackintosh AF, Mary DA (2004) Sympathetic neural activation in nondiabetic metabolic syndrome and its further augmentation by hypertension. Hypertension 44:847–852

    Article  PubMed  CAS  Google Scholar 

  • Jackson K, Silva HM, Zhang W, Michelini LC, Stern JE (2005) Exercise training differentially affects intrinsic excitability of autonomic and neuroendocrine neurons in the hypothalamic paraventricular nucleus. J Neurophysiol 94:3211–3220

    Article  PubMed  Google Scholar 

  • Kop WJ, Synowski SJ, Newell ME, Schmidt LA, Waldstein SR, Fox NA (2011) Autonomic nervous system reactivity to positive and negative mood induction: the role of acute psychological responses and frontal electrocortical activity. Biol Psychol 86:230–238

    Article  PubMed  Google Scholar 

  • La Rovere MT, Pinna GD, Hohnloser SH, Marcus FI, Mortara A, Nohara R, Bigger JT Jr, Camm AJ, Schwartz PJ (2001) Baroreflex sensitivity and heart rate variability in the identification of patients at risk for life-threatening arrhythmias: implications for clinical trials. Circulation 103:2072–2077

    Article  PubMed  Google Scholar 

  • Lambert E, Dawood T, Straznicky N, Sari C, Schlaich M, Esler M, Lambert G (2010) Association between the sympathetic firing pattern and anxiety level in patients with the metabolic syndrome and elevated blood pressure. J Hypertens 28:543–550

    Article  PubMed  CAS  Google Scholar 

  • Laterza MC, de Matos LD, Trombetta IC, Braga AM, Roveda F, Alves MJ, Krieger EM, Negrao CE, Rondon MU (2007) Exercise training restores baroreflex sensitivity in never-treated hypertensive patients. Hypertension 49:1298–1306

    Article  PubMed  CAS  Google Scholar 

  • Lucini D, Di Fede G, Parati G, Pagani M (2005) Impact of chronic psychosocial stress on autonomic cardiovascular regulation in otherwise healthy subjects. Hypertension 46:1201–1206

    Article  PubMed  CAS  Google Scholar 

  • Lucini D, Cusumano G, Bellia A, Kozakova M, Difede G, Lauro R, Pagani M (2006) Is reduced baroreflex gain a component of the metabolic syndrome? Insights from the LINOSA study. J Hypertens 24:361–370

    Article  PubMed  CAS  Google Scholar 

  • Malliani A, Pagani M, Lombardi F, Cerutti S (1991) Cardiovascular neural regulation explored in the frequency domain. Circulation 84:482–492

    Article  PubMed  CAS  Google Scholar 

  • Martinez DG, Nicolau JC, Lage RL, Toschi-Dias E, de Matos LD, Alves MJ, Trombetta IC, Dias da Silva VJ, Middlekauff HR, Negrao CE, Rondon MU (2011) Effects of long-term exercise training on autonomic control in myocardial infarction patients. Hypertension 58:1049–1056

    Article  PubMed  CAS  Google Scholar 

  • McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904

    Article  PubMed  Google Scholar 

  • Montano N, Ruscone TG, Porta A, Lombardi F, Pagani M, Malliani A (1994) Power spectrum analysis of heart rate variability to assess the changes in sympathovagal balance during graded orthostatic tilt. Circulation 90:1826–1831

    Article  PubMed  CAS  Google Scholar 

  • Norcross JC, Guadagnoli E, Prochaska JO (1984) Factor structure of the profile of mood states (POMS): two partial replications. J Clin Psychol 40:1270–1277

    Article  PubMed  CAS  Google Scholar 

  • Pagani M, Lombardi F, Guzzetti S, Rimoldi O, Furlan R, Pizzinelli P, Sandrone G, Malfatto G, Dell’Orto S, Piccaluga E (1986) Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog. Circ Res 59:178–193

    Article  PubMed  CAS  Google Scholar 

  • Pagani M, Somers V, Furlan R, Dell’Orto S, Conway J, Baselli G, Cerutti S, Sleight P, Malliani A (1988) Changes in autonomic regulation induced by physical training in mild hypertension. Hypertension 12:600–610

    Article  PubMed  CAS  Google Scholar 

  • Pruessner JC, Baldwin MW, Dedovic K, Renwick R, Mahani NK, Lord C, Meaney M, Lupien S (2005) Self-esteem, locus of control, hippocampal volume, and cortisol regulation in young and old adulthood. Neuroimage 28:815–826

    Article  PubMed  Google Scholar 

  • Rosmond R (2005) Role of stress in the pathogenesis of the metabolic syndrome. Psychoneuroendocrinology 30:1–10

    Article  PubMed  CAS  Google Scholar 

  • Scott JP, McNaughton LR, Polman RC (2006) Effects of sleep deprivation and exercise on cognitive, motor performance and mood. Physiol Behav 87:396–408

    Article  PubMed  CAS  Google Scholar 

  • Skilton MR, Moulin P, Terra JL, Bonnet F (2007) Associations between anxiety, depression, and the metabolic syndrome. Biol Psychiatry 62:1251–1257

    Article  PubMed  CAS  Google Scholar 

  • Vallbo AB, Hagbarth KE, Torebjork HE, Wallin BG (1979) Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves. Physiol Rev 59:919–957

    PubMed  CAS  Google Scholar 

  • Virtanen R, Jula A, Salminen JK, Voipio-Pulkki LM, Helenius H, Kuusela T, Airaksinen J (2003) Anxiety and hostility are associated with reduced baroreflex sensitivity and increased beat-to-beat blood pressure variability. Psychosom Med 65:751–756

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by Conselho Nacional de Pesquisa (CNPq # 476385/2006-7), by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP # 2010/50048-1) and, in part, by Fundação Zerbini. Toschi-Dias E, Negrão CE and Rondon MUPB were supported by Conselho Nacional de Pesquisa (CNPq # 140643/2009-5, # 301867/2010-0, # 308068/2011-4, respectively). Trombetta IC was supported by Fundação de Amparo à Pesquisa (FAPESP # 2008/03714-6). Maki-Nunes C and Martinez DG were supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

Conflict of interest

The authors declared no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria Urbana P. B. Rondon.

Additional information

Communicated by Dag Linnarsson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Toschi-Dias, E., Trombetta, I.C., da Silva, V.J.D. et al. Symptoms of anxiety and mood disturbance alter cardiac and peripheral autonomic control in patients with metabolic syndrome. Eur J Appl Physiol 113, 671–679 (2013). https://doi.org/10.1007/s00421-012-2476-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-012-2476-8

Keywords

Navigation