Increased Sympathetic Cardiac Autonomic Modulation after Two Consecutive Tilt Tests in Women with Polycystic Ovary Syndrome

Abstract

Objective The present study aimed to analyze cardiac autonomic modulation via spectral and symbolic analysis of heart rate variability (HRV) in women with polycystic ovary syndrome (PCOS) who were subjected to two consecutive tilt tests.

Methods A total of 64 women were selected and divided into 2 groups: control (without PCOS), and PCOS. Concentrations of follicle-stimulating hormone, luteinizing hormone, prolactin, estradiol, homocysteine, sex hormone-binding globulin, thyroid stimulating hormone, fasting insulin, testosterone, androstenedione, and 17-hydroxyprogesterone levels, triglycerides, free androgen index (FAI), and homeostasis assessment model (HOMA-IR) were assessed. Cardiac autonomic modulation was evaluated by spectral and symbolic analyses during two consecutive tilt tests (two moments) and supine moments before, between and after (three moments) the tilt tests.

Results Women with PCOS had higher fasting insulin, HOMA-IR indexes, testosterone and FAI. Additionally, we observed that the PCOS group had greater sympathetic autonomic cardiac modulation in supine 2, tilt 1, and supine 3 moments compared with controls.

Conclusion Women with PCOS had higher autonomic sympathetic cardiac modulation even after a second tilt test. No adaptation to this provocative test was observed. Spectral analysis was more sensitive for identifying differences between groups than the symbolic analysis.

Resumo

Objetivo O presente estudo teve como objetivo analisar a modulação autonômica cardíaca por análise espectral e simbólica da variabilidade da frequência cardíaca (VFC) em mulheres com síndrome dos ovários policísticos (SOP) que foram submetidas a dois testes consecutivos de inclinação.

Métodos Um total de 64 mulheres foram selecionadas e divididas em 2 grupos: controle (sem SOP) e SOP. Concentrações de hormônio folículo-estimulante, hormônio luteinizante, prolactina, estradiol, homocisteína, globulina de ligação a hormônios sexuais, hormônio estimulante da tireóide, insulina em jejum, testosterona e androstenediona e níveis de 17-hidroxiprogesterona, triglicerídeos, índice de andrógeno livre (FAI) e homeostase modelo de avaliação (HOMA-IR) foram avaliados. A modulação autonômica cardíaca foi avaliada por análises espectrais e simbólicas durante dois testes de inclinação consecutivos (dois momentos) e momentos supinos antes, entre e após (três momentos) os testes de inclinação.

Resultados Mulheres com SOP apresentaram insulina em jejuM, índices HOMA-IR, testosterona e FAI mais altos. Além disso, observamos que o grupo PCOS apresentou maior modulação cardíaca autonômica simpática nos momentos supino 2, inclinado 1 e supino 3 em comparação aos controles.

Conclusão Mulheres com SOP apresentaram modulação cardíaca simpática autonômica mais alta mesmo após um segundo teste de inclinação. Nenhuma adaptação a esse teste provocativo foi observada. A análise espectral foi mais sensível para identificar diferenças entre os grupos do que a análise simbólica.

Keywords

polycystic ovary syndrome - cardiac autonomic modulation - hyperandrogenism - spectral analysis - symbolic analysis

Descritores

síndrome dos ovários policísticos - modulação autonômica cardíaca - hiperandrogenismo - análise espectral - análise simbólica

Contributions

All authors were involved in the design and interpretation of the analyses, contributed to the writing of the manuscript, read and approved the final manuscript.

• References

• 1 Ding T, Hardiman PJ, Petersen I, Wang FF, Qu F, Baio G. The prevalence of polycystic ovary syndrome in reproductive-aged women of different ethnicity: a systematic review and meta-analysis. Oncotarget. 2017; 8 (56) 96351-96358 . Doi: 10.18632/oncotarget.19180
• 2 Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil Steril. 2004; 81 (01) 19-25 . Doi: 10.1016/j.fertnstert.2003.10.004
• 3 Ribeiro VB, Kogure GS, Reis RM, Gastaldi AC, De Araújo JE, Mazon JH. , et al. Polycystic ovary syndrome presents higher sympathetic cardiac autonomic modulation that is not altered by strength training. Int J Exerc Sci. 2016; 9 (05) 554-566
• 4 Chan JL, Kar S, Vanky E, Morin-Papunen L, Piltonen T, Puurunen J. , et al. Racial and ethnic differences in the prevalence of metabolic syndrome and its components of metabolic syndrome in women with polycystic ovary syndrome: a regional cross-sectional study. Am J Obstet Gynecol. 2017; 217 (02) 189.e1-189.e8
• 5 Jena D, Choudhury AK, Mangaraj S, Singh M, Mohanty BK, Baliarsinha AK. Study of visceral and subcutaneous abdominal fat thickness and its correlation with cardiometabolic risk factors and hormonal parameters in polycystic ovary syndrome. Indian J Endocrinol Metab. 2018; 22 (03) 321-327 . Doi: 10.4103/ijem.IJEM_646_17
• 6 Pasquali R. Metabolic syndrome in polycystic ovary syndrome. Front Horm Res. 2018; 49: 114-130 . Doi: 10.1159/000485995
• 7 Dargham SR, Shewehy AE, Dakroury Y, Kilpatrick ES, Atkin SL. Prediabetes and diabetes in a cohort of Qatari women screened for polycystic ovary syndrome. Sci Rep. 2018; 8 (01) 3619 . Doi: 10.1038/s41598-018-21987-6
• 8 Kleiger RE, Miller JP, Bigger Jr JT, Moss AJ. Decreased heart rate variability and its association with increased mortality after acute myocardial infarction. Am J Cardiol. 1987; 59 (04) 256-262 . Doi: 10.1016/0002-9149(87)90795-8
• 9 Glintborg D, Rubin KH, Nybo M, Abrahamsen B, Andersen M. Cardiovascular disease in a nationwide population of Danish women with polycystic ovary syndrome. Cardiovasc Diabetol. 2018; 17 (01) 37 . Doi: 10.1186/s12933-018-0680-5
• 10 Gui J, Wang RH. Cardiovascular autonomic dysfunction in women with polycystic ovary syndrome: a systematic review and meta-analysis. Reprod Biomed Online. 2017; 35 (01) 113-120 . Doi: 10.1016/j.rbmo.2017.03.018
• 11 Saranya K, Pal GK, Habeebullah S, Pal P. Assessment of cardiovascular autonomic function in patients with polycystic ovary syndrome. J Obstet Gynaecol Res. 2014; 40 (01) 192-199 . Doi: 10.1111/jog.12154
• 12 Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation. 1996; 93 (05) 1043-1065 . Doi: 10.1161/01.CIR.93.5.1043
• 13 Porta A, Guzzetti S, Montano N, Furlan R, Pagani M, Malliani A. , et al. Entropy, entropy rate, and pattern classification as tools to typify complexity in short heart period variability series. IEEE Trans Biomed Eng. 2001; 48 (11) 1282-1291
• 14 Abad CC, Nascimento AM, Gil S, Kobal R, Loturco I, Nakamura FY. , et al. Cardiac autonomic control in high level Brazilian power and endurance track-and-field athletes. Int J Sports Med. 2014; 35 (09) 772-778 . Doi: 10.1055/s-0033-1363268
• 15 Porta A, Tobaldini E, Guzzetti S, Furlan R, Montano N, Gnecchi-Ruscone T. Assessment of cardiac autonomic modulation during graded head-up tilt by symbolic analysis of heart rate variability. Am J Physiol Heart Circ Physiol. 2007; 293 (01) H702-H708 . Doi: 10.1152/ajpheart.00006.2007
• 16 Freeman R, Chapleau MW. Testing the autonomic nervous system. Handb Clin Neurol. 2013; 115: 115-136 . Doi: 10.1016/B978-0-444-52902-2.00007-2
• 17 Laranjo S, Geraldes V, Oliveira M, Rocha I. Insights into the background of autonomic medicine. Rev Port Cardiol. 2017; 36 (10) 757-771 . Doi: 10.1016/j.repc.2017.01.007
• 18 Fraser IS, Critchley HO, Munro MG, Broder M. ; Writing Group for this Menstrual Agreement Process. A process designed to lead to international agreement on terminologies and definitions used to describe abnormalities of menstrual bleeding. Fertil Steril. 2007; 87 (03) 466-476 . Doi: 10.1016/j.fertnstert.2007.01.023
• 19 Griffin IJ, Cole TJ, Duncan KA, Hollman AS, Donaldson MD. Pelvic ultrasound measurements in normal girls. Acta Paediatr. 1995; 84 (05) 536-543 . Doi: 10.1111/j.1651-2227.1995.tb13689.x
• 20 Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972; 18 (06) 499-502
• 21 Cascella T, Palomba S, Tauchmanovà L, Manguso F, Di Biase S, Labella D. , et al. Serum aldosterone concentration and cardiovascular risk in women with polycystic ovarian syndrome. J Clin Endocrinol Metab. 2006; 91 (11) 4395-4400 . Doi: 10.1210/jc.2006-0399
• 22 Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985; 28 (07) 412-419 . Doi: 10.1007/bf00280883
• 23 International Society for the Advancement of Kinanthropometry. International standards for anthropometric assessment. Potchefstroom: The International Society for Advancement of Kinanthropometry; 2001
• 24 Malliani A, Pagani M, Lombardi F, Cerutti S. Cardiovascular neural regulation explored in the frequency domain. Circulation. 1991; 84 (02) 482-492 . Doi: 10.1161/01.cir.84.2.482
• 25 Shorakae S, Ranasinha S, Abell S, Lambert G, Lambert E, de Courten B. , et al. Inter-related effects of insulin resistance, hyperandrogenism, sympathetic dysfunction and chronic inflammation in PCOS. Clin Endocrinol (Oxf). 2018; 89 (05) 628-633 . Doi: 10.1111/cen.13808
• 26 Kuppusamy S, Pal GK, Habeebullah S, Ananthanarayanan PH, Pal P. Association of sympathovagal imbalance with cardiovascular risks in patients with polycystic ovary syndrome. Endocr Res. 2015; 40 (01) 37-43 . Doi: 10.3109/07435800.2014.920350
• 27 Di Domenico K, Wiltgen D, Nickel FJ, Magalhães JA, Moraes RS, Spritzer PM. Cardiac autonomic modulation in polycystic ovary syndrome: does the phenotype matter?. Fertil Steril. 2013; 99 (01) 286-292 . Doi: 10.1016/j.fertnstert.2012.08.049
• 28 Nohara K, Waraich RS, Liu S, Ferron M, Waget A, Meyers MS. , et al. Developmental androgen excess programs sympathetic tone and adipose tissue dysfunction and predisposes to a cardiometabolic syndrome in female mice. Am J Physiol Endocrinol Metab. 2013; 304 (12) E1321-E1330 . Doi: 10.1152/ajpendo.00620.2012
• 29 Barber TM, Vojtechova P, Franks S. The impact of hyperandrogenism in female obesity and cardiometabolic diseases associated with polycystic ovary syndrome. Horm Mol Biol Clin Investig. 2013; 15 (03) 91-103 . Doi: 10.1515/hmbci-2013-0014
• 30 De Angelis C, Perelli P, Trezza R, Casagrande M, Biselli R, Pannitteri G. , et al. Modified autonomic balance in offsprings of diabetics detected by spectral analysis of heart rate variability. Metabolism. 2001; 50 (11) 1270-1274 . Doi: 10.1053/meta.2001.27225
• 31 de Sá JC, Costa EC, da Silva E, Zuttin RS, da Silva EP, Lemos TM. , et al. Analysis of heart rate variability in polycystic ovary syndrome. Gynecol Endocrinol. 2011; 27 (06) 443-447 . Doi: 10.3109/09513590.2010.501881
• 32 Kangas P, Tikkakoski A, Uitto M, Viik J, Bouquin H, Niemelä O. , et al. Metabolic syndrome is associated with decreased heart rate variability in a sex-dependent manner: a comparison between 252 men and 249 women. Clin Physiol Funct Imaging. 2019; 39 (02) 160-167 . Doi: 10.1111/cpf.12551
• 33 Dutra SGV, Pereira APM, Tezini GCSV, Mazon JH, Martins-Pinge MC, Souza HC. Cardiac autonomic modulation is determined by gender and is independent of aerobic physical capacity in healthy subjects. PLoS One. 2013; 8 (10) e77092 . Doi: 10.1371/journal.pone.0077092
• 34 Sandhu KS, Khan P, Panting J, Nadar S. Tilt-table test: its role in modern practice. Clin Med (Lond). 2013; 13 (03) 227-232 . Doi: 10.7861/clinmedicine.13-3-227