open access

Vol 58, No 2 (2024)
Research Paper
Submitted: 2023-04-11
Accepted: 2023-07-05
Published online: 2023-09-05
Get Citation

Effect of series of periodic limb movements in sleep on blood pressure, heart rate and high frequency heart rate variability

Marta A. Malkiewicz1, Malgorzata Grzywinska2, Krzysztof S. Malinowski3, Eemil Partinen45, Markku Partinen46, Wieslaw J. Cubala7, Pawel J. Winklewski3, Mariusz Sieminski8
·
Pubmed: 37668022
·
Neurol Neurochir Pol 2024;58(2):167-175.
Affiliations
  1. Applied Cognitive Neuroscience Lab, Department of Neurophysiology, Neuropsychology and Neuroinformatics, Medical University of Gdansk, Gdansk, Poland
  2. Neuroinformatics and Artificial Intelligence Lab, Department of Neurophysiology, Neuropsychology and Neuroinformatics, Medical University of Gdansk, Gdansk, Poland
  3. Department of Neurophysiology, Neuropsychology and Neuroinformatics, Medical University of Gdansk, Gdansk, Poland
  4. Helsinki Sleep Clinic, Terveystalo Healthcare, Helsinki, Finland
  5. Department of Neurology, Helsinki University Central Hospital, Helsinki, Finland
  6. Department of Neurosciences, Clinicum, University of Helsinki, Helsinki, Finland
  7. Department of Psychiatry, Medical University of Gdansk, Gdansk, Poland
  8. Department of Emergency Medicine, Medical University of Gdansk, Marii Sklodowskiej-Curie 3a, 80-210 Gdansk, Poland

open access

Vol 58, No 2 (2024)
Research papers
Submitted: 2023-04-11
Accepted: 2023-07-05
Published online: 2023-09-05

Abstract

Introduction. The phenomenon known as periodic limb movements in sleep (PLMS) has been linked to a change in autonomic nervous system (ANS) activity and its effect on circulatory regulation. Autonomic dysfunction or dysregulation in patients with PLMS has been described in some domains; however, any relationship between heart rate variability (HRV) and PLMS has not been clearly established. HRV analysis is a recognised, non-invasive research method that describes the influence of the ANS on heart rate (HR). The aim of our study was to further investigate the dysregulation of autonomic HR control in patients with PLMS.

Material and methods. We undertook a retrospective analysis of the polysomnographic (PSG), demographic and medical data of five patients with a total number of 1,348 PLMS. We analysed HR, HRV HF, systolic blood pressure (SBP), and diastolic blood pressure (DBP) for 10 heartbeats before the series of PLMS and 10 consecutive heartbeats as beat-to-beat measurements. The presented method of using successive, short, 10 RR interval segments refers to the time-frequency measurement, which is very clear and useful for presenting changes in the calculated parameters over time and thereby illustrating their dynamics. This method allowed us to assess dynamic changes in HRV HF during successive PLMS series. Statistical analysis was performed using IBM SPSS Statistics (v. 28.0.0.0). The Kruskal–Wallis test was performed to find statistically significant changes from baseline.

Results. No statistically significant changes in HR, SBP, or DBP were found in our group, although an increase in the value of the HRV HF was noted, suggesting an increase in intracardiac parasympathetic activity during the subsequent series of PLMS.

Conclusions. Our study indicates an increase in parasympathetic activity during the appearance of successive PLMS, which, with the simultaneous lack of changes in HR, may suggest an increase in sympathetic activity, and therefore the appearance of so-called ‘autonomic co-activation’ resulting in the possibility of life-threatening cardiac events.

Clinical implications. Our findings add to the literature information regarding HRV in PLMS, and highlight the need for further studies to elucidate the effects of these conditions on the ANS, and on cardiovascular health.

Abstract

Introduction. The phenomenon known as periodic limb movements in sleep (PLMS) has been linked to a change in autonomic nervous system (ANS) activity and its effect on circulatory regulation. Autonomic dysfunction or dysregulation in patients with PLMS has been described in some domains; however, any relationship between heart rate variability (HRV) and PLMS has not been clearly established. HRV analysis is a recognised, non-invasive research method that describes the influence of the ANS on heart rate (HR). The aim of our study was to further investigate the dysregulation of autonomic HR control in patients with PLMS.

Material and methods. We undertook a retrospective analysis of the polysomnographic (PSG), demographic and medical data of five patients with a total number of 1,348 PLMS. We analysed HR, HRV HF, systolic blood pressure (SBP), and diastolic blood pressure (DBP) for 10 heartbeats before the series of PLMS and 10 consecutive heartbeats as beat-to-beat measurements. The presented method of using successive, short, 10 RR interval segments refers to the time-frequency measurement, which is very clear and useful for presenting changes in the calculated parameters over time and thereby illustrating their dynamics. This method allowed us to assess dynamic changes in HRV HF during successive PLMS series. Statistical analysis was performed using IBM SPSS Statistics (v. 28.0.0.0). The Kruskal–Wallis test was performed to find statistically significant changes from baseline.

Results. No statistically significant changes in HR, SBP, or DBP were found in our group, although an increase in the value of the HRV HF was noted, suggesting an increase in intracardiac parasympathetic activity during the subsequent series of PLMS.

Conclusions. Our study indicates an increase in parasympathetic activity during the appearance of successive PLMS, which, with the simultaneous lack of changes in HR, may suggest an increase in sympathetic activity, and therefore the appearance of so-called ‘autonomic co-activation’ resulting in the possibility of life-threatening cardiac events.

Clinical implications. Our findings add to the literature information regarding HRV in PLMS, and highlight the need for further studies to elucidate the effects of these conditions on the ANS, and on cardiovascular health.

Get Citation

Keywords

periodic limb movements in sleep, periodic movement disorder of sleep, heart rate variability, autonomic nervous system, sleep-related movement disorder, autonomic co-activation

About this article
Title

Effect of series of periodic limb movements in sleep on blood pressure, heart rate and high frequency heart rate variability

Journal

Neurologia i Neurochirurgia Polska

Issue

Vol 58, No 2 (2024)

Article type

Research Paper

Pages

167-175

Published online

2023-09-05

Page views

496

Article views/downloads

330

DOI

10.5603/pjnns.95117

Pubmed

37668022

Bibliographic record

Neurol Neurochir Pol 2024;58(2):167-175.

Keywords

periodic limb movements in sleep
periodic movement disorder of sleep
heart rate variability
autonomic nervous system
sleep-related movement disorder
autonomic co-activation

Authors

Marta A. Malkiewicz
Malgorzata Grzywinska
Krzysztof S. Malinowski
Eemil Partinen
Markku Partinen
Wieslaw J. Cubala
Pawel J. Winklewski
Mariusz Sieminski

References (63)
  1. Coleman RM, Pollak CP, Weitzman ED. Periodic movements in sleep (nocturnal myoclonus): relation to sleep disorders. Ann Neurol. 1980; 8(4): 416–421.
  2. Montplaisir J, Boucher S, Poirier G, et al. Clinical, polysomnographic, and genetic characteristics of restless legs syndrome: a study of 133 patients diagnosed with new standard criteria. Mov Disord. 1997; 12(1): 61–65.
  3. El-Ad B, Korczyn AD. Disorders of excessive daytime sleepiness — an update. J Neurol Sci. 1998; 153(2): 192–202.
  4. Jo H, Kim D, Song J, et al. Sleep disturbances and phenoconversion in patients with REM sleep behavior disorder. J Clin Med. 2021; 10(20).
  5. Drakatos P, Olaithe M, Verma D, et al. Periodic limb movements during sleep: a narrative review. J Thorac Dis. 2021; 13(11): 6476–6494.
  6. Lin CC, Chou CH, Fan YM, et al. Increased Risk of Dementia Among Sleep-Related Movement Disorders: A Population-Based Longitudinal Study in Taiwan. Medicine (Baltimore). 2015; 94(51): e2331.
  7. Sasai T, Matsuura M, Inoue Y. Change in heart rate variability precedes the occurrence of periodic leg movements during sleep: an observational study. BMC Neurol. 2013; 13: 139.
  8. Allena M, Campus C, Morrone E, et al. Periodic limb movements both in non-REM and REM sleep: relationships between cerebral and autonomic activities. Clin Neurophysiol. 2009; 120(7): 1282–1290.
  9. Karadeniz D, Ondze B, Besset A, et al. EEG arousals and awakenings in relation with periodic leg movements during sleep. J Sleep Res. 2000; 9(3): 273–277.
  10. Ferrillo F, Beelke M, Canovaro P, et al. Changes in cerebral and autonomic activity heralding periodic limb movements in sleep. Sleep Med. 2004; 5(4): 407–412.
  11. Barone DA, Ebben MR, DeGrazia M, et al. Heart rate variability in restless legs syndrome and periodic limb movements of Sleep. Sleep Sci. 2017; 10(2): 80–86.
  12. Koo BB, Blackwell T, Ancoli-Israel S, et al. Osteoporotic Fractures in Men (MrOS) Study Group. Association of incident cardiovascular disease with periodic limb movements during sleep in older men: outcomes of sleep disorders in older men (MrOS) study. Circulation. 2011; 124(11): 1223–1231.
  13. Walters AS, Rye DB. Review of the relationship of restless legs syndrome and periodic limb movements in sleep to hypertension, heart disease, and stroke. Sleep. 2009; 32(5): 589–597.
  14. Sieminski M, Pyrzowski J, Partinen M. Periodic limb movements in sleep are followed by increases in EEG activity, blood pressure, and heart rate during sleep. Sleep Breath. 2017; 21(2): 497–503.
  15. Pennestri MH, Montplaisir J, Colombo R, et al. Nocturnal blood pressure changes in patients with restless legs syndrome. Neurology. 2007; 68(15): 1213–1218.
  16. Siddiqui F, Strus J, Ming X, et al. Rise of blood pressure with periodic limb movements in sleep and wakefulness. Clin Neurophysiol. 2007; 118(9): 1923–1930.
  17. Sforza E, Nicolas A, Lavigne G, et al. EEG and cardiac activation during periodic leg movements in sleep: support for a hierarchy of arousal responses. Neurology. 1999; 52(4): 786–791.
  18. Thayer JF, Brosschot JF. Psychosomatics and psychopathology: looking up and down from the brain. Psychoneuroendocrinology. 2005; 30(10): 1050–1058.
  19. Koch C, Wilhelm M, Salzmann S, et al. A meta-analysis of heart rate variability in major depression. Psychol Med. 2019; 49(12): 1948–1957.
  20. Faurholt-Jepsen M, Kessing LV, Munkholm K. Heart rate variability in bipolar disorder: A systematic review and meta-analysis. Neurosci Biobehav Rev. 2017; 73: 68–80.
  21. Chalmers JA, Quintana DS, Abbott MJA, et al. Anxiety disorders are associated with reduced heart rate variability: a meta-analysis. Front Psychiatry. 2014; 5: 80.
  22. Clamor A, Lincoln TM, Thayer JF, et al. Resting vagal activity in schizophrenia: meta-analysis of heart rate variability as a potential endophenotype. Br J Psychiatry. 2016; 208(1): 9–16.
  23. Heimrich KG, Lehmann T, Schlattmann P, et al. Heart rate variability analyses in Parkinson's disease: a systematic review and meta-analysis. Brain Sci. 2021; 11(8).
  24. Kwaśniak-Butowska M, Dulski J, Pierzchlińska A, et al. Cardiovascular dysautonomia and cognition in Parkinson's Disease - a possible relationship. Neurol Neurochir Pol. 2021; 55(6): 525–535.
  25. Siuda J. Importance of non-motor symptoms in PD and atypical parkinsonism. Neurol Neurochir Pol. 2021; 55(6): 503–507.
  26. Lee D, Baek JiH, Cho YJi, et al. Association of resting heart rate and heart rate variability with proximal suicidal risk in patients with diverse psychiatric diagnoses. Front Psychiatry. 2021; 12: 652340.
  27. Kang GuE, Patriquin MA, Nguyen H, et al. Objective measurement of sleep, heart rate, heart rate variability, and physical activity in suicidality: A systematic review. J Affect Disord. 2020; 273: 318–327.
  28. Wojtasz I, Tomski A, Kaźmierski R. Association between nocturnal oxygen desaturation and ischaemic stroke outcomes. Neurol Neurochir Pol. 2022; 56(3): 267–275.
  29. Lavoie S, de Bilbao F, Haba-Rubio J, et al. Influence of sleep stage and wakefulness on spectral EEG activity and heart rate variations around periodic leg movements. Clin Neurophysiol. 2004; 115(10): 2236–2246.
  30. Guggisberg AG, Hess CW, Mathis J. The significance of the sympathetic nervous system in the pathophysiology of periodic leg movements in sleep. Sleep. 2007; 30(6): 755–766.
  31. Sforza E, Juony C, Ibanez V. Time-dependent variation in cerebral and autonomic activity during periodic leg movements in sleep: implications for arousal mechanisms. Clin Neurophysiol. 2002; 113(6): 883–891.
  32. Walter LM, Foster AM, Patterson RR, et al. Cardiovascular variability during periodic leg movements in sleep in children. Sleep. 2009; 32(8): 1093–1099.
  33. Sforza E, Pichot V, Barthelemy JC, et al. Cardiovascular variability during periodic leg movements: a spectral analysis approach. Clin Neurophysiol. 2005; 116(5): 1096–1104.
  34. Izzi F, Placidi F, Romigi A, et al. Is autonomic nervous system involved in restless legs syndrome during wakefulness? Sleep Med. 2014; 15(11): 1392–1397.
  35. Gesche H, Grosskurth D, Küchler G, et al. Continuous blood pressure measurement by using the pulse transit time: comparison to a cuff-based method. Eur J Appl Physiol. 2012; 112(1): 309–315.
  36. IBER, C. The AASM Manual for the Scoring of Sleep and Associated Events: Rules. Terminol Tech Specif [Internet]. 2007. https://ci.nii.ac.jp/naid/10024500923 (26.01.2022).
  37. Ferri R, Fulda S, Allen RP, et al. International and European Restless Legs Syndrome Study Groups (IRLSSG and EURLSSG). World Association of Sleep Medicine (WASM) 2016 standards for recording and scoring leg movements in polysomnograms developed by a joint task force from the International and the European Restless Legs Syndrome Study Groups (IRLSSG and EURLSSG). Sleep Med. 2016; 26: 86–95.
  38. Dodds KL, Miller CB, Kyle SD, et al. Heart rate variability in insomnia patients: A critical review of the literature. Sleep Med Rev. 2017; 33: 88–100.
  39. Gosselin N, Lanfranchi P, Michaud M, et al. Age and gender effects on heart rate activation associated with periodic leg movements in patients with restless legs syndrome. Clin Neurophysiol. 2003; 114(11): 2188–2195.
  40. Winkelman JW. The evoked heart rate response to periodic leg movements of sleep. Sleep. 1999; 22(5): 575–580.
  41. Cuellar NG. The effects of periodic limb movements in sleep (PLMS) on cardiovascular disease. Heart Lung. 2013; 42(5): 353–360.
  42. Pagani M, Lombardi F, Guzzetti S, et al. Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog. Circ Res. 1986; 59(2): 178–193.
  43. Goldstein DS, Bentho O, Park MY, et al. Low-frequency power of heart rate variability is not a measure of cardiac sympathetic tone but may be a measure of modulation of cardiac autonomic outflows by baroreflexes. Exp Physiol. 2011; 96(12): 1255–1261.
  44. Reyes del Paso GA, Langewitz W, Mulder LJM, et al. The utility of low frequency heart rate variability as an index of sympathetic cardiac tone: a review with emphasis on a reanalysis of previous studies. Psychophysiology. 2013; 50(5): 477–487.
  45. Ritz T. Studying noninvasive indices of vagal control: the need for respiratory control and the problem of target specificity. Biol Psychol. 2009; 80(2): 158–168.
  46. Massaro S, Pecchia L. Heart rate variability (HRV) analysis: a methodology for organizational neuroscience. Organ Res Methods. 2016; 22(1): 354–393.
  47. Kawano H, Okada R, Yano K. Histological study on the distribution of autonomic nerves in the human heart. Heart Vessels. 2003; 18(1): 32–39.
  48. Crick SJ, Wharton J, Sheppard MN, et al. Innervation of the human cardiac conduction system. A quantitative immunohistochemical and histochemical study. Circulation. 1994; 89(4): 1697–1708.
  49. Behnke M, Kreibig S, Kaczmarek L, et al. Autonomic nervous system activity during positive emotions: a meta-analytic review. Emotion Review. 2022; 14(2): 132–160.
  50. Kollai M, Koizumi K. Reciprocal and non-reciprocal action of the vagal and sympathetic nerves innervating the heart. J Auton Nerv Syst. 1979; 1(1): 33–52.
  51. Paton JFR, Boscan P, Pickering AE, et al. The yin and yang of cardiac autonomic control: vago-sympathetic interactions revisited. Brain Res Brain Res Rev. 2005; 49(3): 555–565.
  52. Chen CY, Luo CF, Hsu YC, et al. Comparison of the effects of atropine and labetalol on trigeminocardiac reflex-induced hemodynamic alterations during percutaneous microballoon compression of the trigeminal ganglion. Acta Anaesthesiol Taiwan. 2012; 50(4): 153–158.
  53. Malinowski KS, Wierzba TH, Neary JP, et al. Heart rate variability at rest predicts heart response to simulated diving. Biology (Basel). 2023; 12(1).
  54. Ito T, Inoue Y, Sugihara T, et al. Autonomic function in the early stage of panic disorder: power spectral analysis of heart rate variability. Psychiatry Clin Neurosci. 1999; 53(6): 667–672.
  55. Rash JA, Prkachin KM. Cardiac vagal reactivity during relived sadness is predicted by affect intensity and emotional intelligence. Biol Psychol. 2013; 92(2): 106–113.
  56. Paine P, Kishor J, Worthen SF, et al. Exploring relationships for visceral and somatic pain with autonomic control and personality. Pain. 2009; 144(3): 236–244.
  57. Hansel J, Solleder I, Gfroerer W, et al. Hypoxia and cardiac arrhythmias in breath-hold divers during voluntary immersed breath-holds. Eur J Appl Physiol. 2009; 105(5): 673–678.
  58. Koo BB, Mehra R, Blackwell T, et al. Osteoporotic Fractures in Men (MrOS) Study Group. Periodic limb movements during sleep and cardiac arrhythmia in older men (MrOS sleep). J Clin Sleep Med. 2014; 10(1): 7–11.
  59. Mirza M, Shen WK, Sofi A, et al. Frequent periodic leg movement during sleep is an unrecognized risk factor for progression of atrial fibrillation. PLoS One. 2013; 8(10): e78359.
  60. May AM, Blackwell T, Stone KL, et al. Osteoporotic Fractures in Men (MrOS) Study Group. Longitudinal relationships of periodic limb movements during sleep and incident atrial fibrillation. Sleep Med. 2016; 25: 78–86.
  61. Shattock M, Tipton M. ‘Autonomic conflict’: a different way to die during cold water immersion? J Physiol. 2012; 590(14): 3219–3230.
  62. Pomeranz B, Macaulay RJ, Caudill MA, et al. Assessment of autonomic function in humans by heart rate spectral analysis. Am J Physiol. 1985; 248(1 Pt 2): H151–H153.
  63. Ferri R, Rundo F, Zucconi M, et al. An evidence-based analysis of the association between periodic leg movements during sleep and arousals in restless legs syndrome. Sleep. 2015; 38(6): 919–924.

Regulations

Important: This website uses cookies. More >>

The cookies allow us to identify your computer and find out details about your last visit. They remembering whether you've visited the site before, so that you remain logged in - or to help us work out how many new website visitors we get each month. Most internet browsers accept cookies automatically, but you can change the settings of your browser to erase cookies or prevent automatic acceptance if you prefer.

By VM Media Group sp. z o.o., ul. Świętokrzyska 73, 80–180 Gdańsk, Poland
tel.:+48 58 320 94 94, fax:+48 58 320 94 60, e-mail: viamedica@viamedica.pl