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Spontaneous cardiac baroreflex sensitivity is enhanced during post-exercise ischemia in men but not in women

  • Milena Samora
  • André L. Teixeira
  • Jeann L. Sabino-Carvalho
  • Lauro C. Vianna
Original Article

Abstract

Purpose

To investigate the effect of isolated muscle metaboreflex activation on spontaneous cardiac baroreflex sensitivity (cBRS), and to characterize the potential sex-related differences in this interaction in young healthy subjects.

Methods

40 volunteers (20 men and 20 women, age: 22 ± 0.4 year) were recruited. After 5-min rest period, the subjects performed 90 s of isometric handgrip exercise at 40% of maximal voluntary contraction followed by 3 min of post-exercise ischemia (PEI). Beat-to-beat heart rate and arterial blood pressure were continuously measured by finger photopletysmography. Spontaneous cBRS was assessed using the sequence technique and heart rate variability was measured in time (RMSSD—standard deviation of the RR intervals) and frequency domains (LF—low and HF—high frequency power).

Results

Resting cBRS was similar between men and women. During PEI, cBRS was increased in men (Δ3.0 ± 1.1 ms mmHg− 1, P = 0.03) but was unchanged in women (Δ-0.04 ± 1.0 ms mmHg− 1, P = 0.97). In addition, RMSSD and HF power of heart rate variability increased in women (Δ7.4 ± 2.6 ms, P = 0.02; Δ373.4 ± 197.3 ms2; P = 0.04, respectively) and further increased in men (Δ26.4 ± 7.1 ms, P < 0.01; Δ1874.9 ± 756.2 ms2; P = 0.02, respectively). Arterial blood pressure increased from rest during handgrip exercise and remained elevated during PEI in both groups, however, these responses were attenuated in women.

Conclusions

These findings allow us to suggest a sex-related difference in spontaneous cBRS elicited by isolated muscle metaboreflex activation in healthy humans.

Keyword

Exercise pressor reflex Autonomic nervous system Heart rate Blood pressure Sex differences 

Abbreviations

ANOVA

Analyses of variance

BMI

Body mass index

BSA

Body surface area

cBRS

Cardiac baroreflex sensitivity

CI

Cardiac index

CO

Cardiac output

DBP

Diastolic blood pressure

HF

High frequency

HR

Heart rate

HRV

Heart rate variability

ICC

Intraclass correlation coefficient

IHG

Isometric handgrip

LF

Low frequency

MBP

Mean blood pressure

MVC

Maximal voluntary contraction

NK1-R

Neurokinin-1 receptor

NTS

Nucleus tractus solitaries

PEI

Post-exercise ischemia

RMSSD

Root of the mean of the sum of successive differences

SBP

Systolic blood pressure

SV

Stroke volume

TVC

Total vascular conductance

TVCI

Vascular conductance index

VLF

Very low frequency

Notes

Acknowledgements

The time and effort expended by all the volunteer subjects is greatly appreciated.

Author contributions

MS and LCV conceived and designed research. MS, ALT, JLSC and LCV performed experiments. MS, ALT and LCV analyzed data. MS, ALT and LCV interpreted results of experiments. MS prepared figures. MS, ALT and LCV drafted manuscript. All authors read and approved final version of manuscript.

Funding

This study was supported by grants and scholarships from the Brazilian National Council of Scientific and Technological Development (CNPq), the Foundation for Research Support of Federal District (FAPDF), Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES) and partially supported by an American Physiological Society Arthur C. Guyton Awards for Excellence in Integrative Physiology (to L.C. Vianna).

Compliance with ethical standards

Conflict of interest

None of the authors declares a conflict of interest.

References

  1. (1996) Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Circulation 93(5):1043–1065Google Scholar
  2. Abdel-Rahman AR, Merrill RH, Wooles WR (1994) Gender-related differences in the baroreceptor reflex control of heart rate in normotensive humans. J Appl Physiol (1985) 77(2):606–613CrossRefGoogle Scholar
  3. Antonino D, Teixeira AL, Maia-Lopes PM, Souza MC, Sabino-Carvalho JL, Murray AR, Deuchars J, Vianna LC (2017) Non-invasive vagus nerve stimulation acutely improves spontaneous cardiac baroreflex sensitivity in healthy young men: A randomized placebo-controlled trial. Brain Stimul 10(5):875–881.  https://doi.org/10.1016/j.brs.2017.05.006 CrossRefPubMedGoogle Scholar
  4. Beske SD, Alvarez GE, Ballard TP, Davy KP (2001) Gender difference in cardiovagal baroreflex gain in humans. J Appl Physiol (1985) 91(5):2088–2092CrossRefGoogle Scholar
  5. Carrington CA, White MJ (2001) Exercise-induced muscle chemoreflex modulation of spontaneous baroreflex sensitivity in man. J Physiol 536(Pt 3):957–962CrossRefGoogle Scholar
  6. Chen CY, Bonham AC (2010) Postexercise hypotension: central mechanisms. Exerc Sport Sci Rev 38(3):122–127CrossRefGoogle Scholar
  7. Chen CY, Bechtold AG, Tabor J, Bonham AC (2009) Exercise reduces GABA synaptic input onto nucleus tractus solitarii baroreceptor second-order neurons via NK1 receptor internalization in spontaneously hypertensive rats. J Neurosci 29(9):2754–2761CrossRefGoogle Scholar
  8. Convertino VA (1998) Gender differences in autonomic functions associated with blood pressure regulation. Am J Physiol 275(6 Pt 2):R1909–R1920PubMedGoogle Scholar
  9. Cui J, Wilson TE, Shibasaki M, Hodges NA, Crandall CG (2001) Baroreflex modulation of muscle sympathetic nerve activity during posthandgrip muscle ischemia in humans. J Appl Physiol (1985) 91(4):1679–1686CrossRefGoogle Scholar
  10. Dipla K, Papadopoulos S, Zafeiridis A, Kyparos A, Nikolaidis MG, Vrabas IS (2013) Determinants of muscle metaboreflex and involvement of baroreflex in boys and young men. Eur J Appl Physiol 113(4):827–838CrossRefGoogle Scholar
  11. Du Bois D, Du Bois EF (1989) A formula to estimate the approximate surface area if height and weight be known. 1916. Nutrition 5(5):303–311 (discussion 312–303)PubMedGoogle Scholar
  12. Ettinger SM, Silber DH, Collins BG, Gray KS, Sutliff G, Whisler SK, McClain JM, Smith MB, Yang QX, Sinoway LI (1996) Influences of gender on sympathetic nerve responses to static exercise. J Appl Physiol (1985) 80(1):245–251CrossRefGoogle Scholar
  13. Fadel PJ, Raven PB (2012) Human investigations into the arterial and cardiopulmonary baroreflexes during exercise. Exp Physiol 97(1):39–50.  https://doi.org/10.1113/expphysiol.2011.057554 CrossRefPubMedGoogle Scholar
  14. Fisher JP, Young CN, Fadel PJ (2008) Effect of muscle metaboreflex activation on carotid-cardiac baroreflex function in humans. Am J Physiol Heart Circ Physiol 294(5):H2296–H2304.  https://doi.org/10.1152/ajpheart.91497.2007 CrossRefPubMedGoogle Scholar
  15. Fisher JP, Seifert T, Hartwich D, Young CN, Secher NH, Fadel PJ (2010) Autonomic control of heart rate by metabolically sensitive skeletal muscle afferents in humans. J Physiol 588(Pt 7):1117–1127.  https://doi.org/10.1113/jphysiol.2009.185470 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Fisher JP, Young CN, Fadel PJ (2015) Autonomic adjustments to exercise in humans. Compr Physiol 5(2):475–512.  https://doi.org/10.1002/cphy.c140022 CrossRefPubMedGoogle Scholar
  17. Hart EC, Charkoudian N (2014) Sympathetic neural regulation of blood pressure: influences of sex and aging. Physiol (Bethesda) 29(1):8–15.  https://doi.org/10.1152/physiol.00031.2013 CrossRefGoogle Scholar
  18. Hartwich D, Dear WE, Waterfall JL, Fisher JP (2011) Effect of muscle metaboreflex activation on spontaneous cardiac baroreflex sensitivity during exercise in humans. J Physiol 589(Pt 24):6157–6171.  https://doi.org/10.1113/jphysiol.2011.219964 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hartwich D, Aldred S, Fisher JP (2013) Influence of menstrual cycle phase on muscle metaboreflex control of cardiac baroreflex sensitivity, heart rate and blood pressure in humans. Exp Physiol 98(1):220–232.  https://doi.org/10.1113/expphysiol.2012.066498 CrossRefPubMedGoogle Scholar
  20. Hayward CS, Kelly RP (1997) Gender-related differences in the central arterial pressure waveform. J Am Coll Cardiol 30(7):1863–1871CrossRefGoogle Scholar
  21. Hopkins WG (2000) Measures of reliability in sports medicine and science. Sports Med 30(1):1–15CrossRefGoogle Scholar
  22. Huikuri HV, Pikkujamsa SM, Airaksinen KE, Ikaheimo MJ, Rantala AO, Kauma H, Lilja M, Kesaniemi YA (1996) Sex-related differences in autonomic modulation of heart rate in middle-aged subjects. Circulation 94(2):122–125CrossRefGoogle Scholar
  23. Ichinose M, Saito M, Wada H, Kitano A, Kondo N, Nishiyasu T (2002) Modulation of arterial baroreflex dynamic response during muscle metaboreflex activation in humans. J Physiol 544(Pt 3):939–948CrossRefGoogle Scholar
  24. Iellamo F, Massaro M, Raimondi G, Peruzzi G, Legramante JM (1999a) Role of muscular factors in cardiorespiratory responses to static exercise: contribution of reflex mechanisms. J Appl Physiol (1985) 86(1):174–180CrossRefGoogle Scholar
  25. Iellamo F, Pizzinelli P, Massaro M, Raimondi G, Peruzzi G, Legramante JM (1999b) Muscle metaboreflex contribution to sinus node regulation during static exercise: insights from spectral analysis of heart rate variability. Circulation 100(1):27–32CrossRefGoogle Scholar
  26. Jarvis SS, VanGundy TB, Galbreath MM, Shibata S, Okazaki K, Reelick MF, Levine BD, Fu Q (2011) Sex differences in the modulation of vasomotor sympathetic outflow during static handgrip exercise in healthy young humans. Am J Physiol Regul Integr Comp Physiol 301(1):20CrossRefGoogle Scholar
  27. Joyner MJ, Barnes JN, Hart EC, Wallin BG, Charkoudian N (2015) Neural control of the circulation: how sex and age differences interact in humans. Compr Physiol 5(1):193–215PubMedPubMedCentralGoogle Scholar
  28. Kaufman MP (2012) The exercise pressor reflex in animals. Exp Physiol 97(1):51–58.  https://doi.org/10.1113/expphysiol.2011.057539 CrossRefPubMedGoogle Scholar
  29. Mitchell JH (1990) J.B. Wolffe memorial lecture. Neural control of the circulation during exercise. Med Sci Sports Exerc 22(2):141–154CrossRefGoogle Scholar
  30. Mitchell JH, Kaufman MP, Iwamoto GA (1983) The exercise pressor reflex: its cardiovascular effects, afferent mechanisms, and central pathways. Annu Rev Physiol 45:229–242.  https://doi.org/10.1146/annurev.ph.45.030183.001305 CrossRefPubMedGoogle Scholar
  31. Notay K, Lee JB, Incognito AV, Seed JD, Arthurs AA, Millar PJ (2018) Muscle strength influences pressor responses to static handgrip in men and women. Med Sci Sports Exerc 50(4):778–784CrossRefGoogle Scholar
  32. Parati G, Di Rienzo M, Mancia G (2000) How to measure baroreflex sensitivity: from the cardiovascular laboratory to daily life. J Hypertens 18(1):7–19CrossRefGoogle Scholar
  33. Pelletier G, Liao N, Follea N, Govindan MV (1988) Mapping of estrogen receptor-producing cells in the rat brain by in situ hybridization. Neurosci Lett 94(1–2):23–28CrossRefGoogle Scholar
  34. Potts JT (2006) Inhibitory neurotransmission in the nucleus tractus solitarii: implications for baroreflex resetting during exercise. Exp Physiol 91(1):59–72.  https://doi.org/10.1113/expphysiol.2005.032227 CrossRefPubMedGoogle Scholar
  35. Potts JT, Mitchell JH (1998) Rapid resetting of carotid baroreceptor reflex by afferent input from skeletal muscle receptors. Am J Physiol 275(6 Pt 2):H2000–H2008PubMedGoogle Scholar
  36. Potts JT, Shi XR, Raven PB (1993) Carotid baroreflex responsiveness during dynamic exercise in humans. Am J Physiol 265(6 Pt 2):H1928–H1938PubMedGoogle Scholar
  37. Raven PB, Fadel PJ, Ogoh S (2006) Arterial baroreflex resetting during exercise: a current perspective. Exp Physiol 91(1):37–49.  https://doi.org/10.1113/expphysiol.2005.032250 CrossRefPubMedGoogle Scholar
  38. Rowell LB, O’Leary DS (1990) Reflex control of the circulation during exercise: chemoreflexes and mechanoreflexes. J Appl Physiol (1985) 69(2):407–418CrossRefGoogle Scholar
  39. Sabino-Carvalho JL, Teixeira AL, Samora M, Daher M, Vianna LC (2018) Blunted cardiovascular responses to exercise in Parkinson’s disease patients: role of the muscle metaboreflex. J Neurophysiol 120(4):1516–1524CrossRefGoogle Scholar
  40. Sala-Mercado JA, Ichinose M, Hammond RL, Ichinose T, Pallante M, Stephenson LW, O’Leary DS, Iellamo F (2007) Muscle metaboreflex attenuates spontaneous heart rate baroreflex sensitivity during dynamic exercise. Am J Physiol Heart Circ Physiol 292(6):H2867–H2873.  https://doi.org/10.1152/ajpheart.00043.2007 CrossRefPubMedGoogle Scholar
  41. Sheehan D, Mulholland JH, Safiroff B (1941) Surgical anatomy of the carotid sinus nerve. Anat Rec 80:431–442CrossRefGoogle Scholar
  42. Sheriff DD, O’Leary DS, Scher AM, Rowell LB (1990) Baroreflex attenuates pressor response to graded muscle ischemia in exercising dogs. Am J Physiol 258(2 Pt 2):H305–H310.  https://doi.org/10.1152/ajpheart.1990.258.2.H305 CrossRefPubMedGoogle Scholar
  43. Simonian SX, Herbison AE (1997) Differential expression of estrogen receptor and neuropeptide Y by brainstem A1 and A2 noradrenaline neurons. Neuroscience 76(2):517–529CrossRefGoogle Scholar
  44. Smith JR, Broxterman RM, Hammer SM, Alexander AM, Didier KD, Kurti SP, Barstow TJ, Harms CA (2016) Sex differences in the cardiovascular consequences of the inspiratory muscle metaboreflex. Am J Physiol Regul Integr Comp Physiol 311(3):3CrossRefGoogle Scholar
  45. Spaak J, Sundblad P, Linnarsson D (1998) Human carotid baroreflex during isometric lower arm contraction and ischemia. Am J Physiol 275(3 Pt 2):H940–H945PubMedGoogle Scholar
  46. Teixeira AL, Daher M, Souza MC, Ramos PS, Fisher JP, Vianna LC (2018a) Sympathetically mediated cardiac responses to isolated muscle metaboreflex activation following exercise are modulated by body position in humans. Am J Physiol Heart Circ Physiol 314(3):H593–H602PubMedGoogle Scholar
  47. Teixeira AL, Ramos PS, Samora M, Sabino-Carvalho JL, Ricardo DR, Colombari E, Vianna LC (2018b) GABAergic contribution to the muscle mechanoreflex-mediated heart rate responses at the onset of exercise in humans. Am J Physiol Heart Circ Physiol 314(4):H716–H723CrossRefGoogle Scholar
  48. Teixeira AL, Ritti-Dias R, Antonino D, Bottaro M, Millar PJ, Vianna LC (2018c) Sex differences in cardiac baroreflex sensitivity after isometric handgrip exercise. Med Sci Sports Exerc 50(4):770–777CrossRefGoogle Scholar
  49. Vianna LC, Fernandes IA, Barbosa TC, Teixeira AL, Nobrega ACL (2018) Capsaicin-based analgesic balm attenuates the skeletal muscle metaboreflex in healthy humans. J Appl Physiol 125(2):362–368CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Milena Samora
    • 1
  • André L. Teixeira
    • 1
  • Jeann L. Sabino-Carvalho
    • 1
  • Lauro C. Vianna
    • 1
  1. 1.NeuroVASQ-Integrative Physiology Laboratory, Faculty of Physical EducationUniversity of Brasília, Darcy Ribeiro CampusBrasíliaBrazil

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