Skip to main content
SpringerLink
Log in

Vasoconstriction during non-hypotensive hypovolemia is not associated with activation of baroreflex: A causality-based approach

  • Organ Physiology
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

Non-hypotensive hypovolemia simulated with oscillatory lower body negative pressure in the range of -10 to -20 mmHg is associated with vasoconstriction {increase in total peripheral vascular resistance (TPVR)}. Due to the mechanical stiffening of vessels, there is a disjuncture of mechano-neural coupling at the level of arterial baroreceptors which has not been investigated. The study was designed to quantify both the cardiac and vascular arms of the baroreflex using an approach based on Wiener-Granger causality (WGC) – partial directed coherence (PDC). Thirty-three healthy human volunteers were recruited and continuous heart rate and blood pressure {systolic (SBP), diastolic (DBP), and mean (MBP)} were recorded. The measurements were taken in resting state, at -10 mmHg (level 1) and -15 mmHg (level 2). Spectral causality - PDC was estimated from the MVAR model in the low-frequency band using the GMAC MatLab toolbox. PDC from SBP and MBP to RR interval and TPVR was calculated. The PDC from MBP to RR interval showed no significant change at -10 mmHg and -15 mmHg. No significant change in PDC from MBP to TPVR at -10 mmHg and -15 mmHg was observed. Similar results were obtained for PDC estimation using SBP as input. However, a significant increase in TPVR from baseline at both levels of oscillatory LBNP (p-value <0.001). No statistically significant change in PDC from blood pressure to RR interval and blood pressure to TPVR implies that vasoconstriction is not associated with activation of the arterial baroreflex in ≤-15 mmHg LBNP. Thereby, indicating the role of cardiopulmonary reflexes during the low level of LBNP simulated non-hypotensive hypovolemia.

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

Access this article

Log in via an institution

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
Fig. 4

Similar content being viewed by others

Data availability

The data underlying this article will be shared on reasonable request to the corresponding author.

References

  1. Aletti F, Ferrario M, Xu D, Greaves DK, Shoemaker JK, Arbeille P, Baselli G, Hughson RL (2012) Short-term variability of blood pressure: Effects of lower-body negative pressure and long-duration bed rest. Amer J Physiol Regul Integr Comp Physiol 303(1):R77–R85. https://doi.org/10.1152/ajpregu.00050.2012

    Article  CAS  Google Scholar 

  2. Barbieri R, Triedman JK, Saul JP (2002) Heart rate control and mechanical cardiopulmonary coupling to assess central volume: A systems analysis. Amer J Physiol Regul Integr Comp Physiol 283(5):R1210–R1220. https://doi.org/10.1152/ajpregu.00127.2002

    Article  Google Scholar 

  3. Chicharro D (2011) On the spectral formulation of Granger causality. Biological Cybernetics 105(5–6):331–347. https://doi.org/10.1007/s00422-011-0469-z

    Article  CAS  PubMed  Google Scholar 

  4. Convertino VA, Koons NJ, Suresh MR (2021) Physiology of Human Hemorrhage and Compensation. Compr Physiol 11(1):1531–1574. https://doi.org/10.1002/cphy.c200016

    Article  PubMed  Google Scholar 

  5. Convertino VA, Rickards CA, Ryan KL (2012) Autonomic mechanisms associated with heart rate and vasoconstrictor reserves. Clin Auton Res 22(3):123–130. https://doi.org/10.1007/s10286-011-0151-5

    Article  PubMed  Google Scholar 

  6. Cooke WH, Hoag JB, Crossman AA, Kuusela TA, Tahvanainen KUO, Eckberg DL (1999) Human responses to upright tilt: A window on central autonomic integration. J Physiol 517(2):617–628. https://doi.org/10.1111/j.1469-7793.1999.0617t.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Cooke WH, Ryan KL, Convertino VA (2004) Lower body negative pressure as a model to study progression to acute hemorrhagic shock in humans. J App Physiol 96(4):1249–1261. https://doi.org/10.1152/japplphysiol.01155.2003

    Article  Google Scholar 

  8. Dawson EA, Secher NH, Dalsgaard MK, Ogoh S, Yoshiga CC, González-Alonso J, Steensberg A, Raven PB (2004) Standing up to the challenge of standing: A siphon does not support cerebral blood flow in humans. Amer J Physiol Regul Integr Comp Physiol 287(4):R911–R914. https://doi.org/10.1152/ajpregu.00196.2004

    Article  CAS  Google Scholar 

  9. Franke WD, Johnson CP, Steinkamp JA, Wang R, Halliwill JR (2003) Cardiovascular and autonomic responses to lower body negative pressure. Clin Auton Res 13(1):36–44. https://doi.org/10.1007/s10286-003-0066-x

    Article  PubMed  Google Scholar 

  10. Fu Q, Shibata S, Hastings JL, Prasad A, Palmer MD, Levine BD (2009) Evidence for unloading arterial baroreceptors during low levels of lower body negative pressure in humans. Amer J Physiol Heart Circ Physiol 296(2):H480–H488. https://doi.org/10.1152/ajpheart.00184.2008

    Article  CAS  Google Scholar 

  11. Furlan R, Jacob G, Palazzolo L, Rimoldi A, Diedrich A, Harris PA, Porta A, Malliani A, Mosqueda-Garcia R, Robertson D (2001) Sequential Modulation of Cardiac Autonomic Control Induced by Cardiopulmonary and Arterial Baroreflex Mechanisms. Circulation 104(24):2932–2937. https://doi.org/10.1161/hc4901.100360

    Article  CAS  PubMed  Google Scholar 

  12. Hinojosa-Laborde C, Howard JT, Mulligan J, Grudic GZ, Convertino VA (2016) Comparison of compensatory reserve during lower-body negative pressure and hemorrhage in nonhuman primates. Amer J Physiol Regul Integr Comp Physiol 310(11):R1154–R1159. https://doi.org/10.1152/ajpregu.00304.2015

    Article  Google Scholar 

  13. Hinojosa-Laborde C, Rickards CA, Ryan KL Convertino VA (2011) Heart rate variability during simulated hemorrhage with lower body negative pressure in high and low tolerant subjects. Front Physiol 2:85. https://doi.org/10.3389/fphys.2011.00085

  14. Hisdal J, Toska K, Flatebø T, Walløe L (2002) Onset of mild lower body negative pressure induces transient change in mean arterial pressure in humans. Europ J App Physiol 87(3):251–256. https://doi.org/10.1007/s00421-002-0630-4

    Article  Google Scholar 

  15. Hisdal J, Toska K, Walløe L (2001) Beat-to-beat cardiovascular responses to rapid, low-level LBNP in humans. Amer J Physiol Regul Integr Comp Physiol 281(1):R213–R221. https://doi.org/10.1152/ajpregu.2001.281.1.R213

    Article  CAS  Google Scholar 

  16. Johnson BD, van Helmond N, Curry TB, van Buskirk CM, Convertino VA, Joyner MJ (2014) Reductions in central venous pressure by lower body negative pressure or blood loss elicit similar hemodynamic responses. J App Physiol 117(2):131–141. https://doi.org/10.1152/japplphysiol.00070.2014

    Article  CAS  Google Scholar 

  17. Johnson JM, Rowell LB, Niederberger M, Eisman MM (1974) Human Splanchnic and Forearm Vasoconstrictor Responses to Reductions of Right Atrial and Aortic Pressures. Circ Res 34(4):515–524. https://doi.org/10.1161/01.RES.34.4.515

    Article  CAS  PubMed  Google Scholar 

  18. Korzeniewska A, Mańczak M, Kamiński M, Blinowska KJ, Kasicki S (2003) Determination of information flow direction among brain structures by a modified directed transfer function (dDTF) method. J Neurosci Methods 125(1–2):195–207. https://doi.org/10.1016/S0165-0270(03)00052-9

    Article  PubMed  Google Scholar 

  19. Krohova J, Faes L, Czippelova B, Pernice R, Turianikova Z, Wiszt R, Mazgutova N, Busacca A, Javorka M (2020) Vascular resistance arm of the baroreflex: Methodology and comparison with the cardiac chronotropic arm. J App Physiol 128(5):1310–1320. https://doi.org/10.1152/japplphysiol.00512.2019

    Article  CAS  Google Scholar 

  20. Kwiatkowski D, Phillips PCB, Schmidt P, Shin Y (1992) Testing the null hypothesis of stationarity against the alternative of a unit root. J Econ 54(1–3):159–178. https://doi.org/10.1016/0304-4076(92)90104-Y

    Article  Google Scholar 

  21. László Z, Rössler A, Hinghofer-Szalkay HG (2001) Cardiovascular and hormonal changes with different angles of head-up tilt in men. Physiol Res 50(1):71–82

    PubMed  Google Scholar 

  22. Matzen S, Knigge U, Schütten HJ, Warberg J, Secher NH (1990) Atrial natriuretic peptide during head-up tilt induced hypovolaemic shock in man. Acta Physiol Scand 140(2):161–166. https://doi.org/10.1111/j.1748-1716.1990.tb08987.x

    Article  CAS  PubMed  Google Scholar 

  23. Millar PJ, Murai H, Morris BL, Floras JS (2013) Microneurographic evidence in healthy middle-aged humans for a sympathoexcitatory reflex activated by atrial pressure. Amer J Physiol Heart Circ Physiol 305(6):H931–H938. https://doi.org/10.1152/ajpheart.00375.2013

    Article  CAS  Google Scholar 

  24. Nollo G, Faes L, Porta A, Antolini R, Ravelli F (2005) Exploring directionality in spontaneous heart period and systolic pressure variability interactions in humans: Implications in the evaluation of baroreflex gain. Amer J Physiol Heart Circ Physiol 288(4):H1777–H1785. https://doi.org/10.1152/ajpheart.00594.2004

    Article  CAS  Google Scholar 

  25. Porta A, Bassani T, Bari V, Tobaldini E, Takahashi ACM, Catai AM, Montano N (2012) Model-based assessment of baroreflex and cardiopulmonary couplings during graded head-up tilt. Comput Biol Med 42(3):298–305. https://doi.org/10.1016/j.compbiomed.2011.04.019

    Article  PubMed  Google Scholar 

  26. Porta A, Faes L (2016) Wiener-Granger Causality in Network Physiology With Applications to Cardiovascular Control and Neuroscience. Proc IEEE 104(2):282–309. https://doi.org/10.1109/JPROC.2015.2476824

    Article  Google Scholar 

  27. Porta A, Marchi A, Bari V, De Maria B, Esler M, Lambert E, Baumert M (2017) Assessing the strength of cardiac and sympathetic baroreflex controls via transfer entropy during orthostatic challenge. Philos Trans Royal Soc A 375(2096):20160290. https://doi.org/10.1098/rsta.2016.0290

    Article  Google Scholar 

  28. Rea RF, Hamdan M, Clary MP, Randels MJ, Dayton PJ, Strauss RG (1991) Comparison of muscle sympathetic responses to hemorrhage and lower body negative pressure in humans. J App Physiol 70(3):1401–1405. https://doi.org/10.1152/jappl.1991.70.3.1401

    Article  CAS  Google Scholar 

  29. Rosenberg AJ, Kay VL, Anderson GK, Sprick JD, Rickards CA (2021) A comparison of protocols for simulating hemorrhage in humans: step versus ramp lower body negative pressure. J Appl Physiol 130(2) 380–389. https://doi.org/10.1152/japplphysiol.00230.2020

  30. Saitoh T, Ogawa Y, Aoki K, Shibata S, Otsubo A, Kato J, Iwasaki K (2008) Bell-shaped relationship between central blood volume and spontaneous baroreflex function. Auton Neurosci 143(1–2):46–52. https://doi.org/10.1016/j.autneu.2008.07.011

    Article  PubMed  Google Scholar 

  31. Schadt JC, Ludbrook J (1991) Hemodynamic and neurohumoral responses to acute hypovolemia in conscious mammals. Amer J Physiol 260(2 Pt 2):H305–318. https://doi.org/10.1152/ajpheart.1991.260.2.H305

  32. Tanaka H, Sjöberg BJ, Thulesius O (1996) Cardiac output and blood pressure during active and passive standing. Clin Physiol 16(2):157–170. https://doi.org/10.1111/j.1475-097X.1996.tb00565.x

    Article  CAS  PubMed  Google Scholar 

  33. Victor RG, Leimbach WN (1987) Effects of lower body negative pressure on sympathetic discharge to leg muscles in humans. J App Physiol 63(6):2558–2562. https://doi.org/10.1152/jappl.1987.63.6.2558

    Article  CAS  Google Scholar 

  34. Wesseling KH, Jansen JR, Settels JJ, Schreuder JJ (1993) Computation of aortic flow from pressure in humans using a nonlinear, three-element model. J App Physiol 74(5):2566–2573. https://doi.org/10.1152/jappl.1993.74.5.2566

    Article  CAS  Google Scholar 

  35. Xiang L, Hinojosa-Laborde C, Ryan KL, Rickards CA, Convertino VA (2018) Time course of compensatory physiological responses to central hypovolemia in high- and low-tolerant human subjects. Amer J Physiol Regul Integr Comp Physiol 315(2):R408–R416. https://doi.org/10.1152/ajpregu.00361.2017

    Article  CAS  Google Scholar 

  36. Yadav K (2022) ‘To study the mechanism of altered spontaneous baroreflex sensitivity’, PhD thesis, All India Institute of Medical Sciences, New Delhi

  37. Zoller RP, Mark AL, Abboud FM, Schmid PG, Heistad DD (1972) The role of low pressure baroreceptors in reflex vasoconstrictor responses in man. J Clin Investig 51(11):2967–2972. https://doi.org/10.1172/JCI107121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

Not applicable (No Funding taken for the study)

Author information

Authors and Affiliations

  1. Department of Physiology, All India Institute of Medical Sciences, New Delhi, 110029, India

    Mansi Jain, Dinu S Chandran, Ashok Kumar Jaryal & K. K. Deepak

  2. Department of Physiology, All India Institute of Medical Sciences, Rajkot, India

    Vinay Chitturi

Authors
  1. Mansi Jain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vinay Chitturi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dinu S Chandran
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ashok Kumar Jaryal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. K. K. Deepak
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Dr Mansi Jain: This author helped with intellectual content, study design, data collection, writing and editing all sections of manuscript, and approving manuscript for publication

Dr Vinay Chitturi: This author helped with intellectual content, study design, data collection, writing and editing all sections of manuscript, and approving manuscript for publication

Dr Dinu S Chandran: This author helped with intellectual content, study design, data collection, writing and editing all sections of manuscript, and approving manuscript for publication

Dr Ashok Kumar Jaryal: This author helped with intellectual content, study design, data collection, writing and editing all sections of manuscript, and approving manuscript for publication

Dr KK Deepak: This author helped with intellectual content, study design, data collection, writing and editing all sections of manuscript, and approving manuscript for publication

Corresponding author

Correspondence to K. K. Deepak.

Ethics declarations

Ethical approval

Ethical approval from Institute Ethics Committee was taken - IECPG-510/23.09.2020, RT-43/21.10.2020

Consent to articipate

Informed consent was taken before the start of recording

Consent to publish

Informed consent was taken before the start of recording for scientific publishing of data.

Competing interests

None of the authors has any conflicts of interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jain, M., Chitturi, V., Chandran, D.S. et al. Vasoconstriction during non-hypotensive hypovolemia is not associated with activation of baroreflex: A causality-based approach. Pflugers Arch - Eur J Physiol 475, 747–755 (2023). https://doi.org/10.1007/s00424-023-02811-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-023-02811-1

Keywords

Search

Navigation