Skip to main content
Log in

Stimulation of sympathetic activity by carbon dioxide in patients with autonomic failure compared to normal subjects

  • Research Paper
  • Published:
Clinical Autonomic Research Aims and scope Submit manuscript

Abstract

In vivo studies selectively assessing preganglionic and central autonomic nervous system activity in patients with autonomic failure have so far been limited to testing pituitary function. In animal experiments carbon dioxide (CO2) selectively stimulates central sympathetic nuclei in the ventrolateral medulla and preganglionic sympathetic neurons in the cervical trunk. This central stimulation seems to overrule less pronounced peripheral vasodilatatory effects. This study addressed the question of whether hypercapnea is a suitable challenge procedure to test preganglionic and central autonomic activity in healthy subjects and in patients with autonomic failure of preganglionic and central origin. Seven patients with multiple system atrophy (MSA) and 30 age-matched healthy volunteers underwent a protocol including a Valsalva manoeuvre (VM) under normo- and hypercapnic conditions and exposure to hypercapnea under supine resting conditions. Blood pressure (BP), heart rate (HR) and end-tidal CO2 partial pressure were measured continuously and non-invasively. In normal controls hypercapnea induced significantly higher BP values in phases II, IIe, III and IV of the VM compared to the normocapnic VM and a significant increase in BP during steady-state supine exposure compared to normocapnic baseline. HR increased significantly only after 40 s of steady-state hypercapnea during the latter challenge. In patients with MSA and autonomic failure, in whom a predominantly preganglionic lesion of the autonomic nervous system is established, no significant effects of hypercapnea on the cardiovascular parameters were found. Although this non-invasive challenge procedure cannot differentiate between pre- and postganglionic autonomic failure, exposure to hypercapnea enables the investigation of efferent autonomic activity to vasoconstrictors generated from autonomic centres in the brainstem and cervical trunk.

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.

Similar content being viewed by others

References

  1. Polinsky RJ, Brown RT, Lee GKet al. Beta-endorphin, ACTH and catecholamine response in chronic autonomic failure.Ann Neurol 1987;21(6):573–577.

    Google Scholar 

  2. Thomaides TN, Chaudhuri KR, Maule S, Watson L, Marsden CD, Mathias CJ. Growth hormone response to clonidine in central and peripheral autonomic failure.Lancet 1992;340:263–266.

    Google Scholar 

  3. Kaufmann H, Oribe E, Miller M, Knott P, Wiltshire-Clement M, Yahr MD. Hypotension induced vasopressin release distinguishes between pure autonomic failure and multiple system atrophy with autonomic failure.Neurology 1992;42(3 Pt 1):590–593.

    Google Scholar 

  4. Lioy F, Hanna BD, Polosa C. CO2 dependent component of the neurogenic vascular tone in the cat.Pflugers Arch 1978;374: 187–191.

    Google Scholar 

  5. Lioy F, Blinkhorn MT, Garneau C. Regional hemodynamic effects of changes in PaCO2 in the vagotomized, sino-aortic deafferented rat.J Auton Nerv System 1985;12:301–314.

    Google Scholar 

  6. Lioy F. Role of the ventrolateral medulla in the cardiovascular responses to changes in the carbon dioxide tension in the arterial blood.Prog Brain Res 1989;81:205–213.

    Google Scholar 

  7. Hoka S, Arimura H, Bosnjak ZJ, Kampine JP. Regional venous out-flow, blood volume and sympathetic nerve activity during hypercapnia and hypoxic hypercapnia.Can J Physiol Pharmacol 1992;7: 1032–1039.

    Google Scholar 

  8. Seller H, Konig S, Czachurski J. Chemosensitivity of sympathoexcitatory neurones in the rostroventrolateral medulla of the rat.Pflugers Arch 1990;416:735–741.

    Google Scholar 

  9. Dampney RA, Goodchild AK, Robertson LG, Montgomery W. Role of the ventrolateral medulla in vasomotor regulation: A correlative anatomical and physiological study.Brain Res 1982;249:223–235.

    Google Scholar 

  10. Anderson RJ, Rose JR, Berns AS, Erickson AL, Arnold PE. Mechanism of effect of hypercapnic acidosis on renin secretion in the dog.Am J Physiol 1980;238:F119-F125.

    Google Scholar 

  11. Wang BC, Sundet WD, Goetz KL. Vasopressin in plasma and cerebrospinal fluid of dogs during hypoxia or acidosis.Am J Physiol 1984;247:E449-E455.

    Google Scholar 

  12. Biesold D, Kurosawa M, Sato A, Trzebski A. Hypoxia and hypercapnia increase sympathoadrenal medullary functions in anaesthetized, artificially ventilated rats.Japanese J Physiol 1989;39: 511–522.

    Google Scholar 

  13. Accili EA, Puttaswamaiah S, Lioy F. Effects of carbon dioxide on hindlimb vascular resistance in the acute spinal cat.J Auton Nerv Syst 1988;23:87–94.

    Google Scholar 

  14. Rothe CF, Stein PM, MacAnespie CL, Gaddis M. Vascular capacitance responses to severe hypercapnia and hypoxia in dogs.Am J Physiol 1985;249:H1061-H1069.

    Google Scholar 

  15. Potter EK, McCloskey DI, Courtice GP. Effects of hypoxia, hypercapnia and acidemia on vagal action at the heart in the dog.J Auton Nerv Sys 1986;16:79–83.

    Google Scholar 

  16. Somers VK, Mark AL, Zavala DC, Abboud FM. Influence of ventilation and hypocapnia on sympathetic nerve responses to hypoxia in normal humans.J Appl Physiol 1989;67(5):2095–2100.

    Google Scholar 

  17. Braune S, Auer A, SchulteMonting J, Schwerbrock S, Lucking CH. Cardiovascular parameters: sensitivity to detect autonomic dysfunction and influence of age and sex in normal controls.Clin Autonom Res 1996;6:3–15.

    Google Scholar 

  18. Ziegler MG, Lake CR, Williams AC, Teychenne PF, Shoulson I, Steinsland O. Bromocriptine inhibits norepinephrine release.Clin Pharmacol Ther 1979;25(2):137–142.

    Google Scholar 

  19. Cavero I, Massingham R, Lefevre-Borg F. Peripheral dopamine receptors, potential targets for a new class of antihypertensive agents.Life Sci 1982;31:1050–1069.

    Google Scholar 

  20. Montastruc JL, Chamontin B, Rascol A. Parkinson's disease and hypertension: chronic bromocriptine treatment.Neurology 1985;35: 1644–1647.

    Google Scholar 

  21. Sachs C, Berglung B, Kaijser L. Autonomic cardiovascular responses in parkinsonism: effect of levodopa with dopa-decarboxylase inhibition.Acta Neurol Scand 1985:71:37–42.

    Google Scholar 

  22. Mesec A, Sega S, Kiauta T. The influence of the type, duration, severity and levodopa treatment of Parkinson's disease on cardiovascular autonomic response.Clin Autonom Res 1993;3:339–344.

    Google Scholar 

  23. van Dijk JG, Haan J, Zwinderman K, Kremer B, van Hilten BJ, Roos RAC. Autonomic nervous system dysfunction in Parkinson's disease: relationship with age, mediation, duration and severity.J Neurol Neurosurg Psychiat 1993;56:1090–1095.

    Google Scholar 

  24. Parati G, Casadei R, Gropelli A, Di Rienzo M, Mancia G. Comparison of finger and intra-arterial blood pressure monitoring in rest and during laboratory testing.Hypertension 1989;13:647–655.

    Google Scholar 

  25. Silke B, Spiers JP, Boyd E, Graham E, McParland G, Scott ME. Evaluation of non-invasive blood pressure measurement by the Finapres method at rest and during exercise in subjects with cardiovascular insufficiency.Clin Autonom Res 1994;4:49–56.

    Google Scholar 

  26. Young WL, Prohovnik I, Ornstein E, Ostapkovich N, Matteo RS. Cerebral blood flow reactivity to changes in carbon dioxide calculated using end-tidal versus arterial tensions.J Cereb Blood Flow Metab 1991;11:1031–1035.

    Google Scholar 

  27. Bennarroch EE, Opfer-Gehrking TL, Low PA. Use of the photoplethysmographic technique to analyze the Valsalva maneuver in normal man.Muscle Nerve 1991;14:1165–1172.

    Google Scholar 

  28. Braune S, Schulte-Monting J, Schwerbrock S, Lucking CH. Reproducibility of cardiovascular parameters in autonomic testing.J Auton Nerv Sys 1996;60:103–107.

    Google Scholar 

  29. Oppenheimer DR. Lateral horn cells in progressive autonomic fallure.J Neurol Sci 1980;46:393–404.

    Google Scholar 

  30. Gray F, Vincent D, Hauw JJ. Quantitative study of lateral horn cells in 15 cases of multiple system atrophy.Acta Neuropathol Berlin 1988;75:513–518.

    Google Scholar 

  31. Polinsky RJ, Kopin IJ, Ebert MW, Weise V. Pharmacologic distinction of different orthostatic hypotension syndromes.Neurology 1981;31:1–7.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Braune, S., Hetzel, A., Prasse, A. et al. Stimulation of sympathetic activity by carbon dioxide in patients with autonomic failure compared to normal subjects. Clinical Autonomic Research 7, 327–332 (1997). https://doi.org/10.1007/BF02267726

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02267726

Keywords

Navigation