Advertisement

Wiener klinische Wochenschrift

, Volume 128, Issue 13–14, pp 504–512 | Cite as

Cardiovagal and adrenergic function tests in unilateral carotid artery stenosis patients—a Valsalva manoeuvre tool to show an autonomic dysfunction?

  • Viktor Švigelj
  • Matjaž Šinkovec
  • Viktor Avbelj
  • Roman Trobec
  • Ludovit Gaspar
  • Daniel Petrovič
  • Peter Kruzliak
original article
  • 117 Downloads

Summary

Background

The stability of an arterial baroreflex depends also upon the integrity of the afferent limb. For its quantification, we can use a noninvasive test such as baroreceptor sensitivity estimation during Valsalva manoeuvre. The aim of this study was to evaluate potential autonomic dysfunction in patients with unilateral severe carotid disease and compare the results to the results obtained from an age and gender matched group of healthy volunteers.

Methods

We evaluated dynamic changes during Valsalva manoeuvre (Valsalva ratio, cardiovagal and adrenergic baroreceptor sensitivity, sympathetic indexes and its dynamic ranges) in 41 patients (29 males; 62.9 ± 7.4 years) and compared the results to results obtained from volunteers (62.8 ± 7.0 years).

Results

Valsalva ratio between the patients and control group revealed no significant difference, as well as cardiovagal and adrenergic baroreceptor sensitivity. Sympathetic indexes, except for sympathetic index 2, reflecting the sympathetic vasoconstrictor baroreceptor response in late phase 2 of Valsalva manoeuvre (7.1 ± 13.1 mmHg in patients vs. 11.4 ± 10.2 mmHg in control group; p = 0.012) showed no significant differences between the studied groups. The most prominent dynamic range between the groups was within the sympathetic index 2.

Conclusion

With some Valsalva manoeuvre test results, we were not able to show severe autonomic dysfunction in unilateral severe carotid stenosis patients except for lower vasoconstriction response within the late phase 2 of the manoeuvre.

Keywords

Autonomic nervous system disorders Baroreflex Valsalva manoeuvre Carotid artery stenosis Carotid sinus 

Notes

Compliance with ethical standards

Conflict of interest

V. Švigelj, M. Šinkovec, V. Avbelj, R. Trobec, L. Gaspar, D. Petrovič, and P. Kruzliak declare that there are no actual or potential conflicts of interest in relation to this article.

References

  1. 1.
    Isaka Y, Nagano K, Narita M, Ashida K, Imaizumi M. High signal intensity on T2-Weighted magnetic resonance imaging and cerebral hemodynamic reserve in carotid occlusive disease. Stroke. 1997;28(2):354–7.CrossRefPubMedGoogle Scholar
  2. 2.
    Neff KW, Horn P, Dinter D, Vajkoczy P, Schmiedek P, Düber C. Extracranial–intracranial arterial bypass surgery improves total brain blood supply in selected symptomatic patients with unilateral internal carotid artery occlusion and insufficient collateralization. Neuroradiology. 2004;46(9):730–7.CrossRefPubMedGoogle Scholar
  3. 3.
    Jongen LM, van der Worp HB, Waaijer A, van der Graaf Y, Mali WPTM. Interrelation between the degree of carotid stenosis, collateral circulation and cerebral perfusion. Cerebrovasc Dis. 2010;30(3):277–4.CrossRefPubMedGoogle Scholar
  4. 4.
    Roffi M, Sievert H, GrayWA, et al. Carotid artery stenting versus surgery: adequate comparisons? Lancet Neurol. 2010;9(4):339–41.CrossRefPubMedGoogle Scholar
  5. 5.
    Brott TG, Hobson RW, Howard G, et al. Stenting versus endarterectomy for treatment of carotid-artery stenosis. N Engl J Med. 2010;363(1):11–23.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Coutts SB, Hill MD, Hu WY. Hyperperfusion syndrome: toward a stricter definition. Neurosurgery. 2003;53(5):1053–8.CrossRefPubMedGoogle Scholar
  7. 7.
    Karapanayiotides T, Meuli R, Devuyst G, et al. Postcarotid endarterectomy hyperperfusion or reperfusion syndrome. Stroke. 2005;36(1):21–6.CrossRefPubMedGoogle Scholar
  8. 8.
    Bouri S, Thapar A, Shalhoub J, et al. Hypertension and the post-carotid endarterectomy cerebral Hyperperfusion Syndrome. Eur J Vasc Endovasc Surg. 2011;41(2):229–37.CrossRefPubMedGoogle Scholar
  9. 9.
    van Mook WN, Rennenberg RJ, Schurink GW, et al. Cerebral hyperperfusion syndrome. Lancet Neurol. 2005;4(12):877–88.CrossRefPubMedGoogle Scholar
  10. 10.
    Ogasawara K, Mikami C, Inoue T, Ogawa A. Delayed cerebral hyperperfusion syndrome caused by prolonged impairment of cerebrovascular autoregulation after carotid endarterectomy: case report. Neurosurgery. 2004;54(5):1258–62.CrossRefPubMedGoogle Scholar
  11. 11.
    Canovas D, Estela J, Perendreu J, et al. Cerebral hyperperfusion syndrome after angioplasty. In: Forbes T, editor. Angioplasty, various techniques and challenges in treatment of congenital and acquired vascular stenoses. Rijeka: InTech; 2012. p. 9–40.Google Scholar
  12. 12.
    Švigelj V, Šinkovec M, Avbelj V, Trobec R. Simple cardiovagal and adrenergic function tests in carotid artery stenosis patients as a potential tool for determining a transient autonomic dysfunction. Clin Auton Res. 2015;25(6):383–90.CrossRefPubMedGoogle Scholar
  13. 13.
    Švigelj V, Šinkovec M, Avbelj V, Trobec R. Can we predict complications after elective carotid artery angioplasty and stenting with a simple Valsalva test? Signa Vitae. 2015;10(1):93–102.Google Scholar
  14. 14.
    Benarroch EE, Opfer-Gehrking TL, Low PA. Use of the photoplethysmographic technique to analyze the Valsalva maneuver in normal man. Muscle Nerve. 1991;14(12):1165–72.CrossRefPubMedGoogle Scholar
  15. 15.
    Denq J-C, O’Brien PC, Low PA. Normative data on phases of Valsalva maneuver. J Clin Neurophysiol. 1998;15(6):535–40.CrossRefPubMedGoogle Scholar
  16. 16.
    Low PA, Tomalia VA, Park KJ. Autonomic function: some clinical aplications. J Clin Neurol. 2013;9:1–8.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Vogel ER, Sandroni P, Low PA. Blood pressure recovery from Valsalva maneuver in patients with autonomic failure. Neurology. 2005;65:1533–7.CrossRefPubMedGoogle Scholar
  18. 18.
    Schrezenmaier C, Singer W, Muenter Swift N, Sletten D, Tanabe J, Low PA. Adrenergic and vagal baroreflex sensitivity in autonomic failure. Arch Neurol. 2007;64:381–6.CrossRefPubMedGoogle Scholar
  19. 19.
    Eckberg DL, Rea RF, Andersson OK, et al. Baroreflex modulation of sympathetic activity and sympathetic neurotransmitters in humans. Acta Physiol Scand. 1988;133(2):221–31.CrossRefPubMedGoogle Scholar
  20. 20.
    Rudas L, Crossman AA, Morillo CA, et al. Sympathetic and vagal baroreflex responses to sequential nitroprusside and phenylephrine. Am J Physiol. 1999;276(5 Pt 2):H1691–8.PubMedGoogle Scholar
  21. 21.
    Hilz MJ, Dütsch M. Quantitative studies of autonomic function. Muscle Nerve. 2006;33(1):6–20.CrossRefPubMedGoogle Scholar
  22. 22.
    Kirchheim HR. Systemic arterial baroreceptor reflexes. Physiol Rev. 1976;56(1):100–77.PubMedGoogle Scholar
  23. 23.
    Korner PI, Tonkin AM, Uther JB. Reflex and mechanical circulatory effects of graded Valsalva maneuvers in normal man. J Appl Physiol. 1976;40(3):434–40.PubMedGoogle Scholar
  24. 24.
    Sandroni P, Benarroch E, Low P. Pharmacological dissection of components of the Valsalva maneuver in adrenergic failure. J Appl Physiol. 1991;71(4):1563–7.PubMedGoogle Scholar
  25. 25.
    Smith ML, Beightol LA, Fritsch-Yelle JM, et al. Valsalva’s maneuver revisited: a quantitative method yielding insights into human autonomic control. Am J Physiol. 1996;271(3 Pt 2):H1240–9.PubMedGoogle Scholar
  26. 26.
    Novak P. Assessment of sympathetic index from Valsalva maneuver. Neurology. 2011;76(23):2010–16.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Le Winter MM. Normal physiology of the cardiovascular system. In: Fuster V, Alexander W, Wellens GJJ, editors. Hurst’s The Heart. 10th edn. New York: McGraw-Hill Coimpanies, Inc; 2001. p. 63–94.Google Scholar
  28. 28.
    Kjeldsen S, Feldman RD, Lisheng L, et al. Updated national and international hypertension guidelines: a review of current recommendations. Drugs. 2014;74(17):2033–51.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Pontus PB, DiRienzo M, Castiglioni P, et al. Time versus frequency domain techniques for assessing baroreflex sensitivity. J Hypertens. 2001;19:1699–705.CrossRefGoogle Scholar
  30. 30.
    Weston PJ, James MA, Panerai R, et al. Abnormal baroreceptor-cardiac reflex sensitivity is not detected by conventional tests of autonomic function in patients with insulin-dependent diabetes mellitus. Clin Sci (Lon). 1996;91:59–64.CrossRefGoogle Scholar
  31. 31.
    Pitzalis MV, Mastropasqua F, Passantino A, et al. Comparison between noninvasive indices of baroreceptor sensitivity and the phenylephrine method in postmyocardial infarction patients. Circulation. 1998;97:1362–7.CrossRefPubMedGoogle Scholar
  32. 32.
    Pickering TG, Gribbin B, Sleight P. Comparison of the reflex heart rate response to rising and falling arterial pressure in man. Cardiovasc Res. 1972;6:277–83.CrossRefPubMedGoogle Scholar
  33. 33.
    Milic M, Sun P, Liu F, et al. A comparison of pharmacologic and spontaneous baroreflex methods in aging and hypertension. J Hypertens. 2009;27:1243–51.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Yakhou L, Constant I, Merle JC, Laude D, Becquemin JP, Duvaldestin P. Noninvasive investigation of autonomic activity after carotid stenting or carotid endarterectomy. J Vasc Surg. 2006;44:472–9.CrossRefPubMedGoogle Scholar
  35. 35.
    Bishop VS, Haywood JR, Shade RE, Siegel M, Hamm C. Aortic baroreceptor deafferentation in the baboon. J Appl Physiol. 1986;60:798–801.PubMedGoogle Scholar
  36. 36.
    Shade RE, Bishop VS, Haywood JR, Hamm CK. Cardiovascular and neuroendocrine responses to baroreceptor denervation in baboons. Am J Physiol. 1990;258:R930–8.PubMedGoogle Scholar
  37. 37.
    Huang C-C, Wu Y-S, Chen T, et al. Long-term effects of baroreflex function after stenting in patients with carotid artery stenosis. Auton Neurosci. 2010;158:100–4.CrossRefPubMedGoogle Scholar
  38. 38.
    Timmers HJ, Karemaker JM, Wieling W, Buskens FG, Lenders JW. Arterial barroreflex function after unilateral carotid endarterectomy. Clin Auton Res. 2001;11:188–9.Google Scholar
  39. 39.
    Gianaros PH, Jennings JR, Olafsson GB, et al. Greater intima-media thickness in the carotid bulb is associated with reduced baroreflex sensitivity. Am J Hypertens. 2002;15:486–91.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Soinne L, Helenius J, Tatlisumak T, et al. Cerebral hemodynamics in asymptomatic and symptomatic patients with high-grade carotid stenosis undergoing carotid endarterectomy. Stroke. 2003;34:1655–61.CrossRefPubMedGoogle Scholar
  41. 41.
    Henderson RD, Eliasziw M, Fox AJ, Rothwell PM, Barnett HJM. Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis. Stroke. 2000;31:128–32.CrossRefPubMedGoogle Scholar
  42. 42.
    Jongen LM, van der Worp HB, Waaijer A, van der Graaf Y, Mali WPTM. Interrelation between the degree of carotid stenosis, collateral circulation and cerebral perfusion. Cerebrovasc Dis. 2010;30:277–84.CrossRefPubMedGoogle Scholar
  43. 43.
    Ito K, Sasaki M, Kobayashi M, et al. Noninvasive evaluation of collateral blood flow through circle of Willis in cervical carotid stenosis using selective magnetic resonance angiography. J Stroke Cerebrovasc Dis. 2014;23:1019–23.CrossRefPubMedGoogle Scholar
  44. 44.
    Zhu G, Yuan Q, Yang J, Yeo J. Experimental study of hemodynamics in the Circle of Willis. Biomed Eng Online. 2015;14(Suppl 1):S10. doi: 10.1186/1475-925X-14-S1-S10.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Mense L, Reimann M, Rüdiger H, et al. Autonomic function and cerebral autoregulation in patients undergoing carotid endarterectomy. Circ J. 2010;74:2139–45.CrossRefPubMedGoogle Scholar
  46. 46.
    Dalla Vecchia L, Barbic F, Galli A, et al. Favorable effects of carotid endarterectomy on baroreflex sensitivity and cardiovascular neural modulation: a 4-month follow-up. Am J Physiol Regul Integr Comp Physiol. 2013;304:R1114–20.CrossRefPubMedGoogle Scholar
  47. 47.
    Demirci M, Saribaş O, Uluç K, Cekirge S, Böke E, Ay H. Carotid artery stenting and endarterectomy have different effects on heart rate variability. J Neurol Sci. 2006;241:45–51.CrossRefPubMedGoogle Scholar
  48. 48.
    Alici G, Ozkan B, Acar G, et al. Evaluation of autonomic functions by heart rate variability after stenting in patients with carotid artery stenosis. Ann Noninvasive Electrocardiol. 2013;18:126–9.CrossRefPubMedGoogle Scholar
  49. 49.
    Heathers JAJ. Everything Hertz: methodological issues in short-term frequency-domain HRV. Front Physiol. 2014;5:177.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Acampa M, Guideri F, Marotta G, et al. Autonomic activity and baroreflex sensitivity in patients submitted to carotid stenting. Neurosci Lett. 2011;491:221–6.51.CrossRefPubMedGoogle Scholar
  51. 51.
    Xiong L, Leung HW, Chen XY, et al. Autonomic dysfunction in ischemic stroke with carotid stenosis. Acta Neurol Scand. 2012;126:122–8.CrossRefPubMedGoogle Scholar
  52. 52.
    Akinola A, Mathias CJ, Mansfield A, et al. Cardiovascular, autonomic, and plasma catecholamine responses in unilateral and bilateral carotid artery stenosis. J Neurol Neurosurg Psychiatry. 1999;67:428–32.53.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Doux JD, Yun AJ. The link between carotid artery disease and ischemic stroke may be partially attributable to autonomic dysfunction and failure of cerebrovascular autoregulation triggered by Darwinian maladaptation of the carotid baroreceptors and chemoreceptors. Med Hypotheses. 2006;66:176–81.CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  • Viktor Švigelj
    • 1
  • Matjaž Šinkovec
    • 2
  • Viktor Avbelj
    • 3
  • Roman Trobec
    • 3
  • Ludovit Gaspar
    • 4
  • Daniel Petrovič
    • 5
  • Peter Kruzliak
    • 6
    • 7
  1. 1.Division of Neurology, Department of Vascular Neurology and Neurological Intensive Care, Neurological Intensive Care UnitUniversity Medical Centre LjubljanaLjubljanaSlovenia
  2. 2.Division of Internal Medicine, Department of CardiologyUniversity Medical Centre Ljubljana1525 LjubljanaSlovenia
  3. 3.Department of Communication SystemsJožef Stefan Institute1000 LjubljanaSlovenia
  4. 4.2nd Department of Internal Medicine, Faculty of MedicineComenius University and University HospitalBratislavaSlovak Republic
  5. 5.Institute of Histology and Embryology, Faculty of MedicineUniversity of Ljubljana1000 LjubljanaSlovenia
  6. 6.2nd Department of Internal Medicine, Faculty of MedicineMasaryk UniversityBrnoCzech Republic
  7. 7.Laboratory of Structural Biology and Proteomics, Faculty of PharmacyUniversity of Veterinary Medicine and Pharmaceutical SciencesBrnoCzech Republic

Personalised recommendations