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

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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.

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References

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  4. Roffi M, Sievert H, GrayWA, et al. Carotid artery stenting versus surgery: adequate comparisons? Lancet Neurol. 2010;9(4):339–41.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Coutts SB, Hill MD, Hu WY. Hyperperfusion syndrome: toward a stricter definition. Neurosurgery. 2003;53(5):1053–8.

    Article  PubMed  Google Scholar 

  7. Karapanayiotides T, Meuli R, Devuyst G, et al. Postcarotid endarterectomy hyperperfusion or reperfusion syndrome. Stroke. 2005;36(1):21–6.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  9. van Mook WN, Rennenberg RJ, Schurink GW, et al. Cerebral hyperperfusion syndrome. Lancet Neurol. 2005;4(12):877–88.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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. 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.

    Article  PubMed  Google Scholar 

  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. 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.

    Article  CAS  PubMed  Google Scholar 

  15. Denq J-C, O’Brien PC, Low PA. Normative data on phases of Valsalva maneuver. J Clin Neurophysiol. 1998;15(6):535–40.

    Article  CAS  PubMed  Google Scholar 

  16. Low PA, Tomalia VA, Park KJ. Autonomic function: some clinical aplications. J Clin Neurol. 2013;9:1–8.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Vogel ER, Sandroni P, Low PA. Blood pressure recovery from Valsalva maneuver in patients with autonomic failure. Neurology. 2005;65:1533–7.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  21. Hilz MJ, Dütsch M. Quantitative studies of autonomic function. Muscle Nerve. 2006;33(1):6–20.

    Article  PubMed  Google Scholar 

  22. Kirchheim HR. Systemic arterial baroreceptor reflexes. Physiol Rev. 1976;56(1):100–77.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  26. Novak P. Assessment of sympathetic index from Valsalva maneuver. Neurology. 2011;76(23):2010–16.

    Article  PubMed  PubMed Central  Google Scholar 

  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. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Pontus PB, DiRienzo M, Castiglioni P, et al. Time versus frequency domain techniques for assessing baroreflex sensitivity. J Hypertens. 2001;19:1699–705.

    Article  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  35. Bishop VS, Haywood JR, Shade RE, Siegel M, Hamm C. Aortic baroreceptor deafferentation in the baboon. J Appl Physiol. 1986;60:798–801.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  49. Heathers JAJ. Everything Hertz: methodological issues in short-term frequency-domain HRV. Front Physiol. 2014;5:177.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  51. Xiong L, Leung HW, Chen XY, et al. Autonomic dysfunction in ischemic stroke with carotid stenosis. Acta Neurol Scand. 2012;126:122–8.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Division of Neurology, Department of Vascular Neurology and Neurological Intensive Care, Neurological Intensive Care Unit, University Medical Centre Ljubljana, Zaloška 2, 1525, Ljubljana, Slovenia

    Viktor Švigelj

  2. Division of Internal Medicine, Department of Cardiology, University Medical Centre Ljubljana, Zaloška 2, 1525 Ljubljana, Slovenia

    Matjaž Šinkovec

  3. Department of Communication Systems, Jožef Stefan Institute, Jamova 39, 1000 Ljubljana, Slovenia

    Viktor Avbelj &  Roman Trobec

  4. 2nd Department of Internal Medicine, Faculty of Medicine, Comenius University and University Hospital, Mickiewiczova 13, 813 69, Bratislava, Slovak Republic

    Ludovit Gaspar

  5. Institute of Histology and Embryology, Faculty of Medicine, University of Ljubljana, Korytkova 2, 1000 Ljubljana, Slovenia

    Daniel Petrovič

  6. 2nd Department of Internal Medicine, Faculty of Medicine, Masaryk University, Pekarska 53, 656 91, Brno, Czech Republic

    Peter Kruzliak

  7. Laboratory of Structural Biology and Proteomics, Faculty of Pharmacy, University of Veterinary Medicine and Pharmaceutical Sciences, Brno, Czech Republic

    Peter Kruzliak

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  1. Viktor Švigelj
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Correspondence to Viktor Švigelj.

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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.

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Švigelj, V., Šinkovec, M., Avbelj, V. et al. Cardiovagal and adrenergic function tests in unilateral carotid artery stenosis patients—a Valsalva manoeuvre tool to show an autonomic dysfunction?. Wien Klin Wochenschr 128, 504–512 (2016). https://doi.org/10.1007/s00508-016-0980-2

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