Skip to main content
SpringerLink
Log in

Autonomic control of the heart and peripheral vessels in human septic shock

  • Original
  • Published:
Intensive Care Medicine Aims and scope Submit manuscript

Abstract

Objective

Circulating endotoxin impairs the sympathetic regulation of the cardiovascular system in animals. We studied the changes in the autonomic control of the heart and circulation during septic shock in humans.

Design

12 patients (age 43.0±6, 17–83 years) were investigated during septic shock (mean duration: 3.5±0.5 days) and during recovery, fluctuations in R-R interval, invasive arterial pressure (AP) and peripheral arteriolar circulation (PC, photoplethysmography) were evaluated by spectral analysis as a validated nonivasive measure of sympathovagal tone. Apache II score was adopted as the disease severity index. Low frequency components (0.03–0.15 Hz) of the frequency spectra were expressed as relative to the overall variability (LFnu) for each cardiovascular variable.

Results

LFnu were low or absent during shock but, in the 10 patients who recovered, increased by the time of discharge (post-shock). R-R LFnu increased from 17±6 to 47±9 (p<0.03), AP LFnu from 6±3 to 35±4 (p<0.02) and PC LFnu from 18±3 to 66±4 (p<0.001). Apache II fell from 23.1±1, at admission, to 14.8±1.8 at discharge (p<0.005). Two patients died showing no LFnu increase.

Conclusion

Reduced LF components of the variability of cardiovascular signals are characteristic of septic shock, confirming the presence of abnormal autonomic control. Restored sympathetic (LF) modulation seems to be associated with a favourable prognosis.

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

Similar content being viewed by others

References

  1. The Veterans Administration Systemic Sepsis Cooperative Study Group (1987) Effect of high dose glucocorticoid therapy on mortality in patients with clinical signs of systemic sepsis. N Engl J Med 317:659–665

    Google Scholar 

  2. Parrillo JE (1989) The cardiovascular pathophysiology of sepsis. Ann Rev Med 40:469–485

    Google Scholar 

  3. Cumming AD, Kline R, Linton AL (1988) Association between renal and sympathetic responses to nonhypotensive systemic sepsis. Crit Care Med 16:1132–1137

    Google Scholar 

  4. Koyama S (1986) Central impairment of renal nerve response to stimulation of medullary pressor area in rabbit endotoxic hypotension. Brain Res 366:217–223

    Google Scholar 

  5. Witt NJ, Zochodne DW, Bolton CF, Grand'Maison F, Wells G, Young GB, Sibbald WJ (1991) Peripheral nerve function in sepsis and multiple organ failure. Chest 99:176–184

    Google Scholar 

  6. Parker MM, Suffredini AF, Natanson, C, Ognibene FP, shelhamer JH, Parrillo JE (1989) Responses of left ventricular function in survivors and nonsurvivors of septic shock. J Crit Care 4:19–25

    Google Scholar 

  7. Parrillo JE, Burch C, Shelhamer JH, Parker MM, Natanson C, Schuette W (1985) A circulating myocardial depressant substance in humans with septic shock. Septic shock patients with a reduced ejection fraction have a circulating factor that depresses in vitro myocardial cell performance. J Clin Invest 76:1539–1553

    Google Scholar 

  8. Archer LT (1985) Myocardial dysfunction in endotoxin-and E. coli-induced shock: pathophysiological mechanisms. Circ Shock 15:261–280

    Google Scholar 

  9. Jones SB, Romano FD (1990) Myocardial beta adrenergic receptor coupling to adenylate cyclase during developing septic shock. Circ Shock 32:51–61

    Google Scholar 

  10. Silverman HJ, Lee NH, el-Fakahany EE (1990) Effects of canine endotoxin shock on lymphocytic beta-adrenergic receptors. Circ Shock 32:293–306

    Google Scholar 

  11. Dennhardt R, Gramm HJ, Meinhold K, Voigt K (1989) Patterns of endocrine secretion during sepsis. Prog Clin Biol Res 308:751–756

    Google Scholar 

  12. Woolf PD, Hamill RW, Lee LA, McDonal JV (1988) Free and total catecholamines in critical illness. Am J Physiol 254:E287-E291

    Google Scholar 

  13. Garrard CS, Kontoyannis DA, Piepoli M (1993) Spectral analysis of heart rate variability in the sepsis syndrome. Clin Auton Res 3:5–13

    Google Scholar 

  14. Pagani M, Lombardi F, Guzzetti S, Rimoldi O, Furlan R, Pizzinelli P, Sandrone G, Malfatto G, Dell'Orto S, Piccaluga E, Turiel M, Baselli G, Cerutti S, Malliani A (1986) Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympathovagal interaction in man and conscious dog. Circ Res 59:178–193

    Google Scholar 

  15. Bernardi L, Rossi M, Fratino P, Finardi G, Mevio E, Orlandi C (1989) Relationship between phasic changes in human skin blood flow and autonomic tone. Microvasc Res 37:16–27

    Google Scholar 

  16. Malliani A, Pagani M, Lombardi F, Cerutti S (1991) Cardiovascular neural regulation explored in the frequency domain. Circulation 84:482–492

    Google Scholar 

  17. Bone RC, Fisher CJ, Clemmer TP, Slotman GJ, Metz CA, Balk RA (1989) Sepsis syndrome: a valid clinical entity. Crit Care Med 17:389–393

    Google Scholar 

  18. Knaus WA, Draper EA, Wagner DP, Zimmerman JE (1985) Apache II: a severity of disease classification system. Crit Care Med 13:818–829

    Google Scholar 

  19. Challoner AVJ (1979) Photoelectric plethysmography for estimating cutaneous blood flow. In: Rolfe P (ed) Non-invasive physiological measurements, vol 9. Academic Press, London, pp 125–151

    Google Scholar 

  20. Bernardi L, Leuzzi S (in press) Laser Doppler flowmetry and photoplethysmography. Hardware and measuring principles. In: Berardesca, E, Elsner P, Maibach H (eds) Handbooks of skin bioengineering. Cutaneous blood flow and erythema. CRC Press, Boca Raton FL, USA

  21. Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1986) Numerical recipes: the art of scientific computing: Cambridge University Press, New York, pp 495–497

    Google Scholar 

  22. Kay SM, Marple SL Jr (1981) Spectrum analysis — a modern perspective. Proc IEEE 69:1380–1419

    Google Scholar 

  23. Bernardi L, Salvucci F, Suardi R, Solda' PL, Calciati A, Perlini S, Falcone C, Ricciardi L (1990) Evidence for an intrinsic mechanism regulating heart rate variability in the transplanted and the intact heart during submaximal dynamic exercise?. Cardiovasc Res 24: 969–981

    Google Scholar 

  24. Ulrych TJ, Bishop TN (1975) Maximum entropy spectral analysis and autoregressive decomposition. Rev Geophys Space Phys 13:183–200

    Google Scholar 

  25. Zetterberg LH (1969) Estimation of parameters for a linear difference equation with application to EEG analysis. Math Biosci 5:227–275

    Google Scholar 

  26. Isaksson A, Wennberg A, Zetterberg LH (1981) Computer analysis of EEG signals with parametric models. Proc IEEE 69:451–461

    Google Scholar 

  27. Pomeranz B, Macaulay RJB, Caudill MA, Kutz I, Adam D, Gordon D, Kilborn KM, Barger AC, Shannon DC, Cohen RJ, Benson H (1985) Assessment of autonomic function in man by heart rate spectral analysis. Am J Physiol 248:H151-H153

    Google Scholar 

  28. Scheffé H (1953) A method for judging all contrasts in the analysis of variance. Biometrika 40:87–104

    Google Scholar 

  29. Lundberg DB (1988) Aspects of central and peripheric adrenergic mechanisms in experimental shock. Prog Clin Biol Res 264:275–284

    Google Scholar 

  30. Koyama S (1986) Effects of methylprednisolone on renal nerve response to stimulation of medullary pressor area in endotoxin-induced hypotension. Circ Shock 20:205–215

    Google Scholar 

  31. Suffredini AF, Fromm RE, Parker MM, Brenner M, Kovacs JA, Wesley RA, Parillo JE (1989) The cardiovascular response of normal humans to the administrations of endotoxins. N Engl J Med 321:280–287

    Google Scholar 

  32. Garrison RN, Cryer HM (1983) Role of the microcirculation to skeletal muscle during shock. Prog Clin Biol Res 299:43–52

    Google Scholar 

  33. Bernardi L, Ricordi L, Lazzari P, Solda' PL, Calciati A, Ferrari MR (1992) Impaired circadian modulation of sympathovagal activity in diabetes. Circulation 86:1443–1452

    Google Scholar 

  34. Hirsch S, Bishop B (1981) Respiratory sinus arrhythmia in humans: how breathing patterns modulate heart rate. Am J Physiol 241:H620-H629

    Google Scholar 

  35. Bernardi L, Keller F, Sanders M, Reddy PS, Griffith B, Meno F, Pinsky MR (1989) Respiratory sinus arrhythmia in the denervated human heart. J Appl Physiol 67:1447–1455

    Google Scholar 

  36. Levy MN, Blatberg B (1967) Changes in heart rate induced by bacterial endotoxin. Am J Physiol 213:1485–1492

    Google Scholar 

  37. Zhou ZZ, Wurster RD, Jones SB (1992) Arterial baroreflex are not essential in mediating sympathodrenal activation in conscious rats. J Auton Nerv Syst 39:1–12

    Google Scholar 

  38. DeBoer RW, Karemaker KM, Strackee J (1987) Hemodynamic fluctuations and baroreflex sensitivity in humans: a beat-to-beat model. Am J Physiol 253: 680–689

    Google Scholar 

  39. Howell S, Wanigasekera V, Sear JW, Garrard CS (1992) Heart rate spectrum analysis during induction of anaesthesia with thiopentone or propofol. Br J Anaesth 69:536P

    Google Scholar 

  40. Piepoli M, Adamopoulos A, Bernardi L, Sleight P, Coats A (1993) Similar heart rate variability spectral analysis changes are induced by exogenous and endogenous β-receptor stimulation (abstract). Circulation 88:I-362

    Google Scholar 

  41. Parker MM, Shelhamer JH, Natason C, Alling DW, Parillo JE (1987) Serial cardiovascular variables in survivors of human septic shock: heart rate as an early predictor of prognosis. Crit Care Med 15:923–929

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cardiovascular Medicine, John Radcliffe Hospital, University of Oxford, OX3 9DU, Oxford, UK

    M. Piepoli

  2. Intensive Therapy Unit, John Radcliffe Hospital, University of Oxford, OX3 9DU, Oxford, UK

    Ch. S. Garrard

  3. Department of Clinical Therapeutics, Alexandra Hospital, Athens, Greece

    D. A. Kontoyannis

  4. Department of Internal Medicine, University of Pavia, Pavia, Italy

    L. Bernardi

Authors
  1. M. Piepoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ch. S. Garrard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. A. Kontoyannis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. Bernardi
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Piepoli, M., Garrard, C.S., Kontoyannis, D.A. et al. Autonomic control of the heart and peripheral vessels in human septic shock. Intensive Care Med 21, 112–119 (1995). https://doi.org/10.1007/BF01726532

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01726532

Key words

Search

Navigation