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Intensive Care Medicine

, Volume 21, Issue 2, pp 112–119 | Cite as

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

  • M. Piepoli
  • Ch. S. Garrard
  • D. A. Kontoyannis
  • L. Bernardi
Original

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.

Key words

Autonomic nervous system Sepsis syndrome Peripheral circulation Heart rate variability Blood pressure variability Spectral analysis Adrenergic receptors Intensive care 

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References

  1. 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 317:659–665Google Scholar
  2. 2.
    Parrillo JE (1989) The cardiovascular pathophysiology of sepsis. Ann Rev Med 40:469–485Google Scholar
  3. 3.
    Cumming AD, Kline R, Linton AL (1988) Association between renal and sympathetic responses to nonhypotensive systemic sepsis. Crit Care Med 16:1132–1137Google Scholar
  4. 4.
    Koyama S (1986) Central impairment of renal nerve response to stimulation of medullary pressor area in rabbit endotoxic hypotension. Brain Res 366:217–223Google Scholar
  5. 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 99:176–184Google Scholar
  6. 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 4:19–25Google Scholar
  7. 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 76:1539–1553Google Scholar
  8. 8.
    Archer LT (1985) Myocardial dysfunction in endotoxin-and E. coli-induced shock: pathophysiological mechanisms. Circ Shock 15:261–280Google Scholar
  9. 9.
    Jones SB, Romano FD (1990) Myocardial beta adrenergic receptor coupling to adenylate cyclase during developing septic shock. Circ Shock 32:51–61Google Scholar
  10. 10.
    Silverman HJ, Lee NH, el-Fakahany EE (1990) Effects of canine endotoxin shock on lymphocytic beta-adrenergic receptors. Circ Shock 32:293–306Google Scholar
  11. 11.
    Dennhardt R, Gramm HJ, Meinhold K, Voigt K (1989) Patterns of endocrine secretion during sepsis. Prog Clin Biol Res 308:751–756Google Scholar
  12. 12.
    Woolf PD, Hamill RW, Lee LA, McDonal JV (1988) Free and total catecholamines in critical illness. Am J Physiol 254:E287-E291Google Scholar
  13. 13.
    Garrard CS, Kontoyannis DA, Piepoli M (1993) Spectral analysis of heart rate variability in the sepsis syndrome. Clin Auton Res 3:5–13Google Scholar
  14. 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 59:178–193Google Scholar
  15. 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 37:16–27Google Scholar
  16. 16.
    Malliani A, Pagani M, Lombardi F, Cerutti S (1991) Cardiovascular neural regulation explored in the frequency domain. Circulation 84:482–492Google Scholar
  17. 17.
    Bone RC, Fisher CJ, Clemmer TP, Slotman GJ, Metz CA, Balk RA (1989) Sepsis syndrome: a valid clinical entity. Crit Care Med 17:389–393Google Scholar
  18. 18.
    Knaus WA, Draper EA, Wagner DP, Zimmerman JE (1985) Apache II: a severity of disease classification system. Crit Care Med 13:818–829Google Scholar
  19. 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 125–151Google Scholar
  20. 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, USAGoogle Scholar
  21. 21.
    Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1986) Numerical recipes: the art of scientific computing: Cambridge University Press, New York, pp 495–497Google Scholar
  22. 22.
    Kay SM, Marple SL Jr (1981) Spectrum analysis — a modern perspective. Proc IEEE 69:1380–1419Google Scholar
  23. 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: 969–981Google Scholar
  24. 24.
    Ulrych TJ, Bishop TN (1975) Maximum entropy spectral analysis and autoregressive decomposition. Rev Geophys Space Phys 13:183–200Google Scholar
  25. 25.
    Zetterberg LH (1969) Estimation of parameters for a linear difference equation with application to EEG analysis. Math Biosci 5:227–275Google Scholar
  26. 26.
    Isaksson A, Wennberg A, Zetterberg LH (1981) Computer analysis of EEG signals with parametric models. Proc IEEE 69:451–461Google Scholar
  27. 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-H153Google Scholar
  28. 28.
    Scheffé H (1953) A method for judging all contrasts in the analysis of variance. Biometrika 40:87–104Google Scholar
  29. 29.
    Lundberg DB (1988) Aspects of central and peripheric adrenergic mechanisms in experimental shock. Prog Clin Biol Res 264:275–284Google Scholar
  30. 30.
    Koyama S (1986) Effects of methylprednisolone on renal nerve response to stimulation of medullary pressor area in endotoxin-induced hypotension. Circ Shock 20:205–215Google Scholar
  31. 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 321:280–287Google Scholar
  32. 32.
    Garrison RN, Cryer HM (1983) Role of the microcirculation to skeletal muscle during shock. Prog Clin Biol Res 299:43–52Google Scholar
  33. 33.
    Bernardi L, Ricordi L, Lazzari P, Solda' PL, Calciati A, Ferrari MR (1992) Impaired circadian modulation of sympathovagal activity in diabetes. Circulation 86:1443–1452Google Scholar
  34. 34.
    Hirsch S, Bishop B (1981) Respiratory sinus arrhythmia in humans: how breathing patterns modulate heart rate. Am J Physiol 241:H620-H629Google Scholar
  35. 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 67:1447–1455Google Scholar
  36. 36.
    Levy MN, Blatberg B (1967) Changes in heart rate induced by bacterial endotoxin. Am J Physiol 213:1485–1492Google Scholar
  37. 37.
    Zhou ZZ, Wurster RD, Jones SB (1992) Arterial baroreflex are not essential in mediating sympathodrenal activation in conscious rats. J Auton Nerv Syst 39:1–12Google Scholar
  38. 38.
    DeBoer RW, Karemaker KM, Strackee J (1987) Hemodynamic fluctuations and baroreflex sensitivity in humans: a beat-to-beat model. Am J Physiol 253: 680–689Google Scholar
  39. 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 69:536PGoogle Scholar
  40. 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-362Google Scholar
  41. 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 15:923–929Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • M. Piepoli
    • 1
  • Ch. S. Garrard
    • 2
  • D. A. Kontoyannis
    • 3
  • L. Bernardi
    • 4
  1. 1.Department of Cardiovascular Medicine, John Radcliffe HospitalUniversity of OxfordUK
  2. 2.Intensive Therapy Unit, John Radcliffe HospitalUniversity of OxfordOxfordUK
  3. 3.Department of Clinical TherapeuticsAlexandra HospitalAthensGreece
  4. 4.Department of Internal MedicineUniversity of PaviaPaviaItaly

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