Abstract
Objective
Sepsis is now considered a disease of the microcirculation. Little is known about the various sepsis-induced changes responsible for microvascular dysfunction. We investigated human microvascular function, regulation, oxygenation, and cellular metabolism during subacute septic shock.
Design and setting
Prospective case-control study in a nine-bed polyvalent surgical ICU of a university hospital.
Patients and participants
A prospectively enrolled group of 26 patients (13 with septic shock, 13 nonseptic postsurgical patients) and 15 healthy volunteer controls.
Measurements and results
The absolute tissue hemoglobin concentrations (oxygenated hemoglobin and deoxyhemoglobin) were measured noninvasively in arterioles, capillaries, and venules by phase-modulation near-infrared spectroscopy in the human brachioradial muscle during a series of venous occlusions and an arterial occlusion (ischemia) induced by applying a pneumatic cuff. These measurements were used to calculate tissue blood volume, postischemic hemoglobin resaturation time, microvascular compliance, and O2 consumption. Patients with sepsis had significantly higher tissue blood volume values and lower compliance than healthy controls. They also had longer postischemic hemoglobin resaturation times than the other two groups and blunted resaturation curves. O2 consumption was lower in patients with sepsis than in healthy controls. In patients with septic shock cuff-induced ischemia left O2 consumption unchanged, whereas in healthy volunteers it reduced O2 consumption to values almost matching those of patients with septic shock.
Conclusions
These findings show that septic shock alters microvascular muscle function and regulation. Diminished local VO2 presumably reflects maldistribution and faulty autoregulation of local blood flow.
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References
Pohl U, De Wit C, Gloe T (2000) Large arterioles in the control of blood flow: role of endothelium-dependent dilation. Acta Physiol Scand 168:505–510
Vallet B (1998) Vascular reactivity and tissue oxygenation. Intensive Care Med 24:3–11
Piper R, Pitt-Hyde M, Li F, Sibbald W, Potter R (1996) Microcirculatory changes in rat skeletal muscle in sepsis. Am J Respir Crit Care Med 154:931–937
Neviere R, Mathieu D, Chagnon JL, Lebleu N, Millien JP, Wattel F (1996) Skeletal muscle microvascular blood flow and oxygen transport in patients with severe sepsis. Am J Respir Crit Care Med 153:191–195
Bauer PR (2002) Microvascular responses to sepsis: clinical significance. Pathophysiology 8:141–148
Spronk P, Zandstra D, Ince C (2004) Bench-to-bedside review: sepsis is a disease of the microcirculation. Crit Care 8:462–468
De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL (2002) Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med 166:98–104
Christ F, Gamble J, Gartside IB, Kox WJ (1998) Increased microvascular water permeability in patients with septic shock, assessed with venous congestion plethysmography. Intensive Care Med 24:18–27
Lam C, Tyml K, Martin C, Sibbald W (1994) Microvascular perfusion is impaired in a rat model of normotensive sepsis. J Clin Invest 94:2077–2083
Astiz M, Tilly E, Rackow E, Weil M (1991) Peripheral vascular tone in sepsis. Chest 99:1072–1075
Adrie C, Bachelet M, Vayssier-Taussat M, Russo-Marie F, Bouchaert I, Adib-Conquy M, Cavaillon JM, Pinsky MR, Dhainaut JF, Polla BS (2001) Mitochondrial membrane potential and apoptosis peripheral blood monocytes in severe human sepsis. Am J Respir Crit Care Med 164:389–395
Fink M (1997) Cytophatic hypoxia in sepsis. Acta Anaesthesiol Scand Suppl 110:87–95
Ellis CG, Bateman RM, Sharpe MD, Sibbald WJ, Gill R (2002) Effect of a maldistribution of microvascular blood flow on capillary O2 extraction in sepsis. Am J Physiol Heart Circ Physiol 282:H156–H164
Liu H, Chance B, Hielscher AH, Jacques SL, Tittel FK (1995) Influence of blood vessels on the measurement of hemoglobin oxygenation as determined by time-resolved reflectance spectroscopy. Med Phys 22:1209–1217
De Blasi RA, Ferrari M, Antonelli M, Conti G, Almenrader N, Gasparetto A (1996) O2 consumption-O2 delivery relationship and arteriolar resistance in the forearm of critically ill patients measured by near infrared spectroscopy. Shock 6:319–325
De Blasi RA, Ferrari M, Natali A, Conti G, Mega A, Gasparetto A (1994) Noninvasive measurement of forearm blood flow and oxygen consumption by near-infrared spectroscopy. J Appl Physiol 76:1388–1393
De Blasi RA, Quaglia E, Ferrari M (1991) Skeletal muscle oxygenation monitoring by near infrared spectroscopy. Biochem Int 25:241–245
Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL, Ramsay G for the International Sepsis Definitions Conference (2003) 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Intensive Care Med 29:530–538
Fantini S, Franceschini MA, Maier JS, Walker SA, Barbieri B, Gratton E (1995) Frequency domain multichannel optical detector for non-invasive tissue spectroscopy and oxymetry. Opt Eng 34:32–42
Van Beekvelt MCP, Colier WN, Wevers RA, Van Engelen GM (2001) Performance of near-infrared spectroscopy in measuring local O2 consumption and blood flow in skeletal muscle. J Appl Physiol 90:511–519
Binzoni T, Quaresima V, Ferrari M, Hiltbrand E, Cerretelli P (2000) Human calf microvascular compliance measured by near-infrared spectroscopy. J Appl Physiol 88:369–372
Revelly JP, Ayuse T, Brienza N, Robotham JL (1995) Dysregulation of the veno-arterial response in the superior mesenteric artery during endotoxic shock. Crit Care Med 23:1519–1527
Halliwill J, Minson C, Joyner M (1999) Measurement of limb venous compliance in humans: technical considerations and physiological findings. J Appl Physiol 87:1555–1563
Freeman R, Lirofonis V, Farquhar W, Risk M (2002) Limb venous compliance in patients with idiopathic orthostatic intolerance and postural tachycardia. J Appl Physiol 93:636–644
Holbeck S, Grande PO (2003) Endotoxin increases both protein and fluid microvascular permeability in cat skeletal muscle. Crit Care Med 31:560–565
Kawabe T, Harris PD, Zakaria ELR, Garrison RN (2003) Sepsis alters vessel contraction by adrenoreceptor-induced nitric oxide and prostanoid. J Surg Res 110:352–359
Haase EB, Shoukas AA (1991) Carotid sinus baroreceptor reflex control of venular pressure-diameter relations in rat intestine. Am J Physiol 260:H752–H758
Tyml K, Yu J, McCormack D (1998) Capillary and arteriolar responses to local vasodilators are impaired in a rat model of sepsis. J Appl Physiol 84:837–844
Price S, Spain D, Wilson M, Harris P, Garrison N (1999) Subacute sepsis impairs vascular smooth muscle contractile machinery and alters vasoconstrictor and dilator mechanisms. J Surg Res 83:75–80
Takakura K, Taniguchi T, Muramatsu I, Takeuchi K, Fukuda S (2002) Modification of α1-adrenoceptors by peroxynitrite as a possible mechanism of systemic hypotension in sepsis. Crit Care Med 30:894–899
Takakura K, Xiaohong W, Takeuchi K, Yasuda Y, Fukuda S (2003) Deactivation of norepinephrine by peroxynitrite as a new pathogenesis in the hypotension of septic shock. Anesthesiology 98:928–934
Pickkers P, Jansen van Rosendaal A, van der Hoeven J, Smits P (2004) Activation of the ATP-dependent potassium channel attenuates norepinephrine-induced vasoconstriction in the human forearm. Shock 22:320–325
Ince C, Sinaasappel M (1999) Microcirculatory oxygenation and shunting in sepsis and shock. Crit Care Med 27:1369–1377
Van Beekvelt MCP, Borghuis MS, van Engelen, Wevers RA, Colier WNJM (2001) Adipose tissue thickness affects in vivo quantitative near-IR spectroscopy in human skeletal muscle. Clin Sci (Lond) 101:21–28
Frank S, Higgins M, Breslow M, Fleisher L, Gorman R, Sitzmann J, Raff Hershel, Beattle C (1995) The catecholamine, cortisol, and hemodynamic responses to mild perioperative hypotermia: a randomized clinical trial. Anesthesiology 82:83–93
Frank S, Fleisher L, Olson K, Gorman R, Higgins M, Breslow M, Sitzmann J, Beattle C (1995) Multivariate determinants of early postoperative oxygen consumption in elderly patients: effect of shivering, body temperature, and gender. Anesthesiology 83:241–249
MacPherson RD, Rasiah RL, McLeod LJ (1993) Propofol attenuates the myogenic response response of vascular smooth muscle. Anesth Analg 76:822–829
Van der Linden P, Schmartz D, Gilbart E, Engelman E, Vincent JL (2000) Effects of propofol, etomidate, and pentobarbital on critical oxygen delivery. Crit Care Med 28:2492–2499
Acknowledgements
The authors are indebted to the ICU nursing staff for their invaluable cooperation during the study.
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De Blasi, R.A., Palmisani, S., Alampi, D. et al. Microvascular dysfunction and skeletal muscle oxygenation assessed by phase-modulation near-infrared spectroscopy in patients with septic shock. Intensive Care Med 31, 1661–1668 (2005). https://doi.org/10.1007/s00134-005-2822-y
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DOI: https://doi.org/10.1007/s00134-005-2822-y