Skip to main content
Top
Published in: Journal of Clinical Monitoring and Computing 4/2013

01-08-2013 | Review

Translational applications of evaluating physiologic variability in human endotoxemia

Authors: Jeremy D. Scheff, Panteleimon D. Mavroudis, Steve E. Calvano, Ioannis P. Androulakis

Published in: Journal of Clinical Monitoring and Computing | Issue 4/2013

Login to get access

Abstract

Dysregulation of the inflammatory response is a critical component of many clinically challenging disorders such as sepsis. Inflammation is a biological process designed to lead to healing and recovery, ultimately restoring homeostasis; however, the failure to fully achieve those beneficial results can leave a patient in a dangerous persistent inflammatory state. One of the primary challenges in developing novel therapies in this area is that inflammation is comprised of a complex network of interacting pathways. Here, we discuss our approaches towards addressing this problem through computational systems biology, with a particular focus on how the presence of biological rhythms and the disruption of these rhythms in inflammation may be applied in a translational context. By leveraging the information content embedded in physiologic variability, ranging in scale from oscillations in autonomic activity driving short-term heart rate variability to circadian rhythms in immunomodulatory hormones, there is significant potential to gain insight into the underlying physiology.
Literature
1.
go back to reference Rittirsch D, Flierl MA, Ward PA. Harmful molecular mechanisms in sepsis. Nat Rev Immunol. 2008;8(10):776–87.PubMedCrossRef Rittirsch D, Flierl MA, Ward PA. Harmful molecular mechanisms in sepsis. Nat Rev Immunol. 2008;8(10):776–87.PubMedCrossRef
2.
go back to reference Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through. N Engl J Med. 2003;348(16):1546–54.PubMedCrossRef Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through. N Engl J Med. 2003;348(16):1546–54.PubMedCrossRef
3.
go back to reference Namas R, Zamora R, Namas R, An G, Doyle J, Dick TE, Jacono FJ, Androulakis IP, Nieman GF, Chang S, Billiar TR, Kellum JA, Angus DC, Vodovotz Y. Sepsis: something old, something new, and a systems view. J Crit Care. 2011;27(3):314 e1–11. Namas R, Zamora R, Namas R, An G, Doyle J, Dick TE, Jacono FJ, Androulakis IP, Nieman GF, Chang S, Billiar TR, Kellum JA, Angus DC, Vodovotz Y. Sepsis: something old, something new, and a systems view. J Crit Care. 2011;27(3):314 e1–11.
4.
go back to reference Novak B, Tyson JJ. Design principles of biochemical oscillators. Nat Rev Mol Cell Biol. 2008;9(12):981–91.PubMedCrossRef Novak B, Tyson JJ. Design principles of biochemical oscillators. Nat Rev Mol Cell Biol. 2008;9(12):981–91.PubMedCrossRef
5.
go back to reference Pigolotti S, Krishna S, Jensen MH. Oscillation patterns in negative feedback loops. Proc Natl Acad Sci USA. 2007;104(16):6533–7.PubMedCrossRef Pigolotti S, Krishna S, Jensen MH. Oscillation patterns in negative feedback loops. Proc Natl Acad Sci USA. 2007;104(16):6533–7.PubMedCrossRef
6.
go back to reference Veldhuis JD, Keenan DM, Pincus SM. Motivations and methods for analyzing pulsatile hormone secretion. Endocr Rev. 2008;29(7):823–64.PubMedCrossRef Veldhuis JD, Keenan DM, Pincus SM. Motivations and methods for analyzing pulsatile hormone secretion. Endocr Rev. 2008;29(7):823–64.PubMedCrossRef
7.
go back to reference Griffin MP, O’Shea TM, Bissonette EA, Harrell FE Jr, Lake DE, Moorman JR. Abnormal heart rate characteristics preceding neonatal sepsis and sepsis-like illness. Pediatr Res. 2003;53(6):920–6.PubMedCrossRef Griffin MP, O’Shea TM, Bissonette EA, Harrell FE Jr, Lake DE, Moorman JR. Abnormal heart rate characteristics preceding neonatal sepsis and sepsis-like illness. Pediatr Res. 2003;53(6):920–6.PubMedCrossRef
8.
go back to reference Moorman JR, Carlo WA, Kattwinkel J, Schelonka RL, Porcelli PJ, Navarrete CT, Bancalari E, Aschner JL, Whit Walker M, Perez JA, Palmer C, Stukenborg GJ, Lake DE, Michael O’Shea T. Mortality reduction by heart rate characteristic monitoring in very low birth weight neonates: a randomized trial. J Pediatr. 2011;159(6):900–6. (e901).PubMedCrossRef Moorman JR, Carlo WA, Kattwinkel J, Schelonka RL, Porcelli PJ, Navarrete CT, Bancalari E, Aschner JL, Whit Walker M, Perez JA, Palmer C, Stukenborg GJ, Lake DE, Michael O’Shea T. Mortality reduction by heart rate characteristic monitoring in very low birth weight neonates: a randomized trial. J Pediatr. 2011;159(6):900–6. (e901).PubMedCrossRef
9.
go back to reference Yehuda R, Teicher MH, Trestman RL, Levengood RA, Siever LJ. Cortisol regulation in posttraumatic stress disorder and major depression: a chronobiological analysis. Biol Psychiatry. 1996;40(2):79–88.PubMedCrossRef Yehuda R, Teicher MH, Trestman RL, Levengood RA, Siever LJ. Cortisol regulation in posttraumatic stress disorder and major depression: a chronobiological analysis. Biol Psychiatry. 1996;40(2):79–88.PubMedCrossRef
10.
go back to reference Rosmond R, Dallman MF, Bjorntorp P. Stress-related cortisol secretion in men: relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J Clin Endocrinol Metab. 1998;83(6):1853–9.PubMedCrossRef Rosmond R, Dallman MF, Bjorntorp P. Stress-related cortisol secretion in men: relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J Clin Endocrinol Metab. 1998;83(6):1853–9.PubMedCrossRef
11.
go back to reference Polk DE, Cohen S, Doyle WJ, Skoner DP, Kirschbaum C. State and trait affect as predictors of salivary cortisol in healthy adults. Psychoneuroendocrinology. 2005;30(3):261–72.PubMedCrossRef Polk DE, Cohen S, Doyle WJ, Skoner DP, Kirschbaum C. State and trait affect as predictors of salivary cortisol in healthy adults. Psychoneuroendocrinology. 2005;30(3):261–72.PubMedCrossRef
12.
go back to reference Sephton SE, Sapolsky RM, Kraemer HC, Spiegel D. Diurnal cortisol rhythm as a predictor of breast cancer survival. J Natl Cancer Inst. 2000;92(12):994–1000.PubMedCrossRef Sephton SE, Sapolsky RM, Kraemer HC, Spiegel D. Diurnal cortisol rhythm as a predictor of breast cancer survival. J Natl Cancer Inst. 2000;92(12):994–1000.PubMedCrossRef
13.
go back to reference Mormont MC, Levi F. Circadian-system alterations during cancer processes: a review. Int J Cancer. 1997;70(2):241–7.PubMedCrossRef Mormont MC, Levi F. Circadian-system alterations during cancer processes: a review. Int J Cancer. 1997;70(2):241–7.PubMedCrossRef
14.
go back to reference Lowry SF. Human endotoxemia: a model for mechanistic insight and therapeutic targeting. Shock. 2005;24(Suppl 1):94–100.PubMedCrossRef Lowry SF. Human endotoxemia: a model for mechanistic insight and therapeutic targeting. Shock. 2005;24(Suppl 1):94–100.PubMedCrossRef
15.
go back to reference Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. Modeling endotoxin-induced systemic inflammation using an indirect response approach. Math Biosci. 2009;217(1):27–42.PubMedCrossRef Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. Modeling endotoxin-induced systemic inflammation using an indirect response approach. Math Biosci. 2009;217(1):27–42.PubMedCrossRef
16.
go back to reference Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. In silico simulation of corticosteroids effect on an NFkB- dependent physicochemical model of systemic inflammation. PLoS ONE. 2009;4(3):e4706.PubMedCrossRef Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. In silico simulation of corticosteroids effect on an NFkB- dependent physicochemical model of systemic inflammation. PLoS ONE. 2009;4(3):e4706.PubMedCrossRef
17.
go back to reference Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. Multiscale model for the assessment of autonomic dysfunction in human endotoxemia. Physiol Genomics. 2010;42(1):5–19.PubMedCrossRef Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. Multiscale model for the assessment of autonomic dysfunction in human endotoxemia. Physiol Genomics. 2010;42(1):5–19.PubMedCrossRef
18.
go back to reference Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. A physiological model for autonomic heart rate regulation in human endotoxemia. Shock. 2011;35(3):229–39.PubMedCrossRef Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. A physiological model for autonomic heart rate regulation in human endotoxemia. Shock. 2011;35(3):229–39.PubMedCrossRef
19.
go back to reference Dong X, Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. Agent-based modeling of endotoxin-induced acute inflammatory response in human blood leukocytes. PLoS ONE. 2010;5(2):e9249.PubMedCrossRef Dong X, Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. Agent-based modeling of endotoxin-induced acute inflammatory response in human blood leukocytes. PLoS ONE. 2010;5(2):e9249.PubMedCrossRef
20.
go back to reference Scheff JD, Calvano SE, Lowry SF, Androulakis IP. Modeling the influence of circadian rhythms on the acute inflammatory response. J Theor Biol. 2010;264(3):1068–76.PubMedCrossRef Scheff JD, Calvano SE, Lowry SF, Androulakis IP. Modeling the influence of circadian rhythms on the acute inflammatory response. J Theor Biol. 2010;264(3):1068–76.PubMedCrossRef
21.
go back to reference Scheff JD, Mavroudis PD, Calvano SE, Lowry SF, Androulakis IP. Modeling autonomic regulation of cardiac function and heart rate variability in human endotoxemia. Physiol Genomics. 2011;43(16):951–64.PubMedCrossRef Scheff JD, Mavroudis PD, Calvano SE, Lowry SF, Androulakis IP. Modeling autonomic regulation of cardiac function and heart rate variability in human endotoxemia. Physiol Genomics. 2011;43(16):951–64.PubMedCrossRef
22.
go back to reference Rassias AJ, Holzberger PT, Givan AL, Fahrner SL, Yeager MP. Decreased physiologic variability as a generalized response to human endotoxemia. Crit Care Med. 2005;33(3):512–9.PubMedCrossRef Rassias AJ, Holzberger PT, Givan AL, Fahrner SL, Yeager MP. Decreased physiologic variability as a generalized response to human endotoxemia. Crit Care Med. 2005;33(3):512–9.PubMedCrossRef
23.
go back to reference Andreasen AS, Krabbe KS, Krogh-Madsen R, Taudorf S, Pedersen BK, Moller K. Human endotoxemia as a model of systemic inflammation. Curr Med Chem. 2008;15(17):1697–705.PubMedCrossRef Andreasen AS, Krabbe KS, Krogh-Madsen R, Taudorf S, Pedersen BK, Moller K. Human endotoxemia as a model of systemic inflammation. Curr Med Chem. 2008;15(17):1697–705.PubMedCrossRef
24.
go back to reference Buttenschoen K, Kornmann M, Berger D, Leder G, Beger HG, Vasilescu C. Endotoxemia and endotoxin tolerance in patients with ARDS. Langenbecks Arch Surg. 2008;393(4):473–8.PubMedCrossRef Buttenschoen K, Kornmann M, Berger D, Leder G, Beger HG, Vasilescu C. Endotoxemia and endotoxin tolerance in patients with ARDS. Langenbecks Arch Surg. 2008;393(4):473–8.PubMedCrossRef
25.
go back to reference Shanker BA, Coyle SM, Reddell MT, Choi CW, Calvano J, Macor MA, Calvano SE, Lowry SF Modeling the human injury response. J Am Coll Surg. 2010;211(3 Suppl 1):53–54. Shanker BA, Coyle SM, Reddell MT, Choi CW, Calvano J, Macor MA, Calvano SE, Lowry SF Modeling the human injury response. J Am Coll Surg. 2010;211(3 Suppl 1):53–54.
26.
go back to reference Lowry SF. The stressed host response to infection: the disruptive signals and rhythms of systemic inflammation. Surg Clin North Am. 2009;89(2):311–26.PubMedCrossRef Lowry SF. The stressed host response to infection: the disruptive signals and rhythms of systemic inflammation. Surg Clin North Am. 2009;89(2):311–26.PubMedCrossRef
27.
go back to reference Deans KJ, Haley M, Natanson C, Eichacker PQ, Minneci PC. Novel therapies for sepsis: a review. J Trauma. 2005;58(4):867–74.PubMedCrossRef Deans KJ, Haley M, Natanson C, Eichacker PQ, Minneci PC. Novel therapies for sepsis: a review. J Trauma. 2005;58(4):867–74.PubMedCrossRef
28.
go back to reference Marshall JC. Such stuff as dreams are made on: mediator-directed therapy in sepsis. Nat Rev Drug Discov. 2003;2(5):391–405.PubMedCrossRef Marshall JC. Such stuff as dreams are made on: mediator-directed therapy in sepsis. Nat Rev Drug Discov. 2003;2(5):391–405.PubMedCrossRef
29.
go back to reference Freeman BD, Natanson C. Anti-inflammatory therapies in sepsis and septic shock. Expert Opin Investig Drugs. 2000;9(7):1651–63.PubMedCrossRef Freeman BD, Natanson C. Anti-inflammatory therapies in sepsis and septic shock. Expert Opin Investig Drugs. 2000;9(7):1651–63.PubMedCrossRef
30.
go back to reference Vodovotz Y, Constantine G, Rubin J, Csete M, Voit EO, An G. Mechanistic simulations of inflammation: current state and future prospects. Math Biosci. 2009;217(1):1–10.PubMedCrossRef Vodovotz Y, Constantine G, Rubin J, Csete M, Voit EO, An G. Mechanistic simulations of inflammation: current state and future prospects. Math Biosci. 2009;217(1):1–10.PubMedCrossRef
31.
go back to reference Day J, Rubin J, Vodovotz Y, Chow CC, Reynolds A, Clermont G. A reduced mathematical model of the acute inflammatory response II. Capturing scenarios of repeated endotoxin administration. J Theor Biol. 2006;242(1):237–56.PubMedCrossRef Day J, Rubin J, Vodovotz Y, Chow CC, Reynolds A, Clermont G. A reduced mathematical model of the acute inflammatory response II. Capturing scenarios of repeated endotoxin administration. J Theor Biol. 2006;242(1):237–56.PubMedCrossRef
32.
go back to reference Kumar R, Clermont G, Vodovotz Y, Chow CC. The dynamics of acute inflammation. J Theor Biol. 2004;230(2):145–55.PubMedCrossRef Kumar R, Clermont G, Vodovotz Y, Chow CC. The dynamics of acute inflammation. J Theor Biol. 2004;230(2):145–55.PubMedCrossRef
33.
go back to reference Reynolds A, Rubin J, Clermont G, Day J, Vodovotz Y, Bard Ermentrout G. A reduced mathematical model of the acute inflammatory response: I. Derivation of model and analysis of anti-inflammation. J Theor Biol. 2006;242(1):220–36.PubMedCrossRef Reynolds A, Rubin J, Clermont G, Day J, Vodovotz Y, Bard Ermentrout G. A reduced mathematical model of the acute inflammatory response: I. Derivation of model and analysis of anti-inflammation. J Theor Biol. 2006;242(1):220–36.PubMedCrossRef
34.
go back to reference Arciero JC, Ermentrout GB, Upperman JS, Vodovotz Y, Rubin JE. Using a mathematical model to analyze the role of probiotics and inflammation in necrotizing enterocolitis. PLoS ONE. 2010;5(4):e10066.PubMedCrossRef Arciero JC, Ermentrout GB, Upperman JS, Vodovotz Y, Rubin JE. Using a mathematical model to analyze the role of probiotics and inflammation in necrotizing enterocolitis. PLoS ONE. 2010;5(4):e10066.PubMedCrossRef
35.
go back to reference Riviere B, Epshteyn Y, Swigon D, Vodovotz Y. A simple mathematical model of signaling resulting from the binding of lipopolysaccharide with Toll-like receptor 4 demonstrates inherent preconditioning behavior. Math Biosci. 2009;217(1):19–26.PubMedCrossRef Riviere B, Epshteyn Y, Swigon D, Vodovotz Y. A simple mathematical model of signaling resulting from the binding of lipopolysaccharide with Toll-like receptor 4 demonstrates inherent preconditioning behavior. Math Biosci. 2009;217(1):19–26.PubMedCrossRef
36.
go back to reference Nieman G, Brown D, Sarkar J, Kubiak B, Ziraldo C, Dutta-Moscato J, Vieau C, Barclay D, Gatto L, Maier K, Constantine G, Billiar TR, Zamora R, Mi Q, Chang S, Vodovotz Y. A two-compartment mathematical model of endotoxin-induced inflammatory and physiologic alterations in swine. Crit Care Med. 2012;40(4):1052–63.PubMedCrossRef Nieman G, Brown D, Sarkar J, Kubiak B, Ziraldo C, Dutta-Moscato J, Vieau C, Barclay D, Gatto L, Maier K, Constantine G, Billiar TR, Zamora R, Mi Q, Chang S, Vodovotz Y. A two-compartment mathematical model of endotoxin-induced inflammatory and physiologic alterations in swine. Crit Care Med. 2012;40(4):1052–63.PubMedCrossRef
37.
go back to reference Torres A, Bentley T, Bartels J, Sarkar J, Barclay D, Namas R, Constantine G, Zamora R, Puyana JC, Vodovotz Y. Mathematical modeling of posthemorrhage inflammation in mice: studies using a novel, computer-controlled, closed-loop hemorrhage apparatus. Shock. 2009;32(2):172–8.PubMedCrossRef Torres A, Bentley T, Bartels J, Sarkar J, Barclay D, Namas R, Constantine G, Zamora R, Puyana JC, Vodovotz Y. Mathematical modeling of posthemorrhage inflammation in mice: studies using a novel, computer-controlled, closed-loop hemorrhage apparatus. Shock. 2009;32(2):172–8.PubMedCrossRef
38.
go back to reference Yang Q, Calvano SE, Lowry SF, Androulakis IP. A dual negative regulation model of Toll-like receptor 4 signaling for endotoxin preconditioning in human endotoxemia. Math Biosci. 2011;232(2):151–63.PubMedCrossRef Yang Q, Calvano SE, Lowry SF, Androulakis IP. A dual negative regulation model of Toll-like receptor 4 signaling for endotoxin preconditioning in human endotoxemia. Math Biosci. 2011;232(2):151–63.PubMedCrossRef
39.
go back to reference Daun S, Rubin J, Vodovotz Y, Roy A, Parker R, Clermont G. An ensemble of models of the acute inflammatory response to bacterial lipopolysaccharide in rats: results from parameter space reduction. J Theor Biol. 2008;253(4):843–53.PubMedCrossRef Daun S, Rubin J, Vodovotz Y, Roy A, Parker R, Clermont G. An ensemble of models of the acute inflammatory response to bacterial lipopolysaccharide in rats: results from parameter space reduction. J Theor Biol. 2008;253(4):843–53.PubMedCrossRef
40.
go back to reference Li NY, Vodovotz Y, Kim KH, Mi Q, Hebda PA, Abbott KV. Biosimulation of acute phonotrauma: an extended model. Laryngoscope. 2011;121(11):2418–28.PubMedCrossRef Li NY, Vodovotz Y, Kim KH, Mi Q, Hebda PA, Abbott KV. Biosimulation of acute phonotrauma: an extended model. Laryngoscope. 2011;121(11):2418–28.PubMedCrossRef
41.
go back to reference Brown BN, Price IM, Toapanta FR, DeAlmeida DR, Wiley CA, Ross TM, Oury TD, Vodovotz Y. An agent-based model of inflammation and fibrosis following particulate exposure in the lung. Math Biosci. 2011;231(2):186–96.PubMedCrossRef Brown BN, Price IM, Toapanta FR, DeAlmeida DR, Wiley CA, Ross TM, Oury TD, Vodovotz Y. An agent-based model of inflammation and fibrosis following particulate exposure in the lung. Math Biosci. 2011;231(2):186–96.PubMedCrossRef
42.
go back to reference Li NY, Vodovotz Y, Hebda PA, Abbott KV. Biosimulation of inflammation and healing in surgically injured vocal folds. Ann Otol Rhinol Laryngol. 2010;119(6):412–23.PubMed Li NY, Vodovotz Y, Hebda PA, Abbott KV. Biosimulation of inflammation and healing in surgically injured vocal folds. Ann Otol Rhinol Laryngol. 2010;119(6):412–23.PubMed
43.
go back to reference Li NY, Verdolini K, Clermont G, Mi Q, Rubinstein EN, Hebda PA, Vodovotz Y. A patient-specific in silico model of inflammation and healing tested in acute vocal fold injury. PLoS ONE. 2008;3(7):e2789.PubMedCrossRef Li NY, Verdolini K, Clermont G, Mi Q, Rubinstein EN, Hebda PA, Vodovotz Y. A patient-specific in silico model of inflammation and healing tested in acute vocal fold injury. PLoS ONE. 2008;3(7):e2789.PubMedCrossRef
44.
go back to reference Mi Q, Riviere B, Clermont G, Steed DL, Vodovotz Y. Agent-based model of inflammation and wound healing: insights into diabetic foot ulcer pathology and the role of transforming growth factor-beta1. Wound Repair Regen. 2007;15(5):671–82.PubMedCrossRef Mi Q, Riviere B, Clermont G, Steed DL, Vodovotz Y. Agent-based model of inflammation and wound healing: insights into diabetic foot ulcer pathology and the role of transforming growth factor-beta1. Wound Repair Regen. 2007;15(5):671–82.PubMedCrossRef
45.
go back to reference An G. In silico experiments of existing and hypothetical cytokine-directed clinical trials using agent-based modeling. Crit Care Med. 2004;32(10):2050–60.PubMedCrossRef An G. In silico experiments of existing and hypothetical cytokine-directed clinical trials using agent-based modeling. Crit Care Med. 2004;32(10):2050–60.PubMedCrossRef
46.
go back to reference An G. Introduction of an agent-based multi-scale modular architecture for dynamic knowledge representation of acute inflammation. Theor Biol Med Model. 2008;5:11.PubMedCrossRef An G. Introduction of an agent-based multi-scale modular architecture for dynamic knowledge representation of acute inflammation. Theor Biol Med Model. 2008;5:11.PubMedCrossRef
47.
go back to reference An G, Mi Q, Dutta-Moscato J, Vodovotz Y. Agent-based models in translational systems biology. Wiley Interdiscip Rev Syst Biol Med. 2009;1(2):159–71.PubMedCrossRef An G, Mi Q, Dutta-Moscato J, Vodovotz Y. Agent-based models in translational systems biology. Wiley Interdiscip Rev Syst Biol Med. 2009;1(2):159–71.PubMedCrossRef
48.
go back to reference Kim M, Christley S, Alverdy JC, Liu D, An G. Immature oxidative stress management as a unifying principle in the pathogenesis of necrotizing enterocolitis: insights from an agent-based model. Surg Infect (Larchmt). 2012;13(1):18–32.CrossRef Kim M, Christley S, Alverdy JC, Liu D, An G. Immature oxidative stress management as a unifying principle in the pathogenesis of necrotizing enterocolitis: insights from an agent-based model. Surg Infect (Larchmt). 2012;13(1):18–32.CrossRef
49.
go back to reference Seal JB, Alverdy JC, Zaborina O, An G. Agent-based dynamic knowledge representation of Pseudomonas aeruginosa virulence activation in the stressed gut: towards characterizing host-pathogen interactions in gut-derived sepsis. Theor Biol Med Model. 2011;8:33.PubMedCrossRef Seal JB, Alverdy JC, Zaborina O, An G. Agent-based dynamic knowledge representation of Pseudomonas aeruginosa virulence activation in the stressed gut: towards characterizing host-pathogen interactions in gut-derived sepsis. Theor Biol Med Model. 2011;8:33.PubMedCrossRef
50.
go back to reference Mi Q, Constantine G, Ziraldo C, Solovyev A, Torres A, Namas R, Bentley T, Billiar TR, Zamora R, Puyana JC, Vodovotz Y. A dynamic view of trauma/hemorrhage-induced inflammation in mice: principal drivers and networks. PLoS ONE. 2011;6(5):e19424.PubMedCrossRef Mi Q, Constantine G, Ziraldo C, Solovyev A, Torres A, Namas R, Bentley T, Billiar TR, Zamora R, Puyana JC, Vodovotz Y. A dynamic view of trauma/hemorrhage-induced inflammation in mice: principal drivers and networks. PLoS ONE. 2011;6(5):e19424.PubMedCrossRef
51.
go back to reference Calvano SE, Xiao W, Richards DR, Felciano RM, Baker HV, Cho RJ, Chen RO, Brownstein BH, Cobb JP, Tschoeke SK, Miller-Graziano C, Moldawer LL, Mindrinos MN, Davis RW, Tompkins RG, Lowry SF. A network-based analysis of systemic inflammation in humans. Nature. 2005;437(7061):1032–7.PubMedCrossRef Calvano SE, Xiao W, Richards DR, Felciano RM, Baker HV, Cho RJ, Chen RO, Brownstein BH, Cobb JP, Tschoeke SK, Miller-Graziano C, Moldawer LL, Mindrinos MN, Davis RW, Tompkins RG, Lowry SF. A network-based analysis of systemic inflammation in humans. Nature. 2005;437(7061):1032–7.PubMedCrossRef
52.
go back to reference Yang EH, Almon RR, Dubois DC, Jusko WJ, Androulakis IP. Identification of global transcriptional dynamics. PLoS ONE. 2009;4(7):e5992.PubMedCrossRef Yang EH, Almon RR, Dubois DC, Jusko WJ, Androulakis IP. Identification of global transcriptional dynamics. PLoS ONE. 2009;4(7):e5992.PubMedCrossRef
53.
go back to reference Aldridge BB, Burke JM, Lauffenburger DA, Sorger PK. Physicochemical modelling of cell signalling pathways. Nat Cell Biol. 2006;8(11):1195–203.PubMedCrossRef Aldridge BB, Burke JM, Lauffenburger DA, Sorger PK. Physicochemical modelling of cell signalling pathways. Nat Cell Biol. 2006;8(11):1195–203.PubMedCrossRef
54.
go back to reference Webster JI, Tonelli L, Sternberg EM. Neuroendocrine regulation of immunity. Annu Rev Immunol. 2002;20:125–63.PubMedCrossRef Webster JI, Tonelli L, Sternberg EM. Neuroendocrine regulation of immunity. Annu Rev Immunol. 2002;20:125–63.PubMedCrossRef
55.
go back to reference Padgett DA, Glaser R. How stress influences the immune response. Trends Immunol. 2003;24(8):444–8.PubMedCrossRef Padgett DA, Glaser R. How stress influences the immune response. Trends Immunol. 2003;24(8):444–8.PubMedCrossRef
56.
go back to reference Elenkov IJ, Wilder RL, Chrousos GP, Vizi ES. The sympathetic nerve–an integrative interface between two super systems: the brain and the immune system. Pharmacol Rev. 2000;52(4):595–638.PubMed Elenkov IJ, Wilder RL, Chrousos GP, Vizi ES. The sympathetic nerve–an integrative interface between two super systems: the brain and the immune system. Pharmacol Rev. 2000;52(4):595–638.PubMed
57.
go back to reference van der Poll T, Coyle SM, Barbosa K, Braxton CC, Lowry SF. Epinephrine inhibits tumor necrosis factor-alpha and potentiates interleukin 10 production during human endotoxemia. J Clin Invest. 1996;97(3):713–9.PubMedCrossRef van der Poll T, Coyle SM, Barbosa K, Braxton CC, Lowry SF. Epinephrine inhibits tumor necrosis factor-alpha and potentiates interleukin 10 production during human endotoxemia. J Clin Invest. 1996;97(3):713–9.PubMedCrossRef
58.
go back to reference van der Poll T. Effects of Catecholamines on the Inflammatory Response. Sepsis. 2000;4:159–67.CrossRef van der Poll T. Effects of Catecholamines on the Inflammatory Response. Sepsis. 2000;4:159–67.CrossRef
59.
go back to reference Pavlov VA, Wang H, Czura CJ, Friedman SG, Tracey KJ. The cholinergic anti-inflammatory pathway: a missing link in neuroimmunomodulation. Mol Med. 2003;9(5–8):125–34.PubMed Pavlov VA, Wang H, Czura CJ, Friedman SG, Tracey KJ. The cholinergic anti-inflammatory pathway: a missing link in neuroimmunomodulation. Mol Med. 2003;9(5–8):125–34.PubMed
60.
go back to reference Alvarez SM, Katsamanis Karavidas M, Coyle SM, Lu SE, Macor M, Oikawa LO, Lehrer PM, Calvano SE, Lowry SF. Low-dose steroid alters in vivo endotoxin-induced systemic inflammation but does not influence autonomic dysfunction. J Endotoxin Res. 2007;13(6):358–68.PubMedCrossRef Alvarez SM, Katsamanis Karavidas M, Coyle SM, Lu SE, Macor M, Oikawa LO, Lehrer PM, Calvano SE, Lowry SF. Low-dose steroid alters in vivo endotoxin-induced systemic inflammation but does not influence autonomic dysfunction. J Endotoxin Res. 2007;13(6):358–68.PubMedCrossRef
61.
go back to reference van der Poll T, Barber AE, Coyle SM, Lowry SF. Hypercortisolemia increases plasma interleukin-10 concentrations during human endotoxemia–a clinical research center study. J Clin Endocrinol Metab. 1996;81(10):3604–6.PubMedCrossRef van der Poll T, Barber AE, Coyle SM, Lowry SF. Hypercortisolemia increases plasma interleukin-10 concentrations during human endotoxemia–a clinical research center study. J Clin Endocrinol Metab. 1996;81(10):3604–6.PubMedCrossRef
62.
go back to reference Jan BU, Coyle SM, Oikawa LO, Lu SE, Calvano SE, Lehrer PM, Lowry SF. Influence of acute epinephrine infusion on endotoxin-induced parameters of heart rate variability: a randomized controlled trial. Ann Surg. 2009;249(5):750–6.PubMedCrossRef Jan BU, Coyle SM, Oikawa LO, Lu SE, Calvano SE, Lehrer PM, Lowry SF. Influence of acute epinephrine infusion on endotoxin-induced parameters of heart rate variability: a randomized controlled trial. Ann Surg. 2009;249(5):750–6.PubMedCrossRef
63.
go back to reference Ramakrishnan R, DuBois DC, Almon RR, Pyszczynski NA, Jusko WJ. Fifth-generation model for corticosteroid pharmacodynamics: application to steady-state receptor down-regulation and enzyme induction patterns during seven-day continuous infusion of methylprednisolone in rats. J Pharmacokinet Pharmacodyn. 2002;29(1):1–24.PubMedCrossRef Ramakrishnan R, DuBois DC, Almon RR, Pyszczynski NA, Jusko WJ. Fifth-generation model for corticosteroid pharmacodynamics: application to steady-state receptor down-regulation and enzyme induction patterns during seven-day continuous infusion of methylprednisolone in rats. J Pharmacokinet Pharmacodyn. 2002;29(1):1–24.PubMedCrossRef
64.
65.
go back to reference Haimovich B, Calvano J, Haimovich AD, Calvano SE, Coyle SM, Lowry SF. In vivo endotoxin synchronizes and suppresses clock gene expression in human peripheral blood leukocytes. Crit Care Med. 2010;38(3):751–8.PubMedCrossRef Haimovich B, Calvano J, Haimovich AD, Calvano SE, Coyle SM, Lowry SF. In vivo endotoxin synchronizes and suppresses clock gene expression in human peripheral blood leukocytes. Crit Care Med. 2010;38(3):751–8.PubMedCrossRef
66.
go back to reference Pollmacher T, Mullington J, Korth C, Schreiber W, Hermann D, Orth A, Galanos C, Holsboer F. Diurnal variations in the human host response to endotoxin. J Infect Dis. 1996;174(5):1040–5.PubMedCrossRef Pollmacher T, Mullington J, Korth C, Schreiber W, Hermann D, Orth A, Galanos C, Holsboer F. Diurnal variations in the human host response to endotoxin. J Infect Dis. 1996;174(5):1040–5.PubMedCrossRef
67.
go back to reference Chakraborty A, Krzyzanski W, Jusko WJ. Mathematical modeling of circadian cortisol concentrations using indirect response models: comparison of several methods. J Pharmacokinet Biopharm. 1999;27(1):23–43.PubMedCrossRef Chakraborty A, Krzyzanski W, Jusko WJ. Mathematical modeling of circadian cortisol concentrations using indirect response models: comparison of several methods. J Pharmacokinet Biopharm. 1999;27(1):23–43.PubMedCrossRef
68.
go back to reference Lightman SL, Conway-Campbell BL. The crucial role of pulsatile activity of the HPA axis for continuous dynamic equilibration. Nat Rev Neurosci. 2010;11(10):710–8.PubMedCrossRef Lightman SL, Conway-Campbell BL. The crucial role of pulsatile activity of the HPA axis for continuous dynamic equilibration. Nat Rev Neurosci. 2010;11(10):710–8.PubMedCrossRef
69.
go back to reference McNally JG, Muller WG, Walker D, Wolford R, Hager GL. The glucocorticoid receptor: rapid exchange with regulatory sites in living cells. Science. 2000;287(5456):1262–5.PubMedCrossRef McNally JG, Muller WG, Walker D, Wolford R, Hager GL. The glucocorticoid receptor: rapid exchange with regulatory sites in living cells. Science. 2000;287(5456):1262–5.PubMedCrossRef
70.
go back to reference Stavreva DA, Wiench M, John S, Conway-Campbell BL, McKenna MA, Pooley JR, Johnson TA, Voss TC, Lightman SL, Hager GL. Ultradian hormone stimulation induces glucocorticoid receptor-mediated pulses of gene transcription. Nat Cell Biol. 2009;11(9):1093–102.PubMedCrossRef Stavreva DA, Wiench M, John S, Conway-Campbell BL, McKenna MA, Pooley JR, Johnson TA, Voss TC, Lightman SL, Hager GL. Ultradian hormone stimulation induces glucocorticoid receptor-mediated pulses of gene transcription. Nat Cell Biol. 2009;11(9):1093–102.PubMedCrossRef
71.
go back to reference McMaster A, Jangani M, Sommer P, Han N, Brass A, Beesley S, Lu W, Berry A, Loudon A, Donn R, Ray DW. Ultradian cortisol pulsatility encodes a distinct, biologically important signal. PLoS ONE. 2011;6(1):e15766.PubMedCrossRef McMaster A, Jangani M, Sommer P, Han N, Brass A, Beesley S, Lu W, Berry A, Loudon A, Donn R, Ray DW. Ultradian cortisol pulsatility encodes a distinct, biologically important signal. PLoS ONE. 2011;6(1):e15766.PubMedCrossRef
72.
go back to reference Scheff JD, Kosmides AK, Calvano SE, Lowry SF, Androulakis IP. Pulsatile glucocorticoid secretion: origins and downstream effects. IEEE Trans Biomed Eng. 2011;58(12):3504–7.PubMedCrossRef Scheff JD, Kosmides AK, Calvano SE, Lowry SF, Androulakis IP. Pulsatile glucocorticoid secretion: origins and downstream effects. IEEE Trans Biomed Eng. 2011;58(12):3504–7.PubMedCrossRef
73.
go back to reference Scheff JD, Calvano SE, Lowry SF, Androulakis IP. Transcriptional implications of ultradian glucocorticoid secretion in homeostasis and in the acute stress response. Physiol Genomics. 2012;44(2):121–9.PubMedCrossRef Scheff JD, Calvano SE, Lowry SF, Androulakis IP. Transcriptional implications of ultradian glucocorticoid secretion in homeostasis and in the acute stress response. Physiol Genomics. 2012;44(2):121–9.PubMedCrossRef
74.
go back to reference Schmidt HB, Werdan K, Muller-Werdan U. Autonomic dysfunction in the ICU patient. Curr Opin Crit Care. 2001;7(5):314–22.PubMedCrossRef Schmidt HB, Werdan K, Muller-Werdan U. Autonomic dysfunction in the ICU patient. Curr Opin Crit Care. 2001;7(5):314–22.PubMedCrossRef
75.
go back to reference Gholami M, Mazaheri P, Mohamadi A, Dehpour T, Safari F, Hajizadeh S, Moore KP, Mani AR. Endotoxemia is Associated With Partial Uncoupling of Cardiac Pacemaker From Cholinergic Neural Control in Rats. Shock. 2012;37(2):219–27.PubMedCrossRef Gholami M, Mazaheri P, Mohamadi A, Dehpour T, Safari F, Hajizadeh S, Moore KP, Mani AR. Endotoxemia is Associated With Partial Uncoupling of Cardiac Pacemaker From Cholinergic Neural Control in Rats. Shock. 2012;37(2):219–27.PubMedCrossRef
76.
go back to reference Godin PJ, Fleisher LA, Eidsath A, Vandivier RW, Preas HL, Banks SM, Buchman TG, Suffredini AF. Experimental human endotoxemia increases cardiac regularity: results from a prospective, randomized, crossover trial. Crit Care Med. 1996;24(7):1117–24.PubMedCrossRef Godin PJ, Fleisher LA, Eidsath A, Vandivier RW, Preas HL, Banks SM, Buchman TG, Suffredini AF. Experimental human endotoxemia increases cardiac regularity: results from a prospective, randomized, crossover trial. Crit Care Med. 1996;24(7):1117–24.PubMedCrossRef
77.
go back to reference Rassias AJ, Guyre PM, Yeager MP. Hydrocortisone at stress-associated concentrations helps maintain human heart rate variability during subsequent endotoxin challenge. J Crit Care. 2011;26(6):636.e1–5. Rassias AJ, Guyre PM, Yeager MP. Hydrocortisone at stress-associated concentrations helps maintain human heart rate variability during subsequent endotoxin challenge. J Crit Care. 2011;26(6):636.e1–5.
78.
go back to reference Sayk F, Vietheer A, Schaaf B, Wellhoener P, Weitz G, Lehnert H, Dodt C. Endotoxemia causes central downregulation of sympathetic vasomotor tone in healthy humans. Am J Physiol Regul Integr Comp Physiol. 2008;295(3):R891–8.PubMedCrossRef Sayk F, Vietheer A, Schaaf B, Wellhoener P, Weitz G, Lehnert H, Dodt C. Endotoxemia causes central downregulation of sympathetic vasomotor tone in healthy humans. Am J Physiol Regul Integr Comp Physiol. 2008;295(3):R891–8.PubMedCrossRef
79.
go back to reference Jan BU, Coyle SM, Macor MA, Reddell M, Calvano SE, Lowry SF. Relationship of basal heart rate variability to in vivo cytokine responses after endotoxin exposure. Shock. 2010;33(4):363–8.PubMedCrossRef Jan BU, Coyle SM, Macor MA, Reddell M, Calvano SE, Lowry SF. Relationship of basal heart rate variability to in vivo cytokine responses after endotoxin exposure. Shock. 2010;33(4):363–8.PubMedCrossRef
80.
go back to reference Kox M, Ramakers BP, Pompe JC, van der Hoeven JG, Hoedemaekers CW, Pickkers P. Interplay between the acute inflammatory response and heart rate variability in healthy human volunteers. Shock. 2011;36(2):115–20.PubMedCrossRef Kox M, Ramakers BP, Pompe JC, van der Hoeven JG, Hoedemaekers CW, Pickkers P. Interplay between the acute inflammatory response and heart rate variability in healthy human volunteers. Shock. 2011;36(2):115–20.PubMedCrossRef
81.
go back to reference Akselrod S, Gordon D, Ubel FA, Shannon DC, Berger AC, Cohen RJ. Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science. 1981;213(4504):220–2. doi:10.1126/science.6166045.PubMedCrossRef Akselrod S, Gordon D, Ubel FA, Shannon DC, Berger AC, Cohen RJ. Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science. 1981;213(4504):220–2. doi:10.​1126/​science.​6166045.PubMedCrossRef
82.
go back to reference Task. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task force of the European society of cardiology and the North American society of pacing and electrophysiology. Circulation. 1996;93(5):1043–65.CrossRef Task. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task force of the European society of cardiology and the North American society of pacing and electrophysiology. Circulation. 1996;93(5):1043–65.CrossRef
83.
go back to reference Berntson GG, Bigger JT Jr, Eckberg DL, Grossman P, Kaufmann PG, Malik M, Nagaraja HN, Porges SW, Saul JP, Stone PH, van der Molen MW. Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology. 1997;34(6):623–48.PubMedCrossRef Berntson GG, Bigger JT Jr, Eckberg DL, Grossman P, Kaufmann PG, Malik M, Nagaraja HN, Porges SW, Saul JP, Stone PH, van der Molen MW. Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology. 1997;34(6):623–48.PubMedCrossRef
84.
go back to reference deBoer RW, Karemaker JM, Strackee J. Hemodynamic fluctuations and baroreflex sensitivity in humans: a beat-to-beat model. Am J Physiol. 1987;253(3 Pt 2):H680–9.PubMed deBoer RW, Karemaker JM, Strackee J. Hemodynamic fluctuations and baroreflex sensitivity in humans: a beat-to-beat model. Am J Physiol. 1987;253(3 Pt 2):H680–9.PubMed
85.
go back to reference Karemaker JM. Autonomic integration: the physiological basis of cardiovascular variability. J Physiol. 1999;517(Pt 2):316.PubMedCrossRef Karemaker JM. Autonomic integration: the physiological basis of cardiovascular variability. J Physiol. 1999;517(Pt 2):316.PubMedCrossRef
86.
go back to reference Dick TE, Molkov YI, Nieman G, Hsieh YH, Jacono FJ, Doyle J, Scheff JD, Calvano SE, Androulakis IP, An G, Vodovotz Y. Linking inflammation, cardiorespiratory variability, and neural control in acute inflammation via computational modeling. Front Physiol. 2012;3:222.PubMedCrossRef Dick TE, Molkov YI, Nieman G, Hsieh YH, Jacono FJ, Doyle J, Scheff JD, Calvano SE, Androulakis IP, An G, Vodovotz Y. Linking inflammation, cardiorespiratory variability, and neural control in acute inflammation via computational modeling. Front Physiol. 2012;3:222.PubMedCrossRef
87.
go back to reference Boyett MR, Honjo H, Kodama I. The sinoatrial node, a heterogeneous pacemaker structure. Cardiovasc Res. 2000;47(4):658–87.PubMedCrossRef Boyett MR, Honjo H, Kodama I. The sinoatrial node, a heterogeneous pacemaker structure. Cardiovasc Res. 2000;47(4):658–87.PubMedCrossRef
88.
go back to reference Stys A, Stys T. Current clinical applications of heart rate variability. Clin Cardiol. 1998;21(10):719–24.PubMedCrossRef Stys A, Stys T. Current clinical applications of heart rate variability. Clin Cardiol. 1998;21(10):719–24.PubMedCrossRef
89.
go back to reference Annane D, Trabold F, Sharshar T, Jarrin I, Blanc AS, Raphael JC, Gajdos P. Inappropriate sympathetic activation at onset of septic shock: a spectral analysis approach. Am J Respir Crit Care Med. 1999;160(2):458–65.PubMedCrossRef Annane D, Trabold F, Sharshar T, Jarrin I, Blanc AS, Raphael JC, Gajdos P. Inappropriate sympathetic activation at onset of septic shock: a spectral analysis approach. Am J Respir Crit Care Med. 1999;160(2):458–65.PubMedCrossRef
90.
91.
go back to reference Batchinsky AI, Skinner JE, Necsoiu C, Jordan BS, Weiss D, Cancio LC. New measures of heart-rate complexity: effect of chest trauma and hemorrhage. J Trauma. 2010;68(5):1178–85.PubMedCrossRef Batchinsky AI, Skinner JE, Necsoiu C, Jordan BS, Weiss D, Cancio LC. New measures of heart-rate complexity: effect of chest trauma and hemorrhage. J Trauma. 2010;68(5):1178–85.PubMedCrossRef
92.
go back to reference Cancio LC, Batchinsky AI, Salinas J, Kuusela T, Convertino VA, Wade CE, Holcomb JB. Heart-rate complexity for prediction of prehospital lifesaving interventions in trauma patients. J Trauma. 2008;65(4):813–9.PubMedCrossRef Cancio LC, Batchinsky AI, Salinas J, Kuusela T, Convertino VA, Wade CE, Holcomb JB. Heart-rate complexity for prediction of prehospital lifesaving interventions in trauma patients. J Trauma. 2008;65(4):813–9.PubMedCrossRef
93.
go back to reference Morris JA Jr, Norris PR, Waitman LR, Ozdas A, Guillamondegui OD, Jenkins JM. Adrenal insufficiency, heart rate variability, and complex biologic systems: a study of 1, 871 critically ill trauma patients. J Am Coll Surg. 2007;204(5):885–92. (discussion 892-883).PubMedCrossRef Morris JA Jr, Norris PR, Waitman LR, Ozdas A, Guillamondegui OD, Jenkins JM. Adrenal insufficiency, heart rate variability, and complex biologic systems: a study of 1, 871 critically ill trauma patients. J Am Coll Surg. 2007;204(5):885–92. (discussion 892-883).PubMedCrossRef
94.
go back to reference Riordan WP Jr, Norris PR, Jenkins JM, Morris JA Jr. Early loss of heart rate complexity predicts mortality regardless of mechanism, anatomic location, or severity of injury in 2178 trauma patients. J Surg Res. 2009;156(2):283–9.PubMedCrossRef Riordan WP Jr, Norris PR, Jenkins JM, Morris JA Jr. Early loss of heart rate complexity predicts mortality regardless of mechanism, anatomic location, or severity of injury in 2178 trauma patients. J Surg Res. 2009;156(2):283–9.PubMedCrossRef
95.
go back to reference Ahmad S, Ramsay T, Huebsch L, Flanagan S, McDiarmid S, Batkin I, McIntyre L, Sundaresan SR, Maziak DE, Shamji FM, Hebert P, Fergusson D, Tinmouth A, Seely AJ. Continuous multi-parameter heart rate variability analysis heralds onset of sepsis in adults. PLoS ONE. 2009;4(8):e6642.PubMedCrossRef Ahmad S, Ramsay T, Huebsch L, Flanagan S, McDiarmid S, Batkin I, McIntyre L, Sundaresan SR, Maziak DE, Shamji FM, Hebert P, Fergusson D, Tinmouth A, Seely AJ. Continuous multi-parameter heart rate variability analysis heralds onset of sepsis in adults. PLoS ONE. 2009;4(8):e6642.PubMedCrossRef
96.
go back to reference Fairchild KD, Srinivasan V, Moorman JR, Gaykema RP, Goehler LE. Pathogen-induced heart rate changes associated with cholinergic nervous system activation. Am J Physiol Regul Integr Comp Physiol. 2011;300(2):R330–9.PubMedCrossRef Fairchild KD, Srinivasan V, Moorman JR, Gaykema RP, Goehler LE. Pathogen-induced heart rate changes associated with cholinergic nervous system activation. Am J Physiol Regul Integr Comp Physiol. 2011;300(2):R330–9.PubMedCrossRef
97.
go back to reference Huang J, Wang Y, Jiang D, Zhou J, Huang X. The sympathetic-vagal balance against endotoxemia. J Neural Transm. 2010;117(6):729–35.PubMedCrossRef Huang J, Wang Y, Jiang D, Zhou J, Huang X. The sympathetic-vagal balance against endotoxemia. J Neural Transm. 2010;117(6):729–35.PubMedCrossRef
98.
go back to reference Schmidt H, Saworski J, Werdan K, Muller-Werdan U. Decreased beating rate variability of spontaneously contracting cardiomyocytes after co-incubation with endotoxin. J Endotoxin Res. 2007;13(6):339–42.PubMedCrossRef Schmidt H, Saworski J, Werdan K, Muller-Werdan U. Decreased beating rate variability of spontaneously contracting cardiomyocytes after co-incubation with endotoxin. J Endotoxin Res. 2007;13(6):339–42.PubMedCrossRef
99.
go back to reference Takayama K, Yuhki K, Ono K, Fujino T, Hara A, Yamada T, Kuriyama S, Karibe H, Okada Y, Takahata O, Taniguchi T, Iijima T, Iwasaki H, Narumiya S, Ushikubi F. Thromboxane A2 and prostaglandin F2alpha mediate inflammatory tachycardia. Nat Med. 2005;11(5):562–6.PubMedCrossRef Takayama K, Yuhki K, Ono K, Fujino T, Hara A, Yamada T, Kuriyama S, Karibe H, Okada Y, Takahata O, Taniguchi T, Iijima T, Iwasaki H, Narumiya S, Ushikubi F. Thromboxane A2 and prostaglandin F2alpha mediate inflammatory tachycardia. Nat Med. 2005;11(5):562–6.PubMedCrossRef
100.
go back to reference Godin PJ, Buchman TG. Uncoupling of biological oscillators: a complementary hypothesis concerning the pathogenesis of multiple organ dysfunction syndrome. Crit Care Med. 1996;24(7):1107–16.PubMedCrossRef Godin PJ, Buchman TG. Uncoupling of biological oscillators: a complementary hypothesis concerning the pathogenesis of multiple organ dysfunction syndrome. Crit Care Med. 1996;24(7):1107–16.PubMedCrossRef
101.
go back to reference Pincus SM. Greater signal regularity may indicate increased system isolation. Math Biosci. 1994;122(2):161–81.PubMedCrossRef Pincus SM. Greater signal regularity may indicate increased system isolation. Math Biosci. 1994;122(2):161–81.PubMedCrossRef
102.
go back to reference Lowry SF, Calvano SE. Challenges for modeling and interpreting the complex biology of severe injury and inflammation. J Leukoc Biol. 2008;83(3):553–7.PubMedCrossRef Lowry SF, Calvano SE. Challenges for modeling and interpreting the complex biology of severe injury and inflammation. J Leukoc Biol. 2008;83(3):553–7.PubMedCrossRef
104.
go back to reference Huston JM, Gallowitsch-Puerta M, Ochani M, Ochani K, Yuan R, Rosas-Ballina M, Ashok M, Goldstein RS, Chavan S, Pavlov VA, Metz CN, Yang H, Czura CJ, Wang H, Tracey KJ. Transcutaneous vagus nerve stimulation reduces serum high mobility group box 1 levels and improves survival in murine sepsis. Crit Care Med. 2007;35(12):2762–8.PubMedCrossRef Huston JM, Gallowitsch-Puerta M, Ochani M, Ochani K, Yuan R, Rosas-Ballina M, Ashok M, Goldstein RS, Chavan S, Pavlov VA, Metz CN, Yang H, Czura CJ, Wang H, Tracey KJ. Transcutaneous vagus nerve stimulation reduces serum high mobility group box 1 levels and improves survival in murine sepsis. Crit Care Med. 2007;35(12):2762–8.PubMedCrossRef
105.
go back to reference Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G, Schibler U. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science. 2000;289(5488):2344–7.PubMedCrossRef Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G, Schibler U. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science. 2000;289(5488):2344–7.PubMedCrossRef
106.
go back to reference Hashiramoto A, Yamane T, Tsumiyama K, Yoshida K, Komai K, Yamada H, Yamazaki F, Doi M, Okamura H, Shiozawa S. Mammalian clock gene Cryptochrome regulates arthritis via proinflammatory cytokine TNF-alpha. J Immunol. 2010;184(3):1560–5.PubMedCrossRef Hashiramoto A, Yamane T, Tsumiyama K, Yoshida K, Komai K, Yamada H, Yamazaki F, Doi M, Okamura H, Shiozawa S. Mammalian clock gene Cryptochrome regulates arthritis via proinflammatory cytokine TNF-alpha. J Immunol. 2010;184(3):1560–5.PubMedCrossRef
107.
go back to reference Motzkus D, Albrecht U, Maronde E. The human PER1 gene is inducible by interleukin-6. J Mol Neurosci. 2002;18(1–2):105–9.PubMedCrossRef Motzkus D, Albrecht U, Maronde E. The human PER1 gene is inducible by interleukin-6. J Mol Neurosci. 2002;18(1–2):105–9.PubMedCrossRef
108.
go back to reference Levi F, Schibler U. Circadian rhythms: mechanisms and therapeutic implications. Annu Rev Pharmacol Toxicol. 2007;47:593–628.PubMedCrossRef Levi F, Schibler U. Circadian rhythms: mechanisms and therapeutic implications. Annu Rev Pharmacol Toxicol. 2007;47:593–628.PubMedCrossRef
109.
go back to reference Mavroudis PD, Scheff JD, Calvano SE, Lowry SF, Androulakis IP. Entrainment of peripheral clock genes by cortisol. Physiol Genomics. 2012;44(11):607–21.PubMedCrossRef Mavroudis PD, Scheff JD, Calvano SE, Lowry SF, Androulakis IP. Entrainment of peripheral clock genes by cortisol. Physiol Genomics. 2012;44(11):607–21.PubMedCrossRef
110.
go back to reference Petrovsky N, Harrison LC. The chronobiology of human cytokine production. Int Rev Immunol. 1998;16(5–6):635–49.PubMedCrossRef Petrovsky N, Harrison LC. The chronobiology of human cytokine production. Int Rev Immunol. 1998;16(5–6):635–49.PubMedCrossRef
111.
go back to reference Donadio V, Cortelli P, Falzone F, Bugiardini E, Giuliani A, Misciali C, Montagna P, Calza L, Liguori R. Isolated generalised anhidrosis induced by postganglionic sympathetic skin nerve fibre degeneration: an incomplete Ross syndrome? J Neurol Neurosurg Psychiatry. 2008;79(8):959–61.PubMedCrossRef Donadio V, Cortelli P, Falzone F, Bugiardini E, Giuliani A, Misciali C, Montagna P, Calza L, Liguori R. Isolated generalised anhidrosis induced by postganglionic sympathetic skin nerve fibre degeneration: an incomplete Ross syndrome? J Neurol Neurosurg Psychiatry. 2008;79(8):959–61.PubMedCrossRef
112.
go back to reference Brown EN, Meehan PM, Dempster AP. A stochastic differential equation model of diurnal cortisol patterns. Am J Physiol Endocrinol Metab. 2001;280(3):E450–61.PubMed Brown EN, Meehan PM, Dempster AP. A stochastic differential equation model of diurnal cortisol patterns. Am J Physiol Endocrinol Metab. 2001;280(3):E450–61.PubMed
113.
go back to reference Charloux A, Gronfier C, Lonsdorfer-Wolf E, Piquard F, Brandenberger G. Aldosterone release during the sleep-wake cycle in humans. Am J Physiol. 1999;276(1 Pt 1):E43–9.PubMed Charloux A, Gronfier C, Lonsdorfer-Wolf E, Piquard F, Brandenberger G. Aldosterone release during the sleep-wake cycle in humans. Am J Physiol. 1999;276(1 Pt 1):E43–9.PubMed
114.
go back to reference Seydnejad SR, Kitney RI. Modeling of Mayer waves generation mechanisms. IEEE Eng Med Biol Mag. 2001;20(2):92–100.PubMedCrossRef Seydnejad SR, Kitney RI. Modeling of Mayer waves generation mechanisms. IEEE Eng Med Biol Mag. 2001;20(2):92–100.PubMedCrossRef
115.
go back to reference Octavio JA, Rodriguez AE, Misticchio F, Marcano A, Jimenez J, Moleiro F. Circadian profiles of heart rate and its instantaneous variability in patients with chronic Chagas’ disease. Rev Esp Cardiol. 2004;57(2):130–7.PubMedCrossRef Octavio JA, Rodriguez AE, Misticchio F, Marcano A, Jimenez J, Moleiro F. Circadian profiles of heart rate and its instantaneous variability in patients with chronic Chagas’ disease. Rev Esp Cardiol. 2004;57(2):130–7.PubMedCrossRef
Metadata
Title
Translational applications of evaluating physiologic variability in human endotoxemia
Authors
Jeremy D. Scheff
Panteleimon D. Mavroudis
Steve E. Calvano
Ioannis P. Androulakis
Publication date
01-08-2013
Publisher
Springer Netherlands
Published in
Journal of Clinical Monitoring and Computing / Issue 4/2013
Print ISSN: 1387-1307
Electronic ISSN: 1573-2614
DOI
https://doi.org/10.1007/s10877-012-9418-1

Other articles of this Issue 4/2013

Journal of Clinical Monitoring and Computing 4/2013 Go to the issue