Modeling physiologic variability in human endotoxemia

Critical Reviews in Biomedical Engineering

Volumn 40, Issue 4, 2012, Pages 313-322

  Scheff, Jeremy D ^a   Mavroudis, Panteleimon D ^b   Foteinou, Panagiota T ^a,d   Calvano, Steve E ^c   Androulakis, Ioannis P ^a,b,c  

^a RUTGERS UNIVERSITY   (United States)

^b The State University of New Jersey   (United States)

^c ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^d Johns Hopkins University   (United States)

Author keywords

Inflammation; Mathematical modeling; Systems biology

Indexed keywords

BIOLOGICAL RHYTHM; CIRCADIAN RHYTHMS; CLINICAL CARE; CONTROL AND MANAGEMENT; DELETERIOUS EFFECTS; GAIN INSIGHT; HEART RATE VARIABILITY; HIGH FREQUENCY HF; INFLAMMATION; INFLAMMATORY MEDIATORS; INFLAMMATORY RESPONSE; PHYSIOLOGICAL PROCESS; SYSTEMIC INFLAMMATION; SYSTEMS BIOLOGY; TIME-SCALES;

MATHEMATICAL MODELS; PATHOLOGY;

PHYSIOLOGY;

ARTICLE; BIOLOGICAL RHYTHM; CIRCADIAN RHYTHM; CONTROLLED STUDY; DISEASE MODEL; ENDOTOXEMIA; HEART RATE VARIABILITY; HIGH FREQUENCY OSCILLATION; INFLAMMATION; MATHEMATICAL MODEL; MEDIATOR RELEASE; PHYSIOLOGY; PRIORITY JOURNAL; SYSTEMS BIOLOGY; TIME SERIES ANALYSIS; TRANSCRIPTION REGULATION; TRANSLATIONAL RESEARCH;

COMPUTER SIMULATION; CYTOKINES; ENDOTOXEMIA; HUMANS; MODELS, IMMUNOLOGICAL; MODELS, STATISTICAL;

EID: 84868328019     PISSN: 0278940X     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevBiomedEng.v40.i4.60     Document Type: Article

References (80)

1. Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med. 2003 Apr 17;348(16):1546-54.
2. Angus DC. The search for effective therapy for sepsis: back to the drawing board? JAMA. 2011 Dec 21;306(23):2614-5.
3. Decker T. Sepsis: avoiding its deadly toll. J Clin Invest. 2004 May;113(10):1387-9.
4. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med. 2001 Jul;29(7): 1303-10.
5. Kochanek KD, Smith BL. Deaths: preliminary data for 2002. Natl Vital Stat Rep. 2004 Feb 11;52(13):1-47.
6. Lowry SF. The stressed host response to infection: the disruptive signals and rhythms of systemic inflammation. Surg Clin North Am. 2009 Apr;89(2):311-26, vii.
7. Lowry SF. Human endotoxemia: a model for mechanistic insight and therapeutic targeting. Shock. 2005 Dec;24 Suppl 1:94-100.
8. Godin PJ, Buchman TG. Uncoupling of biological oscillators: a complementary hypothesis concerning the pathogenesis of multiple organ dysfunction syndrome. Crit Care Med. 1996 Jul;24(7):1107-16.
9. Rassias AJ, Holzberger PT, Givan AL, Fahrner SL, Yeager MR Decreased physiologic variability as a generalized response to human endotoxemia. Crit Care Med. 2005 Mar;33(3):512-9.
10. 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 Mar;38(3):751-8.
11. 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 Jul;24(7):1117-24.
12. 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.
13. Buttenschoen K, Kornmann M, Berger D, Leder G, Beger HG, Vasilescu C. Endotoxemia and endotoxin tolerance in patients with ARDS. Langenbecks Arch Surg. 2008 Jul;393(4):473-8.
14. Shanker B-A, Coyle SM, Reddell MT, Choi CW, Calvano J, Macor MA, Calvano SE, Lowry SF. Modeling the human injury response. Journal of the American College of Surgeons.211(3, Supplement 1):553-4.
15. Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. Modeling endotoxin-induced systemic inflammation using an indirect response approach. Math Biosci. 2009 Jan;217(1):27-42.
16. Tracey KJ. The inflammatory reflex. Nature. 2002 Dec 19-26;420(6917):853-9.
17. Beishuizen A, Thijs LG. Endotoxin and the hypothalamo-pituitary-adrenal (HPA) axis. J Endotoxin Res. 2003;9(1):3-24.
18. Eckberg DL. Sympathovagal balance: a critical appraisal. Circulation. 1997 Nov 4;96(9):3224-32.
19. 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 May;68(5): 1178-85.
20. 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 Oct;65(4):813-9.
21. 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 May;204(5):885-92; discussion 92-3.
22. 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 Oct;156(2):283-9.
23. 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.
24. 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 Dec;159(6):900-6 e1.
25. Bravi A, Longtin A, Seely AJ. Review and classification of variability analysis techniques with clinical applications. Biomed Eng Online. 2011 Oct 10;10(1):90.
26. 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 Feb;37(2):219-27.
27. 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 Apr 20;26(6):636.e1-5.
28. 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 Sep;295(3):R891-8.
29. 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.
30. 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 May;249(5):750-6.
31. 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 Apr;33(4):363-8.
32. 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 Aug;36(2):115-20.
33. Lowry SF, Calvano SE. Challenges for modeling and interpreting the complex biology of severe injury and inflammation. J Leukoc Biol. 2008 Mar;83(3):553-7.
34. Pincus SM. Greater signal regularity may indicate increased system isolation. Math Biosci. 1994 Aug;122(2): 161-81.
35. Levi F, Schibler U. Circadian rhythms: mechanisms and therapeutic implications. Annu Rev Pharmacol Toxicol. 2007;47:593-628.
36. Mavroudis PD, Scheff JD, Calvano SE, Lowry SF, Androulakis IP. Entrainment of peripheral clock genes by cortisol. Physiol Genomics. 2012 Jun 1;44(11):607-21.
37. Bone RC. Immunologic dissonance: a continuing evolution in our understanding of the systemic inflammatory response syndrome (SIRS) and the multiple organ dysfunction syndrome (MODS). Ann Intern Med. 1996 Oct 15;125(8):680-7.
38. Deans KJ, Haley M, Natanson C, Eichacker PQ, Minneci PC. Novel therapies for sepsis: a review. J Trauma. 2005 Apr;58(4):867-74.
39. Marshall JC. Such stuff as dreams are made on: mediator-directed therapy in sepsis. Nat Rev Drug Discov. 2003 May;2(5):391-405.
40. Freeman BD, Natanson C. Anti-inflammatory therapies in sepsis and septic shock. Expert Opin Investig Drugs. 2000 Ju1;9(7):1651-63.
41. Seely AJ, Christou NV. Multiple organ dysfunction syndrome: exploring the paradigm of complex nonlinear systems. Crit Care Med. 2000 Jul;28(7):2193-200.
42. Vodovotz Y, Clermont G, Chow C, An G. Mathematical models of the acute inflammatory response. Curr Opin Crit Care. 2004 Oct;10(5):383-90.
43. Vodovotz Y, Constantine G, Rubin J, Csete M, Voit EO, An G. Mechanistic simulations of inflammation: current state and future prospects. Math Biosci. 2009 Jan;217(1):1-10.
44. Sontag ED. Some new directions in control theory inspired by systems biology. Syst Biol (Stevenage). 2004 Jun;1(1):9-18.
45. Rajasethupathy P, Vayttaden SJ, Bhalla US. Systems modeling: a pathway to drug discovery. Curr Opin Chem Biol. 2005 Aug;9(4):400-6.
46. Kitano H. Systems biology: a brief overview. Science. 2002 Mar 1;295(5560):1662-4.
47. Kumar R, Clermont G, Vodovotz Y, Chow CC. The dynamics of acute inflammation. J Theor Biol. 2004;230(2):145-55.
48. 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 Sep 7;242(1):237-56.
49. 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 Sep 7;242(1):220-36.
50. 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.
51. 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.
52. Vodovotz Y, Csete M, Bartels J, Chang S, An G. Translational systems biology of inflammation. PLoS Comput Biol. 2008 Apr;4(4):e1000014.
53. Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. Translational potential of systems-based models of inflammation. Clin Transl Sci. 2009;2(1):85-9.
54. 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 Jul 26;27(3):314.e1-11.
55. 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 Oct 13;437(7061):1032-7.
56. 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 Feb;29(1):1-24.
57. 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 Feb 1;97(3):713-9.
58. 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 Oct;81(10):3604-6.
59. 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.
60. 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 Aug;232(2):151-63.
61. Scheff JD, Calvano SE, Lowry SF, Androulakis IP. Modeling the influence of circadian rhythms on the acute inflammatory response. J Theor Biol. 2010 Jun 7;264(3): 1068-76.
62. Scheff JD, Kosmides AK, Calvano SE, Lowry SF, Androulakis IP. Pulsatile glucocorticoid secretion: origins and downstream effects. IEEE Trans Biomed Eng. 2011 Dec;58(12):3504-7.
63. 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 Feb 1;44(2):121-9.
64. 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.
65. Foteinou PT, Calvano SE, Lowry SF, Androulakis IP. Multiscale model for the assessment of autonomic dysfunction in human endotoxemia. Physiol Genomics. 2010 Jun;42(1):5-19.
66. Scheff JD, Mavroudis PD, Calvano SE, Lowry SF, Androulakis IP. Modeling autonomic regulation of cardiac function and heart rate variability in human endotox emia. Physiol Genomics. 2011 Aug 24;43(16):951-64.
67. Yang EH, Almon RR, Dubois DC, Jusko WJ, Androulakis IP. Identification of global transcriptional dynamics. PLoS One. 2009;4(7):e5992.
68. Aldridge BB, Burke JM, Lauffenburger DA, Sorger PK. Physicochemical modelling of cell signalling pathways. Nat Cell Biol. 2006 Nov;8(11):1195-203.
69. Jusko WJ, Ko HC. Physiologic indirect response models characterize diverse types of pharmacodynamic effects. Clin Pharmacol Ther. 1994 Oct;56(4):406-19.
70. Coogan AN, Wyse CA. Neuroimmunology of the circadian clock. Brain Res. 2008 Sep 26;1232:104-12.
71. Chakraborty A, Krzyzanski W, Jusko WJ. Mathematical modeling of circadian cortisol concentrations using indirect response models: Comparison of several methods. J Pharmacokinet Biopharmaceut. 1999 Feb;27(1):23-43.
72. Lightman SL, Conway-Campbell BL. The crucial role of pulsatile activity of the HPA axis for continuous dynamic equilibration. Nat Rev Neurosci. 2010 Oct;11(10):710-8.
73. McNally JG, Muller WG, Walker D, Wolford R, Hager GL. The glucocorticoid receptor: rapid exchange with regulatory sites in living cells. Science. 2000 Feb 18;287(5456):1262-5.
74. 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 Sep;11(9):1093-102.
75. 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.
76. Walker JJ, Terry JR, Lightman SL. Origin of ultradian pulsatility in the hypothalamic-pituitary-adrenal axis. Proc Biol Sci. 2010 Jun 7;277(1688):1627-33.
77. Yao Z, DuBois DC, Almon RR, Jusko WJ. Modeling circadian rhythms of glucocorticoid receptor and glutamine synthetase expression in rat skeletal muscle. Pharm Res. 2006 Apr;23(4):670-9.
78. Schmidt HB, Werdan K, Muller-Werdan U. Autonomic dysfunction in the ICU patient. Curr Opin Crit Care. 2001 Oct;7(5):314-22.
79. 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 Mar 1;93(5):1043-65.
80. 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 Nov;34(6):623-48.