Skip to main content
Top
Published in: Heart and Vessels 3/2011

01-05-2011 | Original Article

Impact of serum high-mobility group box 1 protein elevation on oxygenation impairment after thoracic aortic aneurysm repair

Authors: Takashi Kohno, Toshihisa Anzai, Hideyuki Shimizu, Hidehiro Kaneko, Yasuo Sugano, Shingo Yamada, Tsutomu Yoshikawa, Akitoshi Ishizaka, Ryohei Yozu, Satoshi Ogawa

Published in: Heart and Vessels | Issue 3/2011

Login to get access

Abstract

High-mobility group box 1 protein (HMGB1) is a late mediator of inflammatory responses that can cause acute lung injury. We examined the significance of serum HMGB1 elevation in the development of systemic inflammatory response syndrome (SIRS) and lung oxygenation impairment (LOI) after thoracic aortic aneurysm (TAA) repair. Serial measurements of the serum HMGB1 level and SIRS score for 7 days after surgery were determined in 20 patients with TAA who underwent surgical repair. Arterial oxygen tension was measured serially for at least 4 days after surgery, and LOI was defined as the lowest PaO2/FiO2 ratio ≤200 mmHg. The serum HMGB1 level was markedly increased after surgery, peaking on day 2, and remained significantly elevated on day 7. Peak HMGB1 level positively correlated with SIRS duration and the cumulative SIRS score during postoperative days 1–7 (P = 0.0013 and P = 0.0004, respectively). Peak HMGB1 level and cumulative SIRS score were higher in patients with LOI than in those without (P = 0.01 and P = 0.044, respectively). Peak HMGB1 level was negatively correlated with the lowest PaO2/FiO2 ratio (P = 0.0077) and positively correlated with postoperative length of hospitalization (P = 0.042). A greater serum HMGB1 elevation after TAA repair was associated with more severe SIRS and a higher incidence of LOI. HMGB1 might play a key role in the pathogenesis of SIRS and LOI after surgical TAA repair.
Literature
1.
go back to reference Welborn MB, Oldenburg HS, Hess PJ, Huber TS, Martin TD, Rauwerda JA, Wesdorp RI, Espat NJ, Copeland EM 3rd, Moldawer LL, Seeger JM (2000) The relationship between visceral ischemia, proinflammatory cytokines, and organ injury in patients undergoing thoracoabdominal aortic aneurysm repair. Crit Care Med 28:3191–3197PubMedCrossRef Welborn MB, Oldenburg HS, Hess PJ, Huber TS, Martin TD, Rauwerda JA, Wesdorp RI, Espat NJ, Copeland EM 3rd, Moldawer LL, Seeger JM (2000) The relationship between visceral ischemia, proinflammatory cytokines, and organ injury in patients undergoing thoracoabdominal aortic aneurysm repair. Crit Care Med 28:3191–3197PubMedCrossRef
2.
go back to reference Roumen RM, Hendriks T, van der Ven-Jongekrijg J, Nieuwenhuijzen GA, Sauerwein RW, van der Meer JW, Goris RJ (1993) Cytokine patterns in patients after major vascular surgery, hemorrhagic shock, and severe blunt trauma. Relation with subsequent adult respiratory distress syndrome and multiple organ failure. Ann Surg 218:769–776PubMedCrossRef Roumen RM, Hendriks T, van der Ven-Jongekrijg J, Nieuwenhuijzen GA, Sauerwein RW, van der Meer JW, Goris RJ (1993) Cytokine patterns in patients after major vascular surgery, hemorrhagic shock, and severe blunt trauma. Relation with subsequent adult respiratory distress syndrome and multiple organ failure. Ann Surg 218:769–776PubMedCrossRef
3.
go back to reference Shindo S, Ogata K, Kubota K, Kojima A, Kobayashi M, Tada Y, Okuyama K (2003) Vascular prosthetic implantation is associated with prolonged inflammation following aortic aneurysm surgery. J Artif Organs 6:173–178PubMedCrossRef Shindo S, Ogata K, Kubota K, Kojima A, Kobayashi M, Tada Y, Okuyama K (2003) Vascular prosthetic implantation is associated with prolonged inflammation following aortic aneurysm surgery. J Artif Organs 6:173–178PubMedCrossRef
4.
go back to reference Fiane AE, Videm V, Lingaas PS, Heggelund L, Nielsen EW, Geiran OR, Fung M, Mollnes TE (2003) Mechanism of complement activation and its role in the inflammatory response after thoracoabdominal aortic aneurysm repair. Circulation 108:849–856PubMedCrossRef Fiane AE, Videm V, Lingaas PS, Heggelund L, Nielsen EW, Geiran OR, Fung M, Mollnes TE (2003) Mechanism of complement activation and its role in the inflammatory response after thoracoabdominal aortic aneurysm repair. Circulation 108:849–856PubMedCrossRef
5.
go back to reference Hanssen SJ, Derikx JP, Vermeulen Windsant IC, Heijmans JH, Koeppel TA, Schurink GW, Buurman WA, Jacobs MJ (2008) Visceral injury and systemic inflammation in patients undergoing extracorporeal circulation during aortic surgery. Ann Surg 248:117–125PubMedCrossRef Hanssen SJ, Derikx JP, Vermeulen Windsant IC, Heijmans JH, Koeppel TA, Schurink GW, Buurman WA, Jacobs MJ (2008) Visceral injury and systemic inflammation in patients undergoing extracorporeal circulation during aortic surgery. Ann Surg 248:117–125PubMedCrossRef
6.
go back to reference Norwood MG, Bown MJ, Lloyd G, Bell PR, Sayers RD (2004) The clinical value of the systemic inflammatory response syndrome (SIRS) in abdominal aortic aneurysm repair. Eur J Vasc Endovasc Surg 27:292–298PubMed Norwood MG, Bown MJ, Lloyd G, Bell PR, Sayers RD (2004) The clinical value of the systemic inflammatory response syndrome (SIRS) in abdominal aortic aneurysm repair. Eur J Vasc Endovasc Surg 27:292–298PubMed
7.
go back to reference Bustin M (1999) Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol Cell Biol 19:5237–5246PubMed Bustin M (1999) Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol Cell Biol 19:5237–5246PubMed
8.
go back to reference Lotze MT, Tracey KJ (2005) High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 5:331–342PubMedCrossRef Lotze MT, Tracey KJ (2005) High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 5:331–342PubMedCrossRef
9.
go back to reference Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, Manogue KR, Faist E, Abraham E, Andersson J, Andersson U, Molina PE, Abumrad NN, Sama A, Tracey KJ (1999) HMG-1 as a late mediator of endotoxin lethality in mice. Science 285:248–251PubMedCrossRef Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, Manogue KR, Faist E, Abraham E, Andersson J, Andersson U, Molina PE, Abumrad NN, Sama A, Tracey KJ (1999) HMG-1 as a late mediator of endotoxin lethality in mice. Science 285:248–251PubMedCrossRef
10.
go back to reference Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418:191–195PubMedCrossRef Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418:191–195PubMedCrossRef
11.
go back to reference Andersson U, Wang H, Palmblad K, Aveberger AC, Bloom O, Erlandsson-Harris H, Janson A, Kokkola R, Zhang M, Yang H, Tracey KJ (2000) High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med 192:565–570PubMedCrossRef Andersson U, Wang H, Palmblad K, Aveberger AC, Bloom O, Erlandsson-Harris H, Janson A, Kokkola R, Zhang M, Yang H, Tracey KJ (2000) High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med 192:565–570PubMedCrossRef
12.
go back to reference Kohno T, Anzai T, Naito K, Miyasho T, Okamoto M, Yokota H, Yamada S, Maekawa Y, Takahashi T, Yoshikawa T, Ishizaka A, Ogawa S (2009) Role of high-mobility group box 1 protein in post-infarction healing process and left ventricular remodelling. Cardiovasc Res 81:565–573PubMedCrossRef Kohno T, Anzai T, Naito K, Miyasho T, Okamoto M, Yokota H, Yamada S, Maekawa Y, Takahashi T, Yoshikawa T, Ishizaka A, Ogawa S (2009) Role of high-mobility group box 1 protein in post-infarction healing process and left ventricular remodelling. Cardiovasc Res 81:565–573PubMedCrossRef
13.
go back to reference Tsung A, Sahai R, Tanaka H, Nakao A, Fink MP, Lotze MT, Yang H, Li J, Tracey KJ, Geller DA, Billiar TR (2005) The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 201:1135–1143PubMedCrossRef Tsung A, Sahai R, Tanaka H, Nakao A, Fink MP, Lotze MT, Yang H, Li J, Tracey KJ, Geller DA, Billiar TR (2005) The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 201:1135–1143PubMedCrossRef
14.
go back to reference Levy RM, Mollen KP, Prince JM, Kaczorowski DJ, Vallabhaneni R, Liu S, Tracey KJ, Lotze MT, Hackam DJ, Fink MP, Vodovotz Y, Billiar TR (2007) Systemic inflammation and remote organ injury following trauma require HMGB1. Am J Physiol Regul Integr Comp Physiol 293:R1538–R1544PubMedCrossRef Levy RM, Mollen KP, Prince JM, Kaczorowski DJ, Vallabhaneni R, Liu S, Tracey KJ, Lotze MT, Hackam DJ, Fink MP, Vodovotz Y, Billiar TR (2007) Systemic inflammation and remote organ injury following trauma require HMGB1. Am J Physiol Regul Integr Comp Physiol 293:R1538–R1544PubMedCrossRef
15.
go back to reference Ueno H, Matsuda T, Hashimoto S, Amaya F, Kitamura Y, Tanaka M, Kobayashi A, Maruyama I, Yamada S, Hasegawa N, Soejima J, Koh H, Ishizaka A (2004) Contributions of high mobility group box protein in experimental and clinical acute lung injury. Am J Respir Crit Care Med 170:1310–1316PubMedCrossRef Ueno H, Matsuda T, Hashimoto S, Amaya F, Kitamura Y, Tanaka M, Kobayashi A, Maruyama I, Yamada S, Hasegawa N, Soejima J, Koh H, Ishizaka A (2004) Contributions of high mobility group box protein in experimental and clinical acute lung injury. Am J Respir Crit Care Med 170:1310–1316PubMedCrossRef
16.
go back to reference Suda K, Kitagawa Y, Ozawa S, Saikawa Y, Ueda M, Ebina M, Yamada S, Hashimoto S, Fukata S, Abraham E, Maruyama I, Kitajima M, Ishizaka A (2006) Anti-high-mobility group box chromosomal protein 1 antibodies improve survival of rats with sepsis. World J Surg 30:1755–1762PubMedCrossRef Suda K, Kitagawa Y, Ozawa S, Saikawa Y, Ueda M, Ebina M, Yamada S, Hashimoto S, Fukata S, Abraham E, Maruyama I, Kitajima M, Ishizaka A (2006) Anti-high-mobility group box chromosomal protein 1 antibodies improve survival of rats with sepsis. World J Surg 30:1755–1762PubMedCrossRef
17.
go back to reference Ogawa EN, Ishizaka A, Tasaka S, Koh H, Ueno H, Amaya F, Ebina M, Yamada S, Funakoshi Y, Soejima J, Moriyama K, Kotani T, Hashimoto S, Morisaki H, Abraham E, Takeda J (2006) Contribution of high-mobility group box-1 to the development of ventilator-induced lung injury. Am J Respir Crit Care Med 174:400–407PubMedCrossRef Ogawa EN, Ishizaka A, Tasaka S, Koh H, Ueno H, Amaya F, Ebina M, Yamada S, Funakoshi Y, Soejima J, Moriyama K, Kotani T, Hashimoto S, Morisaki H, Abraham E, Takeda J (2006) Contribution of high-mobility group box-1 to the development of ventilator-induced lung injury. Am J Respir Crit Care Med 174:400–407PubMedCrossRef
18.
go back to reference Kim JY, Park JS, Strassheim D, Douglas I, Diaz del Valle F, Asehnoune K, Mitra S, Kwak SH, Yamada S, Maruyama I, Ishizaka A, Abraham E (2005) HMGB1 contributes to the development of acute lung injury after hemorrhage. Am J Physiol Lung Cell Mol Physiol 288:L958–L965PubMedCrossRef Kim JY, Park JS, Strassheim D, Douglas I, Diaz del Valle F, Asehnoune K, Mitra S, Kwak SH, Yamada S, Maruyama I, Ishizaka A, Abraham E (2005) HMGB1 contributes to the development of acute lung injury after hemorrhage. Am J Physiol Lung Cell Mol Physiol 288:L958–L965PubMedCrossRef
19.
go back to reference Kim JB, Sig Choi J, Yu YM, Nam K, Piao CS, Kim SW, Lee MH, Han PL, Park JS, Lee JK (2006) HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J Neurosci 26:6413–6421PubMedCrossRef Kim JB, Sig Choi J, Yu YM, Nam K, Piao CS, Kim SW, Lee MH, Han PL, Park JS, Lee JK (2006) HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J Neurosci 26:6413–6421PubMedCrossRef
20.
go back to reference Milot J, Perron J, Lacasse Y, Letourneau L, Cartier PC, Maltais F (2001) Incidence and predictors of ARDS after cardiac surgery. Chest 119:884–888PubMedCrossRef Milot J, Perron J, Lacasse Y, Letourneau L, Cartier PC, Maltais F (2001) Incidence and predictors of ARDS after cardiac surgery. Chest 119:884–888PubMedCrossRef
21.
go back to reference Bone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, Knaus WA, Schein RM, Sibbald WJ (1992) Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 101:1644–1655PubMedCrossRef Bone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, Knaus WA, Schein RM, Sibbald WJ (1992) Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 101:1644–1655PubMedCrossRef
22.
go back to reference Yamada S, Inoue K, Yakabe K, Imaizumi H, Maruyama I (2003) High mobility group protein 1 (HMGB1) quantified by ELISA with a monoclonal antibody that does not cross-react with HMGB2. Clin Chem 49:1535–1537PubMedCrossRef Yamada S, Inoue K, Yakabe K, Imaizumi H, Maruyama I (2003) High mobility group protein 1 (HMGB1) quantified by ELISA with a monoclonal antibody that does not cross-react with HMGB2. Clin Chem 49:1535–1537PubMedCrossRef
23.
go back to reference Sugano Y, Anzai T, Yoshikawa T, Satoh T, Iwanaga S, Hayashi T, Maekawa Y, Shimizu H, Yozu R, Ogawa S (2005) Serum C-reactive protein elevation predicts poor clinical outcome in patients with distal type acute aortic dissection: association with the occurrence of oxygenation impairment. Int J Cardiol 102:39–45PubMedCrossRef Sugano Y, Anzai T, Yoshikawa T, Satoh T, Iwanaga S, Hayashi T, Maekawa Y, Shimizu H, Yozu R, Ogawa S (2005) Serum C-reactive protein elevation predicts poor clinical outcome in patients with distal type acute aortic dissection: association with the occurrence of oxygenation impairment. Int J Cardiol 102:39–45PubMedCrossRef
24.
go back to reference Bown MJ, Nicholson ML, Bell PR, Sayers RD (2003) The systemic inflammatory response syndrome, organ failure, and mortality after abdominal aortic aneurysm repair. J Vasc Surg 37:600–606PubMedCrossRef Bown MJ, Nicholson ML, Bell PR, Sayers RD (2003) The systemic inflammatory response syndrome, organ failure, and mortality after abdominal aortic aneurysm repair. J Vasc Surg 37:600–606PubMedCrossRef
25.
go back to reference Tan J, Hua Q, Li J, Fan Z (2009) Prognostic value of interleukin-6 during a 3-year follow-up in patients with acute ST-segment elevation myocardial infarction. Heart Vessels 24:329–334PubMedCrossRef Tan J, Hua Q, Li J, Fan Z (2009) Prognostic value of interleukin-6 during a 3-year follow-up in patients with acute ST-segment elevation myocardial infarction. Heart Vessels 24:329–334PubMedCrossRef
26.
go back to reference Jug B, Salobir BG, Vene N, Sebestjen M, Sabovic M, Keber I (2009) Interleukin-6 is a stronger prognostic predictor than high-sensitive C-reactive protein in patients with chronic stable heart failure. Heart Vessels 24:271–276PubMedCrossRef Jug B, Salobir BG, Vene N, Sebestjen M, Sabovic M, Keber I (2009) Interleukin-6 is a stronger prognostic predictor than high-sensitive C-reactive protein in patients with chronic stable heart failure. Heart Vessels 24:271–276PubMedCrossRef
27.
go back to reference Suda K, Kitagawa Y, Ozawa S, Saikawa Y, Ueda M, Abraham E, Kitajima M, Ishizaka A (2006) Serum concentrations of high-mobility group box chromosomal protein 1 before and after exposure to the surgical stress of thoracic esophagectomy: a predictor of clinical course after surgery? Dis Esophagus 19:5–9PubMedCrossRef Suda K, Kitagawa Y, Ozawa S, Saikawa Y, Ueda M, Abraham E, Kitajima M, Ishizaka A (2006) Serum concentrations of high-mobility group box chromosomal protein 1 before and after exposure to the surgical stress of thoracic esophagectomy: a predictor of clinical course after surgery? Dis Esophagus 19:5–9PubMedCrossRef
28.
go back to reference Dybdahl B, Wahba A, Lien E, Flo TH, Waage A, Qureshi N, Sellevold OF, Espevik T, Sundan A (2002) Inflammatory response after open heart surgery: release of heat-shock protein 70 and signaling through toll-like receptor-4. Circulation 105:685–690PubMedCrossRef Dybdahl B, Wahba A, Lien E, Flo TH, Waage A, Qureshi N, Sellevold OF, Espevik T, Sundan A (2002) Inflammatory response after open heart surgery: release of heat-shock protein 70 and signaling through toll-like receptor-4. Circulation 105:685–690PubMedCrossRef
29.
go back to reference Suda K, Kitagawa Y, Ozawa S, Miyasho T, Okamoto M, Saikawa Y, Ueda M, Yamada S, Tasaka S, Funakoshi Y, Hashimoto S, Yokota H, Maruyama I, Ishizaka A, Kitajima M (2007) Neutrophil elastase inhibitor improves postoperative clinical courses after thoracic esophagectomy. Dis Esophagus 20:478–486PubMedCrossRef Suda K, Kitagawa Y, Ozawa S, Miyasho T, Okamoto M, Saikawa Y, Ueda M, Yamada S, Tasaka S, Funakoshi Y, Hashimoto S, Yokota H, Maruyama I, Ishizaka A, Kitajima M (2007) Neutrophil elastase inhibitor improves postoperative clinical courses after thoracic esophagectomy. Dis Esophagus 20:478–486PubMedCrossRef
30.
go back to reference Suda K, Takeuchi H, Hagiwara T, Miyasho T, Okamoto M, Kawasako K, Yamada S, Suganuma K, Wada N, Saikawa Y, Fukunaga K, Funakoshi Y, Hashimoto S, Yokota H, Maruyama I, Ishizaka A, Kitagawa Y (2009) Neutrophil elastase inhibitor improves survival of rats with clinically relevant sepsis. Shock 33:526–531 Suda K, Takeuchi H, Hagiwara T, Miyasho T, Okamoto M, Kawasako K, Yamada S, Suganuma K, Wada N, Saikawa Y, Fukunaga K, Funakoshi Y, Hashimoto S, Yokota H, Maruyama I, Ishizaka A, Kitagawa Y (2009) Neutrophil elastase inhibitor improves survival of rats with clinically relevant sepsis. Shock 33:526–531
Metadata
Title
Impact of serum high-mobility group box 1 protein elevation on oxygenation impairment after thoracic aortic aneurysm repair
Authors
Takashi Kohno
Toshihisa Anzai
Hideyuki Shimizu
Hidehiro Kaneko
Yasuo Sugano
Shingo Yamada
Tsutomu Yoshikawa
Akitoshi Ishizaka
Ryohei Yozu
Satoshi Ogawa
Publication date
01-05-2011
Publisher
Springer Japan
Published in
Heart and Vessels / Issue 3/2011
Print ISSN: 0910-8327
Electronic ISSN: 1615-2573
DOI
https://doi.org/10.1007/s00380-010-0056-6

Other articles of this Issue 3/2011

Heart and Vessels 3/2011 Go to the issue