Comparison of carbamylated erythropoietin-FC fusion protein and recombinant human erythropoietin during porcine aortic balloon occlusion-induced spinal cord ischemia/reperfusion injury

Intensive Care Medicine

Volumn 37, Issue 9, 2011, Pages 1525-1533

  Simon, Florian ^a   Scheuerle, Angelika ^a   Gröger, Michael ^a   Vcelar, Brigitta ^b   McCook, Oscar ^a   Möller, Peter ^a   Georgieff, Michael ^a   Calzia, Enrico ^a   Radermacher, Peter ^a   Schelzig, Hubert ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b POLYMUN SCIENTIFIC IMMUNBIOLOGISCHE FORSCHUNG GMBH   (Austria)

Author keywords

8 Isoprostanes; Cytokines; Lower limb reflexes; Motor evoked potentials; Nissl staining; TUNEL staining

Indexed keywords

8 ISOPROSTANE; ADENOSINE TRIPHOSPHATE; CARBAMYLATED ERYTHROPOIETIN FC FUSION PROTEIN; EOSIN; ESMOLOL; GLYCERYL TRINITRATE; HEMATOXYLIN; HEPARIN; HYBRID PROTEIN; INTERLEUKIN 6; NORADRENALIN; RECOMBINANT ERYTHROPOIETIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTIFICIAL VENTILATION; BALLOON OCCLUSION; CELL INFILTRATION; CONTINUOUS INFUSION; EVOKED MUSCLE RESPONSE; FEMALE; GAS EXCHANGE; HEMODYNAMIC PARAMETERS; MALE; MEAN ARTERIAL PRESSURE; MONONUCLEAR CELL; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PROTEIN BLOOD LEVEL; REPERFUSION INJURY; SPINAL CORD ISCHEMIA; SWINE; TISSUE INJURY;

ANIMALS; AORTA; BALLOON DILATION; ERYTHROPOIETIN; EVOKED POTENTIALS, MOTOR; REPERFUSION INJURY; SPINAL CORD ISCHEMIA; SWINE;

EID: 80054764389     PISSN: 03424642     EISSN: 14321238     Source Type: Journal    
DOI: 10.1007/s00134-011-2303-4     Document Type: Article

References (42)

1. Gelman S (1995) The pathophysiology of aortic cross-clamping and unclamping. Anesthesiology 82:1026-1060
2. Celik M, Gökmen N, Erbayraktar S, Akhisaroglu M, Konakc S, Ulukus C, Genc S, Genc K, Sagiroglu E, Cerami A, Brines M (2002) Erythropoietin prevents motor neuron apoptosis and neurologic disability in experimental spinal cord ischemic injury. Proc Natl Acad Sci USA 99:2258-2263 (Pubitemid 34169048)
3. Sönmez A, Kabakçi B, Vardar E, Gürel D, Sönmez U, Orhan YT, Açikel U, Gökmen N (2007) Erythropoietin attenuates neuronal injury and potentiates the expression of pCREB in anterior horn after transient spinal cord ischemia in rats. Surg Neurol 68:297-303 (Pubitemid 47284375)
4. Simon F, Scheuerle A, Calzia E, Bassi G, Oter S, Duy CN, Kick J, Brückner UB, Radermacher P, Schelzig H (2008) Erythropoietin during porcine aortic balloon occlusion-induced ischemia/reperfusion injury. Crit Care Med 36:2143-2150
5. Ehrenreich H, Weissenborn K, Prange H, Schneider D, Weimar C, Wartenberg K, Schellinger PD, Bohn M, Becker H, Wegrzyn M, Jähnig P, Herrmann M, Knauth M, Bähr M, Heide W, Wagner A, Schwab S, Reichmann H, Schwendemann G, Dengler R, Kastrup A, Bartels C, Stroke Trial Group EPO (2010) Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke 40:647-656
6. Nagai T, Akizawa T, Kohjiro S, Koiwa F, Nabeshima K, Niikura K, Kino K, Kanamori N, Kinugasa E, Ideura T (1996) rHuEPO enhances the production of plasminogen activator inhibitor-1 in cultured endothelial cells. Kidney Int 50:102-107 (Pubitemid 26323703)
7. Brines M, Grasso G, Fiordaliso F, Sfacteria A, Ghezzi P, Fratelli M, Latini R, Xie QW, Smart J, Su-Rick CJ, Pobre E, Diaz D, Gomez D, Hand C, Coleman T, Cerami A (2004) Erythropoietin mediates tissue protection through an erythropoietin and common betasubunit heteroceptor. Proc Natl Acad Sci USA 1:14907-14912 (Pubitemid 39410773)
8. Coleman TR, Westenfelder C, Tögel FE, Yang Y, Hu Z, Swenson L, Leuvenink HG, Ploeg RJ, d Uscio LV, Katusic ZS, Ghezzi P, Zanetti A, Kaushansky K, Fox NE, Cerami A, Brines M (2006) Cytoprotective doses of erythropoietin or carbamylated erythropoietin have markedly different procoagulant and vasoactive activities. Proc Natl Acad Sci USA 103:5965-5970
9. Brines M, Cerami A (2008) Erythropoietin-mediated tissue protection: reducing collateral damage from the primary injury response. J Int Med 264:405-432
10. Leist M, Ghezzi P, Grasso G, Bianchi R, Villa P, Fratelli M, Savino C, Bianchi M, Nielsen J, Gerwien J, Kallunki P, Larsen AK, Helboe L, Christensen S, Pedersen LO, Nielsen M, Torup L, Sager T, Sfacteria A, Erbayraktar S, Erbayraktar Z, Gokmen N, Yilmaz O, Cerami-Hand C, Xie QW, Coleman T, Cerami A, Brines M (2004) Derivatives of erythropoietin that are tissue protective but not erythropoietic. Science 305:239-242 (Pubitemid 38886736)
11. Adembri C, Massagrande A, Tani A, Miranda M, Margheri M, De Gaudio R, Pellegrini-Giampietro DE (2008) Carbamylated erythropoietin is neuroprotective in an experimental model of traumatic brain injury. Crit Care Med 36:975-978
12. Lapchak PA, Kirkeby A, Zivin JA, Sager TN (2008) Therapeutic window for nonerythropoietic carbamylatederythropoietin to improve motor function following multiple infarct ischemic strokes in New Zealand white rabbits. Brain Res 1238:208-214
13. Nijboer WN, Ottens PJ, van Dijk A, van Goor H, Ploeg RJ, Leuvenink HGD (2010) Donor pretreatment with carbamylated erythropoietin in a brain death model reduces inflammation more effectively than erythropoietin while preserving renal function. Crit Care Med 38:1155-1161
14. Schriebl K, Trummer E, Lattenmayer C, Weik R, Kunert R, Mü ller D, Katinger H, Vorauer-Uhl K (2006) Biochemical characterization of rhEPOFc fusion protein expressed in CHO cells. Protein Expr Purif 49:265-275 (Pubitemid 44416228)
15. Simon F, Giudici R, Duy CN, Schelzig H, Oter S, Gröger M, Wachter U, Vogt J, Speit G, Szabó C, Radermacher P, Calzia E (2008) Hemodynamic and metabolic effects of hydrogen sulfide during porcine ischemia/reperfusion injury. Shock 30:359-364
16. Kuriyama T, Latham LP, Horwitz LD, Reeves JT, Wagner WW Jr (1984) Role of collateral ventilation in ventilationperfusion balance. J Appl Physiol 56:1500-1506 (Pubitemid 14122620)
17. Nirmalan M, Willard TM, Edwards DJ, Little RA, Dark PM (2005) Estimation of errors in determining intrathoracic blood volume using the single transpulmonary thermal dilution technique in hypovolemic shock. Anesthesiology 103:805-812 (Pubitemid 41415529)
18. Papakostas JC, Matsagas MI, Toumpoulis IK, Malamou-Mitsi VD, Pappa LS, Gkrepi C, Anagnostopoulos CE, Kappas AM (2006) Evolution of spinal cord injury in a porcine model of prolonged aortic occlusion. J Surg Res 133:159-166 (Pubitemid 43765753)
19. Blaisdell FW, Cooley DA (1962) The mechanism of paraplegia after temporary thoracic aortic occlusion and its relationship to spinal fluid pressure. Surgery 51:351-355
20. Wadouh F, Lindemann EM, Arndt CF, Hetzer R, Borst HG (1984) The arteria radicularis magna anterior as a decisive factor influencing spinal cord damage during aortic occlusion. J Thorac Cardiovasc Surg 88:1-10 (Pubitemid 14088869)
21. Weigang E, Luehr M, von Samson P, Hartert M, Goebel H, Wetzig M, Bernard V, Siegenthaler MP, Beyersdorf F (2005) Development of a special balloon occlusion device top prevent adverse events in high-risk patients during open aortic surgery. Eur Surg Res 37:204-209 (Pubitemid 41547086)
22. Meylaerts SA, De Haan P, Kalkman CJ, Lips J, De Mol BA, Jacobs MJ (1999) The influence of regional spinal cord hypothermia on transcranial myogenic motor-evoked potential monitoring and the efficacy of spinal cord ischemia detection. J Thorac Cardiovasc Surg 118:1038-1045
23. Meylaerts SA, De Haan P, Kalkman CJ, Jaspers J, Vanicky I, Jacobs MJ (2000) Prevention of paraplegia in pigs by selective segmental artery perfusion during aortic crossclamping. J Vasc Surg 32:160-170 (Pubitemid 30461166)
24. Lips J, de Haan P, Bouma GJ, Holman R, van Dongen E, Kalkman CJ (2005) Continuous monitoring of cerebrospinal fluid oxygen tension in relation to motor evoked potentials during spinal cord ischemia in pigs. Anesthesiology 102:340-345 (Pubitemid 40189082)
25. Hauser B, Kick J, Iványi Z, Asfar P, Ehrmann U, Muth CM, Albicini M, Wachter U, Vogt J, Bauer M, Brückner UB, Radermacher P, Bracht H (2006) Effects of 15-deoxy-D12, 14-prostaglandin-J2 during hyperdynamic porcine endotoxemia. Intensive Care Med 3:759-765
26. Kick J, Hauser B, Bracht H, Albicini M, Oter S, Simon F, Ehrmann U, Garrel C, Sträter J, Brückner UB, Leverve XM, Schelzig H, Speit G, Radermacher P, Muth CM (2007) Effects of a cantaloupe melon extract/wheat gliadin biopolymer during aortic crossclamping. Intensive Care Med 33:694-702 (Pubitemid 46474889)
27. Maier C, Scheuerle A, Hauser B, Schelzig H, Szabó C, Radermacher P, Kick J (2007) The selective PARP-1 inhibitor INO1001 reduces spinal cord injury during porcine aortic crossclamping-induced ischemia/reperfusion injury. Intensive Care Med 33:845-850 (Pubitemid 46675322)
28. Villa P, van Beek J, Larsen AK, Gerwien J, Christensen S, Cerami A, Brines M, Leist M, Ghezzi P, Torup L (2007) Reduced functional deficits, neuroinflammation, and secondary tissue damage after treatment of stroke by nonerythropoietic erythropoietin derivatives. J Cerebr Blood Flow Metab 27:552-563
29. Kaptanoglu E, Solaroglu I, Okutan O, Surucu HS, Akbiyik F, Beskonakli E (2004) Erythropoietin exerts neuroprotection after acute spinal cord injury in rats: effect on lipid peroxidation and early ultrastructural findings. Neurosurg Rev 27:113-120 (Pubitemid 38374415)
30. King VR, Averill SA, Hewazy D, Priestley JV, Torup L, Michael-Titus AT (2007) Erythropoietin and carbamylated erythropoietin are neuroprotective following spinal cord hemisection in the rat. Eur J Neurosci 26:90-100 (Pubitemid 47035440)
31. Simon F, Scheuerle A, Gröger M, Stahl B, Wachter U, Vogt J, Speit G, Hauser B, Möller P, Calzia E, Szabó C, Schelzig H, Georgieff M, Radermacher P, Wagner F (2011) Effects of intravenous sulfide during porcine aortic occlusion-induced kidney ischemia/reperfusion injury. Shock 35:156-163
32. Kuluz J, Samdani A, Benglis D, Gonzalez-Brito M, Solano JP, Ramirez MA, Luqman A, De los Santos R, Hutchinson D, Nares M, Padgett K, He D, Huang T, Levi A, Betz R, Dietrich D (2010) Pediatric spinal cord injury in infant piglets: description of a new large animal model and review of the literature. J Spinal Cord Med 33:43-57
33. Lang-Lazdunski L, Heurteaux C, Mignon A, Mantz J, Widmann C, Desmonts J, Lazdunski M (2000) Ischemic spinal cord injury induced by aortic cross-clamping: prevention by riluzole. Eur J Cardiothorac Surg 18:174-181 (Pubitemid 30488814)
34. Wang Q, Ding Q, Zhou Y, Gou X, Hou L, Chen S, Zhu Z, Xiong L (2009) Ethyl pyruvate attenuates spinal cord ischemic injury with a wide therapeutic window through inhibiting highmobility group box 1 release in rabbits. Anesthesiology 110:1279-1286
35. Hu BR, Liu CL, Ouyang Y, Blomgren K, Siesjö BK (2000) Involvement of caspase-3 in cell death after hypoxiaischemia declines during brain maturation. J Cereb Blood Flow Metab 20:1550-1556
36. Kuluz JW, Prado R, He D, Zhao W, Dietrich WD, Watson B (2007) New pediatric model of ischemic stroke in infant piglets by photothrombosis: acute changes in cerebral blood flow, microvasculature, and early histopathology. Stroke 38:1932-1937 (Pubitemid 46847271)
37. Maiese K, Li F, Chong ZZ (2005) New avenues of exploration for erythropoietin. JAMA 293:90-95 (Pubitemid 40066704)
38. Moon C, Krawczyk M, Paik D, Coleman T, Brines M, Juhaszova M, Sollott SJ, Lakatta EG, Talan MI (2006) Erythropoietin, modified to not stimulate red blood cell production, retains its cardioprotective properties. J Pharmacol Exp Ther 316:999-1005 (Pubitemid 43345271)
39. Basu S, Eriksson M (1998) Oxidative injury and survival during endotoxemia. FEBS Lett 438:159-160 (Pubitemid 28529265)
40. Siems W, Quast S, Carluccio F, Wiswedel I, Hirsch D, Augustin W, Kraemer K, Hampl H, Sommerburg O (2003) Oxidative stress in cardio renal anemia syndrome: correlations and therapeutic possibilities. Clin Nephrol 60 Suppl 1:S22-S30 (Pubitemid 36889537)
41. Nalos M, Asfar P, Ichai C, Radermacher P, Leverve XM, Fröba G (2003) Adenosinetriphosphatemagnesium chloride: relevance for intensive care. Intensive Care Med 29:10-18 (Pubitemid 36216376)
42. Maharajh GS, Pascoe EA, Halliday WC, Grocott HP, Thiessen DB, Girling LG, Cheang MS, Mutch WA (1996) Neurological outcome in a porcine model of descending thoracic aortic surgery. Left atrial-femoral artery bypass versus clamp/repair. Stroke 27:2095-2101 (Pubitemid 26372587)