Synergistic effect of erythropoietin but not G-CSF in combination with curcumin on impaired liver regeneration in rats

Langenbeck's Archives of Surgery

Volumn 393, Issue 3, 2008, Pages 325-332

  Seehofer, Daniel ^a   Neumann, Ulf P ^a   Schirmeier, Anja ^a   Carter, Jessica ^a   Cho, Si Young Ria ^a   Lederer, Andri ^a   Rayes, Nada ^a   Menger, Michael D ^b   Nüssler, Andreas K ^c   Neuhaus, Peter ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

CLP; Curcumin; Erythropoietin; G CSF; Liver regeneration; Partial hepatectomy

Indexed keywords

BILIRUBIN; CURCUMIN; CYTOKINE; ERYTHROPOIETIN; GLUTATHIONE; GRANULOCYTE COLONY STIMULATING FACTOR; KI 67 ANTIGEN; LIVER ENZYME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE FLOW; BLOOD SAMPLING; CECUM; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); DRUG EFFECT; DRUG POTENTIATION; HISTOLOGY; LIGATION; LIVER CELL DAMAGE; LIVER FUNCTION; LIVER PROTECTION; LIVER REGENERATION; LIVER RESECTION; LIVER WEIGHT; MALE; MITOSIS INDEX; MONOTHERAPY; MORPHOLOGY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUNCTURE; RAT; SPRAGUE DAWLEY RAT; STIMULATION;

EID: 43349090912     PISSN: 14352443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00423-008-0290-x     Document Type: Article

References (43)

1. 1. M Joyeux-Faure 2007 Cellular protection by erythropoietin: new therapeutic implications? J Pharmacol Exp Ther 323 759 762 17717190 10.1124/jpet.107.127357 1:CAS:528:DC%2BD2sXhsVSgsL3L Joyeux-Faure M (2007) Cellular protection by erythropoietin: new therapeutic implications? J Pharmacol Exp Ther 323:759–762
2. 2. M Brines A Cerami 2006 Discovering erythropoietin’s extra-hematopoietic functions: biology and clinical promise Kidney Int 70 246 250 16738535 10.1038/sj.ki.5001546 1:CAS:528:DC%2BD28XmvFagsL0%3D Brines M, Cerami A (2006) Discovering erythropoietin’s extra-hematopoietic functions: biology and clinical promise. Kidney Int 70:246–250
3. 3. CZ Lu BG Xiao 2006 G-CSF and neuroprotection: a therapeutic perspective in cerebral ischaemia Biochem Soc Trans 34 1327 1333 17073813 10.1042/BST0341327 1:CAS:528:DC%2BD28XhtFKgtbrN Lu CZ, Xiao BG (2006) G-CSF and neuroprotection: a therapeutic perspective in cerebral ischaemia. Biochem Soc Trans 34:1327–1333
4. 4. C Lacombe P Mayeux 1999 The molecular biology of erythropoietin Nephrol Dial Transplant 14 Suppl 2 22 28 10334664 10.1093/ndt/14.suppl_2.22 1:CAS:528:DyaK1MXivVSluro%3D Lacombe C, Mayeux P (1999) The molecular biology of erythropoietin. Nephrol Dial Transplant 14(Suppl 2):22–28
5. 5. F Farrell A Lee 2004 The erythropoetin receptor and its expression in tumor cells and other tissues Oncologist 9 Suppl 5 18 30 15591419 10.1634/theoncologist.9-90005-18 1:CAS:528:DC%2BD2MXltVWksw%3D%3D Farrell F, Lee A (2004) The erythropoetin receptor and its expression in tumor cells and other tissues. Oncologist 9(Suppl 5):18–30
6. 6. M Sakanaka TC Wen S Matsuda S Masuda E Morishita M Nagao R Sasaki 1998 In vivo evidence that erythropoetin protects neurons from ischemic damage Proc Natl Acad Sci USA 95 4635 4640 9539790 10.1073/pnas.95.8.4635 1:CAS:528:DyaK1cXis1Ogsbo%3D Sakanaka M, Wen TC, Matsuda S, Masuda S, Morishita E, Nagao M, Sasaki R (1998) In vivo evidence that erythropoetin protects neurons from ischemic damage. Proc Natl Acad Sci USA 95:4635–4640
7. 7. D Black S Lyman TR Heider KE Behrns 2004 Molecular and cellular features of hepatic regeneration J Surg Res 117 306 315 15047136 10.1016/j.jss.2003.10.026 1:CAS:528:DC%2BD2cXisVSmtbk%3D Black D, Lyman S, Heider TR, Behrns KE (2004) Molecular and cellular features of hepatic regeneration. J Surg Res 117:306–315
8. 8. S Cuzzocrea E Mazzon R Paola di T Genovese NS Patel D Britti M Majo de AP Caputi C Thiemermann 2005 Erythropoietin reduces the degree of arthritis caused by type II collagen in the mouse Arthritis Rheum 52 940 950 15751086 10.1002/art.20875 1:CAS:528:DC%2BD2MXjtVGjtbk%3D Cuzzocrea S, Mazzon E, di Paola R, Genovese T, Patel NS, Britti D, de Majo M, Caputi AP, Thiemermann C (2005) Erythropoietin reduces the degree of arthritis caused by type II collagen in the mouse. Arthritis Rheum 52:940–950
9. 9. X Liu W Xie P Liu M Duan Z Jia W Li J Xu 2006 Mechanism of the cardioprotection of rhEPO pretreatment on suppressing the inflammatory response in ischemia–reperfusion Life Sci 78 2255 2264 16336978 10.1016/j.lfs.2005.09.053 1:CAS:528:DC%2BD28XivVOgsb0%3D Liu X, Xie W, Liu P, Duan M, Jia Z, Li W, Xu J (2006) Mechanism of the cardioprotection of rhEPO pretreatment on suppressing the inflammatory response in ischemia–reperfusion. Life Sci 78:2255–2264
10. 10. E Ates AU Yalcin S Yilmaz T Koken C Tokyol 2004 Protective effect of erythropoietin on renal ischemia and reperfusion injury ANZ J Surg 75 1100 1105 10.1111/j.1445-2197.2005.03612.x Ates E, Yalcin AU, Yilmaz S, Koken T, Tokyol C (2004) Protective effect of erythropoietin on renal ischemia and reperfusion injury. ANZ J Surg 75:1100–1105
11. 11. S Yilmaz E Ates C Tokyol T Pehlivan S Erkasap T Koken 2004 The protective effect of erythropoietin on ischemia–reperfusion injury of liver HPB 3 169 173 Yilmaz S, Ates E, Tokyol C, Pehlivan T, Erkasap S, Koken T (2004) The protective effect of erythropoietin on ischemia–reperfusion injury of liver. HPB 3:169–173
12. 12. G Calapai MC Marciano F Corica A Allegra A Parisi N Frisina AP Caputi M Buemi 2000 Erythropoietin protects against brain ischemic injury by inhibition of nitric oxide formation Eur J Pharmacol 401 349 356 10936493 10.1016/S0014-2999(00)00466-0 1:CAS:528:DC%2BD3cXlsFCgtL0%3D Calapai G, Marciano MC, Corica F, Allegra A, Parisi A, Frisina N, Caputi AP, Buemi M (2000) Erythropoietin protects against brain ischemic injury by inhibition of nitric oxide formation. Eur J Pharmacol 401:349–356
13. 13. JE Baker D Kozik AK Hsu X Fu JS Tweddell GJ Gross 2007 Darbepoetin alfa protects the rat heart against infarction: dose–response, phase of action, and mechanisms J Cardiovasc Pharmacol 49 337 345 17577097 10.1097/FJC.0b013e318040cf81 1:CAS:528:DC%2BD2sXmsFOisrs%3D Baker JE, Kozik D, Hsu AK, Fu X, Tweddell JS, Gross GJ (2007) Darbepoetin alfa protects the rat heart against infarction: dose–response, phase of action, and mechanisms. J Cardiovasc Pharmacol 49:337–345
14. 14. E Ates S Yilmaz E Ihtiyar B Yasar E Karahuseyinoglu 2006 Preconditioning-like amelioration of erythropoietin against laparoscopy-induced oxidative injury Surg Endosc 20 815 819 16502197 10.1007/s00464-005-0428-7 1:STN:280:DC%2BD283lsFCktA%3D%3D Ates E, Yilmaz S, Ihtiyar E, Yasar B, Karahuseyinoglu E (2006) Preconditioning-like amelioration of erythropoietin against laparoscopy-induced oxidative injury. Surg Endosc 20:815–819
15. 15. K Minh Le K Klemm K Abshagen C Eipel MD Menger B Vollmar 2007 Attenuation of inflammation and apoptosis by pre-and posttreatment of darbepoetin-alpha in acute liver failure of mice Am J Pathol 170 1954 1963 17525263 10.2353/ajpath.2007.061056 1:CAS:528:DC%2BD2sXntlOhtL8%3D Le Minh K, Klemm K, Abshagen K, Eipel C, Menger MD, Vollmar B (2007) Attenuation of inflammation and apoptosis by pre-and posttreatment of darbepoetin-alpha in acute liver failure of mice. Am J Pathol 170:1954–1963
16. 16. GA Matchett JB Calinisan GC Matchett RD Martin JH Zhang 2007 The effect of granulocyte-colony stimulating factor in global cerebral ischemia in rats Brain Res 1136 200 207 17210148 10.1016/j.brainres.2006.12.023 1:CAS:528:DC%2BD2sXhs1Cntrw%3D Matchett GA, Calinisan JB, Matchett GC, Martin RD, Zhang JH (2007) The effect of granulocyte-colony stimulating factor in global cerebral ischemia in rats. Brain Res 1136:200–207
17. 17. A Bauhofer B Stinner F Kohlert B Reckzeh W Lorenz I Celik 2002 Granulocyte colony-stimulating factor but not peritoneal lavage increases survival rate after experimental abdominal contamination and infection Br J Surg 89 1457 1464 12390392 10.1046/j.1365-2168.2002.02227.x 1:STN:280:DC%2BD38njt1amsg%3D%3D Bauhofer A, Stinner B, Kohlert F, Reckzeh B, Lorenz W, Celik I (2002) Granulocyte colony-stimulating factor but not peritoneal lavage increases survival rate after experimental abdominal contamination and infection. Br J Surg 89:1457–1464
18. 18. A Bauhofer I Celik U Plaul H Wulf A Torossian 2004 Effects of G-CSF and antibiotic prophylaxis in a 2 × 2 factorial design on outcome in septic rats Inflamm Res 53 Suppl 2 S 126 129 1:CAS:528:DC%2BD2cXns1yiurc%3D Bauhofer A, Celik I, Plaul U, Wulf H, Torossian A (2004) Effects of G-CSF and antibiotic prophylaxis in a 2 × 2 factorial design on outcome in septic rats. Inflamm Res 53(Suppl 2):S 126–129
19. 19. I Görgen T Hartung M Leist M Niehörster G Tiegs S Uhlig F Weitzel A Wendel 1992 Granulocyte colony-stimulating factor treatment protects rodents against lipopolysaccharide-induced toxicity via suppression of systemic tumor necrosis factor-alpha J Immunol 149 918 924 1378868 Görgen I, Hartung T, Leist M, Niehörster M, Tiegs G, Uhlig S, Weitzel F, Wendel A (1992) Granulocyte colony-stimulating factor treatment protects rodents against lipopolysaccharide-induced toxicity via suppression of systemic tumor necrosis factor-alpha. J Immunol 149:918–924
20. 20. CJ Busch GA Wanner MD Menger B Vollmar 2004 Granulocyte colony-stimulating factor (G-CSF) reduces not only gram-negative but also gram-positive infection-associated proinflammatory cytokine release by interaction between Kupffer cells and leukocytes Inflamm Res 53 205 210 15105970 10.1007/s00011-004-1250-8 1:CAS:528:DC%2BD2cXjvVyht7s%3D Busch CJ, Wanner GA, Menger MD, Vollmar B (2004) Granulocyte colony-stimulating factor (G-CSF) reduces not only gram-negative but also gram-positive infection-associated proinflammatory cytokine release by interaction between Kupffer cells and leukocytes. Inflamm Res 53:205–210
21. 21. B Vollmar S Messner GA Wanner T Hartung MD Menger 1997 Immunomodulatory action of G-CSF in a rat model of endotoxin-induced liver injury: an intravital microscopic analysis of Kupffer cell and leukocyte response J Leukoc Biol 62 710 718 9400811 1:CAS:528:DyaK2sXnvFSqsbs%3D Vollmar B, Messner S, Wanner GA, Hartung T, Menger MD (1997) Immunomodulatory action of G-CSF in a rat model of endotoxin-induced liver injury: an intravital microscopic analysis of Kupffer cell and leukocyte response. J Leukoc Biol 62:710–718
22. 22. SE Theocharis E Agapitos AP Margeli N Goutas C Kittas P Davaris 1997 Effect of two forms of granulocyte-colony stimulating factor on hepatic regeneration after 70% partial hepatectomy in rats Clin Sci 92 315 320 9093013 1:CAS:528:DyaK2sXisVaktb8%3D Theocharis SE, Agapitos E, Margeli AP, Goutas N, Kittas C, Davaris P (1997) Effect of two forms of granulocyte-colony stimulating factor on hepatic regeneration after 70% partial hepatectomy in rats. Clin Sci 92:315–320
23. 23. D Inderbitzin G Beldi D Sidler P Studer A Keogh S Bisch-Knaden R Weimann A Kappeler B Gloor D Candinas 2007 Granulocyte colony-stimulating factor supports liver regeneration in a small-for-size liver remnant mouse model J Gastrointest Surg 11 280 285 17458598 10.1007/s11605-007-0096-0 Inderbitzin D, Beldi G, Sidler D, Studer P, Keogh A, Bisch-Knaden S, Weimann R, Kappeler A, Gloor B, Candinas D (2007) Granulocyte colony-stimulating factor supports liver regeneration in a small-for-size liver remnant mouse model. J Gastrointest Surg 11:280–285
24. 24. SE Theocharis LJ Papadimitriou ZP Retsou AP Margeli SS Ninos JD Papadimitriou 2003 Granulocyte-colony stimulating factor administration ameliorates liver regeneration in animal model of fulminant hepatic failure and encephalopathy Dig Dis Sci 48 1797 1803 14561004 10.1023/A:1025463532521 1:CAS:528:DC%2BD3sXmslCks74%3D Theocharis SE, Papadimitriou LJ, Retsou ZP, Margeli AP, Ninos SS, Papadimitriou JD (2003) Granulocyte-colony stimulating factor administration ameliorates liver regeneration in animal model of fulminant hepatic failure and encephalopathy. Dig Dis Sci 48:1797–1803
25. 25. T Ogiso M Nagaki S Takai Y Tsukada T Mukai K Kimura H Moriwaki 2007 Granulocyte colony-stimulating factor impairs liver regeneration in mice through the up-regulation of interleukin-1beta J Hepatol 47 816 25 17869372 10.1016/j.jhep.2007.06.017 1:CAS:528:DC%2BD2sXht12ns7fN Ogiso T, Nagaki M, Takai S, Tsukada Y, Mukai T, Kimura K, Moriwaki H (2007) Granulocyte colony-stimulating factor impairs liver regeneration in mice through the up-regulation of interleukin-1beta. J Hepatol 47:816–25
26. 26. D Seehofer M Stockmann A Schirmeier AK Nüssler SR Cho N Rayes M Koch R Schiller MD Menger P Neuhaus 2007 Intraabdominal bacterial infections significantly alter regeneration and function of the liver in a rat model of major hepatectomy Langenbeck’s Arch Surg 392 273 284 10.1007/s00423-007-0169-2 Seehofer D, Stockmann M, Schirmeier A, Nüssler AK, Cho SR, Rayes N, Koch M, Schiller R, Menger MD, Neuhaus P (2007) Intraabdominal bacterial infections significantly alter regeneration and function of the liver in a rat model of major hepatectomy. Langenbeck’s Arch Surg 392:273–284
27. 27. S Bengmark 2006 Curcumin, an atoxic antioxidant and natural NFkappaB, cyclooxygenase-2, lipooxygenase, and inducible nitric oxide synthase inhibitor: a shield against acute and chronic diseases JPEN J Parenter Enteral Nutr 30 45 51 16387899 1:CAS:528:DC%2BD28XhtVKltLg%3D 10.1177/014860710603000145 Bengmark S (2006) Curcumin, an atoxic antioxidant and natural NFkappaB, cyclooxygenase-2, lipooxygenase, and inducible nitric oxide synthase inhibitor: a shield against acute and chronic diseases. JPEN J Parenter Enteral Nutr 30:45–51
28. 28. JW Cho KS Lee CW Kim 2007 Curcumin attenuates the expression of IL-1beta, IL-6, and TNF-alpha as well as cyclin E in TNF-alpha-treated HaCaT cells; NF-kappaB and MAPKs as potential upstream targets Int J Mol Med 19 469 17273796 1:CAS:528:DC%2BD2sXivVOnsb0%3D Cho JW, Lee KS, Kim CW (2007) Curcumin attenuates the expression of IL-1beta, IL-6, and TNF-alpha as well as cyclin E in TNF-alpha-treated HaCaT cells; NF-kappaB and MAPKs as potential upstream targets. Int J Mol Med 19:469
29. 29. MA Baker GJ Cerniglia A Zaman 1990 Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples Anal Biochem 190 360 2291479 10.1016/0003-2697(90)90208-Q 1:CAS:528:DyaK3cXmt1Ons70%3D Baker MA, Cerniglia GJ, Zaman A (1990) Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples. Anal Biochem 190:360
30. 30. BA Naughton DJ Birnbach P Liu GA Kolks MZ Tung JA Piliero SJ Piliero AS Gordon 1979 Reticuloendothelial system (RES) hyperfunction and erythropoietin (Ep) production in the regenerating liver J Surg Oncol 12 227 242 502565 10.1002/jso.2930120307 1:CAS:528:DyaL3cXlsFKqsg%3D%3D Naughton BA, Birnbach DJ, Liu P, Kolks GA, Tung MZ, Piliero JA, Piliero SJ, Gordon AS (1979) Reticuloendothelial system (RES) hyperfunction and erythropoietin (Ep) production in the regenerating liver. J Surg Oncol 12:227–242
31. 31. BA Naughton C Gamba-Vitalo GK Naughton P Liu AS Gordon 1982 Granulopoiesis and colony stimulating factor production in regenerating liver Exp Hematol 10 451 8 6980134 1:STN:280:DyaL383js1Sgtw%3D%3D Naughton BA, Gamba-Vitalo C, Naughton GK, Liu P, Gordon AS (1982) Granulopoiesis and colony stimulating factor production in regenerating liver. Exp Hematol 10:451–8
32. 32. P Paul SA Rothmann JT McMahon AS Gordon 1984 Erythropoietin secretion by isolated rat Kupffer cells Exp Hematol 12 825 830 6510483 1:CAS:528:DyaL2MXntlenuw%3D%3D Paul P, Rothmann SA, McMahon JT, Gordon AS (1984) Erythropoietin secretion by isolated rat Kupffer cells. Exp Hematol 12:825–830
33. 33. M Schmeding UP Neumann S Boas-Knoop A Spinelli P Neuhaus 2007 Erythropoietin reduces ischemia–reperfusion injury in the rat liver Eur Surg Res 39 189 97 17377393 10.1159/000101009 1:CAS:528:DC%2BD2sXksVyhurw%3D Schmeding M, Neumann UP, Boas-Knoop S, Spinelli A, Neuhaus P (2007) Erythropoietin reduces ischemia–reperfusion injury in the rat liver. Eur Surg Res 39:189–97
34. 34. Schmeding M, Boas-Knoop S, Lippert S, Ruehl M, Somasundaram R, Dagdelen T, Neuhaus P, Neumann UP (2007) Erythropoietin promotes hepatic regeneration after extended liver resection in rats. J Gastroenterol Hepatol DOI 10.1111/j.1440-1746.2007.05265.x
35. 35. BJ Sasu C Hartley H Schultz P McElroy R Khaja S Elliott JC Egrie JK Browne CG Begley G Molineux 2005 Comparison of epoetin alfa and darbepoetin alfa biological activity under different administration schedules in normal mice Acta Haematol 113 163 174 15870486 10.1159/000084446 1:CAS:528:DC%2BD2MXjvVWjt7o%3D Sasu BJ, Hartley C, Schultz H, McElroy P, Khaja R, Elliott S, Egrie JC, Browne JK, Begley CG, Molineux G (2005) Comparison of epoetin alfa and darbepoetin alfa biological activity under different administration schedules in normal mice. Acta Haematol 113:163–174
36. 36. N Yazihan H Ataoğlu B Yener C Aydin 2007 Erythropoietin attenuates hydrogen peroxide-induced damage of hepatocytes Turk J Gastroenterol 18 239 44 18080920 Yazihan N, Ataoğlu H, Yener B, Aydin C (2007) Erythropoietin attenuates hydrogen peroxide-induced damage of hepatocytes. Turk J Gastroenterol 18:239–44
37. 37. WS Alexander 2002 Suppressors of cytokine signaling (SOCS) in the immune system Nat Rev Immunol 2 410 416 12093007 1:CAS:528:DC%2BD38Xksl2murg%3D Alexander WS (2002) Suppressors of cytokine signaling (SOCS) in the immune system. Nat Rev Immunol 2:410–416
38. 38. SM Khopde KI Priyadarsini P Venkatesan MN Rao 1999 Free radical scavenging ability and antioxidant efficiency of curcumin and its substituted analogue Biophys Chemist 80 85 10.1016/S0301-4622(99)00070-8 1:CAS:528:DyaK1MXltlCqtrc%3D Khopde SM, Priyadarsini KI, Venkatesan P, Rao MN (1999) Free radical scavenging ability and antioxidant efficiency of curcumin and its substituted analogue. Biophys Chemist 80:85
39. 39. AC Reddy BR Lokesh 1994 Studies on the inhibitory effects of curcumin and eugenol on the formation of reactive oxygen species and the oxidation of ferrous iron Mol Cell Biochem 137 1 8 7845373 10.1007/BF00926033 1:CAS:528:DyaK2cXmvFaktrY%3D Reddy AC, Lokesh BR (1994) Studies on the inhibitory effects of curcumin and eugenol on the formation of reactive oxygen species and the oxidation of ferrous iron. Mol Cell Biochem 137:1–8
40. 40. DA Dickinson KE Iles H Zhang V Blank HJ Forman 2003 Curcumin alters EpRE and AP-1 binding complexes and elevates glutamate-cystein ligase gene expression FASEB J 17 473 12514113 1:CAS:528:DC%2BD3sXitFaqt7s%3D Dickinson DA, Iles KE, Zhang H, Blank V, Forman HJ (2003) Curcumin alters EpRE and AP-1 binding complexes and elevates glutamate-cystein ligase gene expression. FASEB J 17:473
41. 41. H Choi YS Chun SW Kim MS Kim JW Park 2006 Curcumin inhibits hypoxia-inducible factor-1 by degrading aryl hydrocarbon receptor nuclear translocator: a mechanism of tumor growth inhibition Mol Pharmacol 70 1664 1671 16880289 10.1124/mol.106.025817 1:CAS:528:DC%2BD28XhtFygsbbI Choi H, Chun YS, Kim SW, Kim MS, Park JW (2006) Curcumin inhibits hypoxia-inducible factor-1 by degrading aryl hydrocarbon receptor nuclear translocator: a mechanism of tumor growth inhibition. Mol Pharmacol 70:1664–1671
42. 42. HL Corwin A Gettinger TC Fabian A May RG Pearl S Heard R An PJ Bowers P Burton MA Klausner MJ Corwin 2007 Efficacy and safety of epoetin alfa in critically ill patients N Engl J Med 357 965 976 17804841 10.1056/NEJMoa071533 1:CAS:528:DC%2BD2sXhtVensrbE Corwin HL, Gettinger A, Fabian TC, May A, Pearl RG, Heard S, An R, Bowers PJ, Burton P, Klausner MA, Corwin MJ (2007) Efficacy and safety of epoetin alfa in critically ill patients. N Engl J Med 357:965–976
43. 43. G Beutel A Ganser 2007 Risks and benefits of erythropoiesis-stimulating agents in cancer management Semin Hematol 44 157 65 17631180 10.1053/j.seminhematol.2007.04.004 1:CAS:528:DC%2BD2sXoslGlt74%3D Beutel G, Ganser A (2007) Risks and benefits of erythropoiesis-stimulating agents in cancer management. Semin Hematol 44:157–65