Advertisement

Anemia management in cancer patients with chronic kidney disease

Published:September 15, 2016DOI:https://doi.org/10.1016/j.ejim.2016.08.036

      Highlights

      • ESA usage in anemia care is decreasing due to recent unfavorable clinical results.
      • Iron therapy has gained more significance, although long-term safety is unknown.
      • Insufficient evidence is available in anemia therapy of CKD patients with cancer.
      • Individualized therapy is recommended based on current guidelines.

      Abstract

      Anemia is a common complication of cancer and chronic kidney disease (CKD) associated with decreased physical performance as well as poor prognosis for life expectancy. Renal and cancer-induced anemia share common features regarding pathogenesis and therapeutic strategies. It is typically treated with iron substitution, erythropoiesis-stimulating agents (ESA) and in refractory cases with red blood cell transfusions. However, studies of the past few years unveiled numerous setbacks in the use of ESAs. These included a higher risk of cerebrovascular events and increased mortality without the improvement of cardiovascular outcomes in patients with CKD. Moreover, particularly negative results were observed in patients with previous cancer history under ESA therapy. These unfavorable findings have forced the clinicians to reevaluate the management of renal anemia. This led to decrease of ESA usage, while iron substitution and alternative therapeutic options gained more significance. Iron supplementation is also accompanied with certain risks ranging from gastrointestinal complications to severe allergic reactions and increased rate of infections. Furthermore, the evaluation of the long-term safety of excessive iron therapy is still lacking, especially in CKD patients with cancer. In the absence of these clinical studies, this review aims to summarize the currently available therapeutic strategies in anemia management of CKD patients with concomitant cancer.

      Abbreviations:

      AID (absolute iron deficiency), CKD (chronic kidney disease), eGFR (estimated glomerular filtration Rate), ESA (erythropoiesis-stimulating agents), FID (functional iron deficiency), Hb (hemoglobin), IU (international units), IV (intravenous), TSAT (transferrin saturation)

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to European Journal of Internal Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Koury M.J.
        • Haase V.H.
        Anaemia in kidney disease: harnessing hypoxia responses for therapy.
        Nat Rev Nephrol. 2015; 11: 394-410
        • Knight K.
        • Wade S.
        • Balducci L.
        Prevalence and outcomes of anemia in cancer: a systematic review of the literature.
        Am J Med. 2004; 116: 11S-26S
        • Gilreath J.A.
        • Stenehjem D.D.
        • Rodgers G.M.
        Diagnosis and treatment of cancer-related anemia.
        Am J Hematol. 2014; 89: 203-212
        • Coiffier B.
        The impact and management of anaemia in haematological malignancies.
        Med Oncol. 2000; 17: S2-10
        • Ludwig H.
        • Fritz E.
        Anemia in cancer patients.
        Semin Oncol. 1998; 25: 2-6
        • Means Jr., R.T.
        • Krantz S.B.
        Progress in understanding the pathogenesis of the anemia of chronic disease.
        Blood. 1992; 80: 1639-1647
        • Tisi M.C.
        • Bozzoli V.
        • Giachelia M.
        • Massini G.
        • Ricerca B.M.
        • Maiolo E.
        • et al.
        Anemia in diffuse large B-cell non-Hodgkin lymphoma: the role of interleukin-6, hepcidin and erythropoietin.
        Leuk Lymphoma. 2014; 55: 270-275
        • Zarrabi M.H.
        • Lysik R.
        • DiStefano J.
        • Zucker S.
        The anaemia of chronic disorders: studies of iron reutilization in the anaemia of experimental malignancy and chronic inflammation.
        Br J Haematol. 1977; 35: 647-658
        • Nemeth E.
        • Tuttle M.S.
        • Powelson J.
        • Vaughn M.B.
        • Donovan A.
        • Ward D.M.
        • et al.
        Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization.
        Science. 2004; 306: 2090-2093
        • Singh A.K.
        • Szczech L.
        • Tang K.L.
        • Barnhart H.
        • Sapp S.
        • Wolfson M.
        • et al.
        Correction of anemia with epoetin alfa in chronic kidney disease.
        N Engl J Med. 2006; 355: 2085-2098
        • Jurkovitz C.T.
        • Abramson J.L.
        • Vaccarino L.V.
        • Weintraub W.S.
        • McClellan W.M.
        Association of high serum creatinine and anemia increases the risk of coronary events: results from the prospective community-based atherosclerosis risk in communities (ARIC) study.
        J Am Soc Nephrol. 2003; 14: 2919-2925
        • Sarnak M.J.
        • Tighiouart H.
        • Manjunath G.
        • MacLeod B.
        • Griffith J.
        • Salem D.
        • et al.
        Anemia as a risk factor for cardiovascular disease in the atherosclerosis risk in communities (ARIC) study.
        J Am Coll Cardiol. 2002; 40: 27-33
        • Abramson J.L.
        • Jurkovitz C.T.
        • Vaccarino V.
        • Weintraub W.S.
        • McClellan W.
        Chronic kidney disease, anemia, and incident stroke in a middle-aged, community-based population: the ARIC study.
        Kidney Int. 2003; 64: 610-615
        • Caro J.J.
        • Salas M.
        • Ward A.
        • Goss G.
        Anemia as an independent prognostic factor for survival in patients with cancer: a systemic, quantitative review.
        Cancer. 2001; 91: 2214-2221
        • Locatelli F.
        • Pisoni R.L.
        • Combe C.
        • Bommer J.
        • Andreucci V.E.
        • Piera L.
        • et al.
        Anaemia in haemodialysis patients of five European countries: association with morbidity and mortality in the dialysis outcomes and practice patterns study (DOPPS).
        Nephrol Dial Transplant. 2004; 19: 121-132
        • Henke M.
        • Laszig R.
        • Rube C.
        • Schafer U.
        • Haase K.D.
        • Schilcher B.
        • et al.
        Erythropoietin to treat head and neck cancer patients with anaemia undergoing radiotherapy: randomised, double-blind, placebo-controlled trial.
        Lancet. 2003; 362: 1255-1260
        • Bennett C.L.
        • Silver S.M.
        • Djulbegovic B.
        • Samaras A.T.
        • Blau C.A.
        • Gleason K.J.
        • et al.
        Venous thromboembolism and mortality associated with recombinant erythropoietin and darbepoetin administration for the treatment of cancer-associated anemia.
        JAMA. 2008; 299: 914-924
        • Pfeffer M.A.
        • Burdmann E.A.
        • Chen C.Y.
        • Cooper M.E.
        • de Zeeuw D.
        • Eckardt K.U.
        • et al.
        A trial of darbepoetin alfa in type 2 diabetes and chronic kidney disease.
        N Engl J Med. 2009; 361: 2019-2032
        • Leyland-Jones B.
        • Investigators B.
        • Study G.
        Breast cancer trial with erythropoietin terminated unexpectedly.
        Lancet Oncol. 2003; 4: 459-460
        • Wright J.R.
        • Ung Y.C.
        • Julian J.A.
        • Pritchard K.I.
        • Whelan T.J.
        • Smith C.
        • et al.
        Randomized, double-blind, placebo-controlled trial of erythropoietin in non-small-cell lung cancer with disease-related anemia.
        J Clin Oncol. 2007; 25: 1027-1032
        • Drueke T.B.
        • Locatelli F.
        • Clyne N.
        • Eckardt K.U.
        • Macdougall I.C.
        • Tsakiris D.
        • et al.
        Normalization of hemoglobin level in patients with chronic kidney disease and anemia.
        N Engl J Med. 2006; 355: 2071-2084
        • Winkelmayer W.C.
        Against TREATing all patients alike: lessons from an FDA advisory committee meeting.
        J Am Soc Nephrol. 2011; 22: 1-2
        • Drueke T.B.
        • Parfrey P.S.
        Summary of the KDIGO guideline on anemia and comment: reading between the (guide)line(s).
        Kidney Int. 2012; 82: 952-960
        • Thamer M.
        • Zhang Y.
        • Kshirsagar O.
        • Cotter D.J.
        • Kaufman J.S.
        Erythropoiesis-stimulating agent use among non-dialysis-dependent CKD patients before and after the trial to reduce cardiovascular events with Aranesp therapy (TREAT) using a large US health plan database.
        Am J Kidney Dis. 2014; 64: 706-713
        • Williams A.W.
        • Dwyer A.C.
        • Eddy A.A.
        • Fink J.C.
        • Jaber B.L.
        • Linas S.L.
        • et al.
        Critical and honest conversations: the evidence behind the “choosing wisely” campaign recommendations by the American Society of Nephrology.
        Clin J Am Soc Nephrol. 2012; 7: 1664-1672
        • FDA Drug Safety Communication
        Modified dosing recommendations to improve the safe use of erythropoiesis-stimulating agents (ESAs) in chronic kidney disease.
        • Locatelli F.
        • Barany P.
        • Covic A.
        • De Francisco A.
        • Del Vecchio L.
        • Goldsmith D.
        • et al.
        Kidney disease: improving global outcomes guidelines on anaemia management in chronic kidney disease: a European renal best practice position statement.
        Nephrol Dial Transplant. 2013; 28: 1346-1359
        • Ludwig H.
        • Van Belle S.
        • Barrett-Lee P.
        • Birgegard G.
        • Bokemeyer C.
        • Gascon P.
        • et al.
        The European cancer anaemia survey (ECAS): a large, multinational, prospective survey defining the prevalence, incidence, and treatment of anaemia in cancer patients.
        Eur J Cancer. 2004; 40: 2293-2306
        • Szkandera J.
        • Gerger A.
        • Liegl-Atzwanger B.
        • Stotz M.
        • Samonigg H.
        • Ploner F.
        • et al.
        Pre-treatment anemia is a poor prognostic factor in soft tissue sarcoma patients.
        PLoS One. 2014; 9e107297
        • Troppan K.T.
        • Melchardt T.
        • Deutsch A.
        • Schlick K.
        • Stojakovic T.
        • Bullock M.D.
        • et al.
        The significance of pretreatment anemia in the era of R-IPI and NCCN-IPI prognostic risk assessment tools: a dual-center study in diffuse large B-cell lymphoma patients.
        Eur J Haematol. 2015; 95: 538-544
        • Henry D.H.
        Parenteral iron therapy in cancer-associated anemia.
        Hematol Am Soc Hematol Educ Program. 2010; 2010: 351-356
        • Carless P.A.
        • Henry D.A.
        • Carson J.L.
        • Hebert P.P.
        • McClelland B.
        • Ker K.
        Transfusion thresholds and other strategies for guiding allogeneic red blood cell transfusion.
        Cochrane Database Syst Rev. 2010; CD002042
        • Littlewood T.J.
        • Bajetta E.
        • Nortier J.W.
        • Vercammen E.
        • Rapoport B.
        • Epoetin Alfa Study G
        Effects of epoetin alfa on hematologic parameters and quality of life in cancer patients receiving nonplatinum chemotherapy: results of a randomized, double-blind, placebo-controlled trial.
        J Clin Oncol. 2001; 19: 2865-2874
        • Vansteenkiste J.
        • Pirker R.
        • Massuti B.
        • Barata F.
        • Font A.
        • Fiegl M.
        • et al.
        Double-blind, placebo-controlled, randomized phase III trial of darbepoetin alfa in lung cancer patients receiving chemotherapy.
        J Natl Cancer Inst. 2002; 94: 1211-1220
        • Tonia T.
        • Mettler A.
        • Robert N.
        • Schwarzer G.
        • Seidenfeld J.
        • Weingart O.
        • et al.
        Erythropoietin or darbepoetin for patients with cancer.
        Cochrane Database Syst Rev. 2012; 12CD003407
        • Glaspy J.
        • Crawford J.
        • Vansteenkiste J.
        • Henry D.
        • Rao S.
        • Bowers P.
        • et al.
        Erythropoiesis-stimulating agents in oncology: a study-level meta-analysis of survival and other safety outcomes.
        Br J Cancer. 2010; 102: 301-315
        • Ludwig H.
        • Crawford J.
        • Osterborg A.
        • Vansteenkiste J.
        • Henry D.H.
        • Fleishman A.
        • et al.
        Pooled analysis of individual patient-level data from all randomized, double-blind, placebo-controlled trials of darbepoetin alfa in the treatment of patients with chemotherapy-induced anemia.
        J Clin Oncol. 2009; 27: 2838-2847
        • Spivak J.L.
        • Gascon P.
        • Ludwig H.
        Anemia management in oncology and hematology.
        Oncologist. 2009; 14: 43-56
        • Bohlius J.
        • Schmidlin K.
        • Brillant C.
        • Schwarzer G.
        • Trelle S.
        • Seidenfeld J.
        • et al.
        Erythropoietin or darbepoetin for patients with cancer—meta-analysis based on individual patient data.
        Cochrane Database Syst Rev. 2009; CD007303
        • Hazzan A.D.
        • Shah H.H.
        • Hong S.
        • Sakhiya V.
        • Wanchoo R.
        • Fishbane S.
        Treatment with erythropoiesis-stimulating agents in chronic kidney disease patients with cancer.
        Kidney Int. 2014; 86: 34-39
        • Untch M.
        • Fasching P.A.
        • Konecny G.E.
        • von Koch F.
        • Conrad U.
        • Fett W.
        • et al.
        PREPARE trial: a randomized phase III trial comparing preoperative, dose-dense, dose-intensified chemotherapy with epirubicin, paclitaxel and CMF versus a standard-dosed epirubicin/cyclophosphamide followed by paclitaxel +/− darbepoetin alfa in primary breast cancer—results at the time of surgery.
        Ann Oncol. 2011; 22: 1988-1998
        • Ohashi Y.
        • Uemura Y.
        • Fujisaka Y.
        • Sugiyama T.
        • Ohmatsu H.
        • Katsumata N.
        • et al.
        Meta-analysis of epoetin beta and darbepoetin alfa treatment for chemotherapy-induced anemia and mortality: individual patient data from Japanese randomized, placebo-controlled trials.
        Cancer Sci. 2013; 104: 481-485
        • Schrijvers D.
        • De Samblanx H.
        • Roila F.
        • Group E.G.W.
        Erythropoiesis-stimulating agents in the treatment of anaemia in cancer patients: ESMO clinical practice guidelines for use.
        Ann Oncol. 2010; 21: v244-v247
        • Rizzo J.D.
        • Brouwers M.
        • Hurley P.
        • Seidenfeld J.
        • Arcasoy M.O.
        • Spivak J.L.
        • et al.
        American Society of Clinical Oncology/American Society of Hematology clinical practice guideline update on the use of epoetin and darbepoetin in adult patients with cancer.
        J Clin Oncol. 2010; 28: 4996-5010
        • Adamson J.W.
        The anemia of inflammation/malignancy: mechanisms and management.
        Hematol Am Soc Hematol Educ Program. 2008; : 159-165
        • Aapro M.
        • Osterborg A.
        • Gascon P.
        • Ludwig H.
        • Beguin Y.
        Prevalence and management of cancer-related anaemia, iron deficiency and the specific role of i.v. iron.
        Ann Oncol. 2012; 23: 1954-1962
        • Thomas D.W.
        • Hinchliffe R.F.
        • Briggs C.
        • Macdougall I.C.
        • Littlewood T.
        • Cavill I.
        • et al.
        Guideline for the laboratory diagnosis of functional iron deficiency.
        Br J Haematol. 2013; 161: 639-648
        • Steensma D.P.
        • Sloan J.A.
        • Dakhil S.R.
        • Dalton R.
        • Kahanic S.P.
        • Prager D.J.
        • et al.
        Phase III, randomized study of the effects of parenteral iron, oral iron, or no iron supplementation on the erythropoietic response to darbepoetin alfa for patients with chemotherapy-associated anemia.
        J Clin Oncol. 2011; 29: 97-105
        • Hedenus M.
        • Karlsson T.
        • Ludwig H.
        • Rzychon B.
        • Felder M.
        • Roubert B.
        • et al.
        Intravenous iron alone resolves anemia in patients with functional iron deficiency and lymphoid malignancies undergoing chemotherapy.
        Med Oncol. 2014; 31: 302
        • Auerbach M.
        • Ballard H.
        • Trout J.R.
        • McIlwain M.
        • Ackerman A.
        • Bahrain H.
        • et al.
        Intravenous iron optimizes the response to recombinant human erythropoietin in cancer patients with chemotherapy-related anemia: a multicenter, open-label, randomized trial.
        J Clin Oncol. 2004; 22: 1301-1307
        • Hedenus M.
        • Birgegard G.
        • Nasman P.
        • Ahlberg L.
        • Karlsson T.
        • Lauri B.
        • et al.
        Addition of intravenous iron to epoetin beta increases hemoglobin response and decreases epoetin dose requirement in anemic patients with lymphoproliferative malignancies: a randomized multicenter study.
        Leukemia. 2007; 21: 627-632
        • Henry D.H.
        • Dahl N.V.
        • Auerbach M.
        • Tchekmedyian S.
        • Laufman L.R.
        Intravenous ferric gluconate significantly improves response to epoetin alfa versus oral iron or no iron in anemic patients with cancer receiving chemotherapy.
        Oncologist. 2007; 12: 231-242
        • Petrelli F.
        • Borgonovo K.
        • Cabiddu M.
        • Lonati V.
        • Barni S.
        Addition of iron to erythropoiesis-stimulating agents in cancer patients: a meta-analysis of randomized trials.
        J Cancer Res Clin Oncol. 2012; 138: 179-187
      1. National Comprehensive Cancer Network Clinical Practice Guidelines in oncology (NCCN guidelines®) cancer- and chemotherapy-induced anemia. Version 2.2016.
        • Ludwig H.
        • Evstatiev R.
        • Kornek G.
        • Aapro M.
        • Bauernhofer T.
        • Buxhofer-Ausch V.
        • et al.
        Iron metabolism and iron supplementation in cancer patients.
        Wien Klin Wochenschr. 2015; 127: 907-919
        • Prabhu M.V.
        • Nayak A.
        • Sridhar G.
        • Subhramanyam S.V.
        • Nayak K.S.
        Maximizing the erythropoietin response: iron strategies.
        Contrib Nephrol. 2012; 178: 95-99
        • KDIGO
        Clinical practice guideline for anemia in chronic kidney disease.
        Kidney Int Suppl. 2011; 2012: 279
        • Qunibi W.Y.
        • Martinez C.
        • Smith M.
        • Benjamin J.
        • Mangione A.
        • Roger S.D.
        A randomized controlled trial comparing intravenous ferric carboxymaltose with oral iron for treatment of iron deficiency anaemia of non-dialysis-dependent chronic kidney disease patients.
        Nephrol Dial Transplant. 2011; 26: 1599-1607
        • Besarab A.
        • Coyne D.W.
        Iron supplementation to treat anemia in patients with chronic kidney disease.
        Nat Rev Nephrol. 2010; 6: 699-710
        • Kapoian T.
        • O'Mara N.B.
        • Singh A.K.
        • Moran J.
        • Rizkala A.R.
        • Geronemus R.
        • et al.
        Ferric gluconate reduces epoetin requirements in hemodialysis patients with elevated ferritin.
        J Am Soc Nephrol. 2008; 19: 372-379
        • Macdougall I.C.
        • Bock A.H.
        • Carrera F.
        • Eckardt K.U.
        • Gaillard C.
        • Van Wyck D.
        • et al.
        FIND-CKD: a randomized trial of intravenous ferric carboxymaltose versus oral iron in patients with chronic kidney disease and iron deficiency anaemia.
        Nephrol Dial Transplant. 2014; 29: 2075-2084
        • Kalra P.A.
        • Bhandari S.
        • Saxena S.
        • Agarwal D.
        • Wirtz G.
        • Kletzmayr J.
        • et al.
        A randomized trial of iron isomaltoside 1000 versus oral iron in non-dialysis-dependent chronic kidney disease patients with anaemia.
        Nephrol Dial Transplant. 2015; 31: 646-655
        • Schmid H.
        • Lederer S.R.
        Novel iron-containing phosphate binders for treatment of hyperphosphatemia.
        Expert Opin Pharmacother. 2015; 16: 2179-2191
        • Negri A.L.
        • Urena Torres P.A.
        Iron-based phosphate binders: do they offer advantages over currently available phosphate binders?.
        Clin Kidney J. 2015; 8: 161-167
        • Vaziri N.D.
        • Kalantar-Zadeh K.
        • Wish J.B.
        New options for iron supplementation in maintenance hemodialysis patients.
        Am J Kidney Dis. 2016; 67: 367-375
        • Gupta A.
        • Lin V.
        • Guss C.
        • Pratt R.
        • Ikizler T.A.
        • Besarab A.
        Ferric pyrophosphate citrate administered via dialysate reduces erythropoiesis-stimulating agent use and maintains hemoglobin in hemodialysis patients.
        Kidney Int. 2015; 88: 1187-1194
        • Fishbane S.N.
        • Singh A.K.
        • Cournoyer S.H.
        • Jindal K.K.
        • Fanti P.
        • Guss C.D.
        • et al.
        Ferric pyrophosphate citrate (Triferic) administration via the dialysate maintains hemoglobin and iron balance in chronic hemodialysis patients.
        Nephrol Dial Transplant. 2015; 30: 2019-2026
        • Agarwal R.
        • Kusek J.W.
        • Pappas M.K.
        A randomized trial of intravenous and oral iron in chronic kidney disease.
        Kidney Int. 2015; 88: 905-914
        • Nigwekar S.U.
        • Kroshinsky D.
        • Nazarian R.M.
        • Goverman J.
        • Malhotra R.
        • Jackson V.A.
        • et al.
        Calciphylaxis: risk factors, diagnosis, and treatment.
        Am J Kidney Dis. 2015; 66: 133-146
        • Van Buren P.
        • Velez R.L.
        • Vaziri N.D.
        • Zhou X.J.
        Iron overdose: a contributor to adverse outcomes in randomized trials of anemia correction in CKD.
        Int Urol Nephrol. 2012; 44: 499-507
        • Lapice E.
        • Masulli M.
        • Vaccaro O.
        Iron deficiency and cardiovascular disease: an updated review of the evidence.
        Curr Atheroscler Rep. 2013; 15: 358
        • Gujja P.
        • Rosing D.R.
        • Tripodi D.J.
        • Shizukuda Y.
        Iron overload cardiomyopathy: better understanding of an increasing disorder.
        J Am Coll Cardiol. 2010; 56: 1001-1012
        • Locatelli F.
        • Pozzoni P.
        • Tentori F.
        • del Vecchio L.
        Epidemiology of cardiovascular risk in patients with chronic kidney disease.
        Nephrol Dial Transplant. 2003; 18: vii2-vi9.
        • Foley R.N.
        • Murray A.M.
        • Li S.
        • Herzog C.A.
        • McBean A.M.
        • Eggers P.W.
        • et al.
        Chronic kidney disease and the risk for cardiovascular disease, renal replacement, and death in the United States Medicare population, 1998 to 1999.
        J Am Soc Nephrol. 2005; 16: 489-495
        • Kuragano T.
        • Matsumura O.
        • Matsuda A.
        • Hara T.
        • Kiyomoto H.
        • Murata T.
        • et al.
        Association between hemoglobin variability, serum ferritin levels, and adverse events/mortality in maintenance hemodialysis patients.
        Kidney Int. 2014; 86: 845-854
        • Bailie G.R.
        • Larkina M.
        • Goodkin D.A.
        • Li Y.
        • Pisoni R.L.
        • Bieber B.
        • et al.
        Data from the dialysis outcomes and practice patterns study validate an association between high intravenous iron doses and mortality.
        Kidney Int. 2015; 87: 162-168
        • Karaboyas A.
        • Zee J.
        • Morgenstern H.
        • Nolen J.G.
        • Hakim R.
        • Kalantar-Zadeh K.
        • et al.
        Understanding the recent increase in ferritin levels in United States dialysis patients: potential impact of changes in intravenous iron and erythropoiesis-stimulating agent dosing.
        Clin J Am Soc Nephrol. 2015; 10: 1814-1821
      2. The European Union clinical trials register.
        (Available at:)
        • Maisonneuve P.
        • Agodoa L.
        • Gellert R.
        • Stewart J.H.
        • Buccianti G.
        • Lowenfels A.B.
        • et al.
        Cancer in patients on dialysis for end-stage renal disease: an international collaborative study.
        Lancet. 1999; 354: 93-99
        • Stengel B.
        Chronic kidney disease and cancer: a troubling connection.
        J Nephrol. 2010; 23: 253-262
        • Lin M.Y.
        • Kuo M.C.
        • Hung C.C.
        • Wu W.J.
        • Chen L.T.
        • Yu M.L.
        • et al.
        Association of dialysis with the risks of cancers.
        PLoS One. 2015; 10e0122856
        • Stewart J.H.
        • Buccianti G.
        • Agodoa L.
        • Gellert R.
        • McCredie M.R.
        • Lowenfels A.B.
        • et al.
        Cancers of the kidney and urinary tract in patients on dialysis for end-stage renal disease: analysis of data from the United States, Europe, and Australia and New Zealand.
        J Am Soc Nephrol. 2003; 14: 197-207
        • Butler A.M.
        • Olshan A.F.
        • Kshirsagar A.V.
        • Edwards J.K.
        • Nielsen M.E.
        • Wheeler S.B.
        • et al.
        Cancer incidence among US Medicare ESRD patients receiving hemodialysis, 1996-2009.
        Am J Kidney Dis. 2015; 65: 763-772
        • Vajdic C.M.
        • McDonald S.P.
        • McCredie M.R.
        • van Leeuwen M.T.
        • Stewart J.H.
        • Law M.
        • et al.
        Cancer incidence before and after kidney transplantation.
        JAMA. 2006; 296: 2823-2831
        • Birkeland S.A.
        • Lokkegaard H.
        • Storm H.H.
        Cancer risk in patients on dialysis and after renal transplantation.
        Lancet. 2000; 355: 1886-1887
        • Izzedine H.
        • Perazella M.A.
        Onco-nephrology: an appraisal of the cancer and chronic kidney disease links.
        Nephrol Dial Transplant. 2015; 30: 1979-1988
        • Pedotti P.
        • Cardillo M.
        • Rossini G.
        • Arcuri V.
        • Boschiero L.
        • Caldara R.
        • et al.
        Incidence of cancer after kidney transplant: results from the North Italy transplant program.
        Transplantation. 2003; 76: 1448-1451
        • Launay-Vacher V.
        • Oudard S.
        • Janus N.
        • Gligorov J.
        • Pourrat X.
        • Rixe O.
        • et al.
        Prevalence of renal insufficiency in cancer patients and implications for anticancer drug management: the renal insufficiency and anticancer medications (IRMA) study.
        Cancer. 2007; 110: 1376-1384
        • Janus N.
        • Launay-Vacher V.
        • Byloos E.
        • Machiels J.P.
        • Duck L.
        • Kerger J.
        • et al.
        Cancer and renal insufficiency results of the BIRMA study.
        Br J Cancer. 2010; 103: 1815-1821
        • Szenajch J.
        • Wcislo G.
        • Jeong J.Y.
        • Szczylik C.
        • Feldman L.
        The role of erythropoietin and its receptor in growth, survival and therapeutic response of human tumor cells from clinic to bench — a critical review.
        Biochim Biophys Acta. 1806; 2010: 82-95
        • Oster H.S.
        • Neumann D.
        • Hoffman M.
        • Mittelman M.
        Erythropoietin: the swinging pendulum.
        Leuk Res. 2012; 36: 939-944
        • Butler A.M.
        • Kshirsagar A.V.
        • Olshan A.F.
        • Nielsen M.E.
        • Wheeler S.B.
        • Brookhart M.A.
        Trends in anemia management in hemodialysis patients with cancer.
        Am J Nephrol. 2015; 42: 206-215
        • Macdougall I.C.
        Iron supplementation in nephrology and oncology: what do we have in common?.
        Oncologist. 2011; 16: 25-34
        • Ganzoni A.M.
        Intravenous iron-dextran: therapeutic and experimental possibilities.
        Schweiz Med Wochenschr. 1970; 100: 301-303