563
Views
21
CrossRef citations to date
0
Altmetric
Review

Management of inflammatory bowel disease-related anemia and iron deficiency with specific reference to the role of intravenous iron in current practice

ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon
Pages 1721-1737 | Received 25 Jun 2017, Accepted 10 Oct 2017, Published online: 05 Nov 2017

References

  • Fiorino G, Allocca M, Danese S. Anemia in inflammatory bowel disease: the opening of pandora’s box?. Clin Gastroenterol Hepatol. 2015;13:1767–1769.
  • Larsen S, Bendtzen K, Nielsen OH. Extraintestinal manifestations of inflammatory bowel disease: epidemiology, diagnosis, and management. Ann Med. 2010;42:97–114.
  • Danese S, Hoffman C, Vel S, et al. Anaemia from a patient perspective in inflammatory bowel disease: results from the European Federation of Crohn’s and Ulcerative Colitis Association’s online survey. Eur J Gastroenterol Hepatol. 2014;26:1385–1391.
  • Stein J, Bager P, Befrits R, et al. Anaemia management in patients with inflammatory bowel disease: routine practice across nine European countries. Eur J Gastroenterol Hepatol. 2013;25:1456–1463.
  • Blumenstein I, Dignass A, Vollmer S, et al. Current practice in the diagnosis and management of IBD-associated anaemia and iron deficiency in Germany: the German AnaemIBD Study. J Crohns Colitis. 2014;8:1308–1314.
  • Bager P, Befrits R, Wikman O, et al. The prevalence of anemia and iron deficiency in IBD outpatients in Scandinavia. Scand J Gastroenterol. 2011;46:304–309.
  • Voegtlin M, Vavricka SR, Schoepfer AM, et al. Prevalence of anaemia in inflammatory bowel disease in Switzerland: a cross-sectional study in patients from private practices and university hospitals. J Crohns Colitis. 2010;4:642–648.
  • Bager P, Befrits R, Wikman O, et al. High burden of iron deficiency and different types of anemia in inflammatory bowel disease outpatients in Scandinavia: a longitudinal 2-year follow-up study. Scand J Gastroenterol. 2013;48:1286–1293.
  • Goodhand JR, Kamperidis N, Rao A, et al. Prevalence and management of anemia in children, adolescents, and adults with inflammatory bowel disease. Inflamm Bowel Dis. 2012;18:513–519.
  • Stein J, Dignass AU. Anaemia in the Elderly IBD Patient. Curr Treat Options Gastroenterol. 2015;13:308–318.
  • Rejler M, Tholstrup J, Andersson-Gare B, et al. Low prevalence of anemia in inflammatory bowel disease: a population-based study in Sweden. Scand J Gastroenterol. 2012;47:937–942.
  • Stein J, Dignass AU. Management of iron deficiency anemia in inflammatory bowel disease - a practical approach. Ann Gastroenterol. 2013;26:104–113.
  • Ershler WB, Chen K, Reyes EB, et al. Economic burden of patients with anemia in selected diseases. Value Health. 2005;8:629–638.
  • Wells CW, Lewis S, Barton JR, et al. Effects of changes in hemoglobin level on quality of life and cognitive function in inflammatory bowel disease patients. Inflamm Bowel Dis. 2006;12:123–130.
  • Lopez A, Cacoub P, Macdougall IC, et al. Iron deficiency anaemia. The Lancet. 2016;387:907–916.
  • Dignass AU, Gasche C, Bettenworth D, et al. European consensus on the diagnosis and management of iron deficiency and anaemia in inflammatory bowel diseases. J Crohns Colitis. 2015;9:211–222.
  • Stein J, Hartmann F, Dignass AU. Diagnosis and management of iron deficiency anemia in patients with IBD. Nat Rev Gastroenterol Hepatol. 2010;7:599–610.
  • Walker AM, Szneke P, Bianchi LA, et al. 5-Aminosalicylates, sulfasalazine, steroid use, and complications in patients with ulcerative colitis. Am J Gastroenterol. 1997;92:816–820.
  • Schwab M, Schaffeler E, Marx C, et al. Azathioprine therapy and adverse drug reactions in patients with inflammatory bowel disease: impact of thiopurine S-methyltransferase polymorphism. Pharmacogenetics. 2002;12:429–436.
  • Blanchet E, Beau P, Frat JP. [Bone marrow aplasia following dipyrone treatment in a patient with Crohn’s disease receiving long-term methotrexate]. Gastroenterol Clin Biol. 2004;28:502–503.
  • Danesi R, Del Tacca M. Hematologic toxicity of immunosuppressive treatment. Transplant Proc. 2004;36:703–704.
  • Mast AE, Blinder MA, Gronowski AM, et al. Clinical utility of the soluble transferrin receptor and comparison with serum ferritin in several populations. Clin Chem. 1998;44:45–51.
  • Sharma N, Begum J, Eksteen B, et al. Differential ferritin expression is associated with iron deficiency in coeliac disease. Eur J Gastroenterol Hepatol. 2009;21:794–804.
  • Johnson D, Bayele H, Johnston K, et al. Tumour necrosis factor alpha regulates iron transport and transporter expression in human intestinal epithelial cells. FEBS Lett. 2004;573:195–201.
  • Cartwright GE, Lauritsen MA, Humphreys S, et al. The anemia associated with chronic infection. Science. 1946;103:72–73.
  • Weiss G, Goodnough LT. Anemia of chronic disease. N Engl J Med. 2005;352:1011–1023.
  • Nemeth E, Ganz T. Anemia of inflammation. Hematol Oncol Clin North Am. 2014;28: 671–681. vi.
  • Zarychanski R, Houston DS. Anemia of chronic disease: a harmful disorder or an adaptive, beneficial response? Cmaj. 2008;179:333–337.
  • Van Assche G, Dignass A, Bokemeyer B, et al. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 3: special situations. J Crohns Colitis. 2013;7:1–33.
  • Weiss G, Schett G. Anaemia in inflammatory rheumatic diseases. Nat Rev Rheumatol. 2013;9:205–215.
  • Stein J, Stier C, Raab H, et al. Review article: the nutritional and pharmacological consequences of obesity surgery. Aliment Pharmacol Ther. 2014;40:582–609.
  • Thomas C, Thomas L. Anemia of chronic disease: pathophysiology and laboratory diagnosis. Lab. Hematol. 2005;11(1):14–23.
  • Macdougall IC, Geisser P. Use of intravenous iron supplementation in chronic kidney disease: an update. Iran J Kidney Dis. 2013;7:9–22.
  • Wish JB. Assessing iron status: beyond serum ferritin and transferrin saturation. Clin J Am Soc Nephrol. 2006;1 Suppl 1:S4–8.
  • Martin J, Radeke HH, Dignass A, et al. Current evaluation and management of anemia in patients with inflammatory bowel disease. Expert Rev Gastroenterol Hepatol. 2017;11:19–32.
  • Heimpel H, Diem H, Nebe T. Counting reticulocytes: new importance of an old method. Med Klin (Munich). 2010;105:538–543.
  • Punnonen K, Irjala K, Rajamaki A. Serum transferrin receptor, ferritin and TfR-F index in identification of latent iron deficiency. Eur J Haematol. 1998;60:135–137.
  • Harms K, Kaiser T. Beyond soluble transferrin receptor: old challenges and new horizons. Best Pract Res Clin Endocrinol Metab. 2015;29:799–810.
  • Junca J, Fernandez-Aviles F, Oriol A, et al. The usefulness of the serum transferrin receptor in detecting iron deficiency in the anemia of chronic disorders. Haematologica. 1998;83:676–680.
  • Skikne BS, Punnonen K, Caldron PH, et al. Improved differential diagnosis of anemia of chronic disease and iron deficiency anemia: a prospective multicenter evaluation of soluble transferrin receptor and the sTfR/log ferritin index. Am J Hematol. 2011;86:923–927.
  • Oustamanolakis P, Koutroubakis IE, Messaritakis I, et al. Soluble transferrin receptor-ferritin index in the evaluation of anemia in inflammatory bowel disease: a case-control study. Ann Gastroenterol. 2011;24:108–114.
  • Abitbol V, Borderie D, Polin V, et al. Diagnosis of iron deficiency in inflammatory bowel disease by transferrin receptor-ferritin index. Medicine (Baltimore). 2015;94:e1011.
  • Brugnara C, Mohandas N. Red cell indices in classification and treatment of anemias: from M.M. Wintrobes’s original 1934 classification to the third millennium. Curr Opin Hematol. 2013;20:222–230.
  • Urrechaga E, Borque L, Escanero JF. Percentage of hypochromic erythrocytes as a potential marker of iron availability. Clin Chem Lab Med. 2012;50:685–687.
  • Parodi E, Giraudo MT, Davitto M, et al. Reticulocyte parameters: markers of early response to oral treatment in children with severe iron-deficiency anemia. J Pediatr Hematol Oncol. 2012;34:e249–52.
  • Dagg JH, Goldberg A, Lochhead A. Value of erythrocyte protoporphyrin in the diagnosis of latent iron deficiency (sideropenia). Br J Haematol. 1966;12:326–330.
  • Hastka J, Lasserre JJ, Schwarzbeck A, et al. Zinc protoporphyrin in anemia of chronic disorders. Blood. 1993;81:1200–1204.
  • Wiesenthal M, Dienethal A, Dignass AU, et al. Diagnostic accuracy of zinc protoporphyrin/heme ratio for screening of iron deficiency anaemia in patients with inflammatory bowel disease. Gastroenterology. 2014;146:S599–S599.
  • Akkermans MD, Vreugdenhil M, Hendriks DM, et al. Iron deficiency in inflammatory bowel disease: the use of zincprotoporphyrin and red blood cell distribution width. J Pediatr Gastroenterol Nutr. 2017;64(6):949–954.
  • Wiesenthal M, Dignass A, Hartmann F, et al. Serum hepcidin levels predict intestinal iron absorption in IBD patients. J Crohns Colitis. 2014;8:S120–S120.
  • Martinelli M, Strisciuglio C, Alessandrella A, et al. Serum hepcidin and iron absorption in paediatric inflammatory bowel disease. J Crohns Colitis. 2016;10:566–574.
  • Forbes A, Escher J, Hebuterne X, et al. ESPEN guideline: clinical nutrition in inflammatory bowel disease. Clin Nutr. 2017;36:321–347.
  • Tolkien Z, Stecher L, Mander AP, et al. Ferrous sulfate supplementation causes significant gastrointestinal side-effects in adults: a systematic review and meta-analysis. PLoS One. 2015;10:e0117383.
  • Tay HS, Soiza RL. Systematic review and meta-analysis: what is the evidence for oral iron supplementation in treating anaemia in elderly people? Drugs Aging. 2015;32:149–158.
  • Rampton DS, Goodhand JR, Joshi NM, et al. Oral iron treatment response and predictors in anaemic adolescents and adults with IBD: a prospective controlled open-label trial. J Crohns Colitis. 2017;11:706–715.
  • Camaschella C. Iron-deficiency anemia. N Engl J Med. 2015;372:1832–1843.
  • Kortman GA, Raffatellu M, Swinkels DW, et al. Nutritional iron turned inside out: intestinal stress from a gut microbial perspective. FEMS Microbiol Rev. 2014;38:1202–1234.
  • De Silva AD, Tsironi E, Feakins RM, et al. Efficacy and tolerability of oral iron therapy in inflammatory bowel disease: a prospective, comparative trial. Aliment Pharmacol Ther. 2005;22:1097–1105.
  • Erichsen K, Ulvik RJ, Grimstad T, et al. Effects of ferrous sulphate and non-ionic iron-polymaltose complex on markers of oxidative tissue damage in patients with inflammatory bowel disease. Aliment Pharmacol Ther. 2005;22:831–838.
  • Schroder O, Mickisch O, Seidler U, et al. Intravenous iron sucrose versus oral iron supplementation for the treatment of iron deficiency anemia in patients with inflammatory bowel disease–a randomized, controlled, open-label, multicenter study. Am J Gastroenterol. 2005;100:2503–2509.
  • Gisbert JP, Bermejo F, Pajares R, et al. Oral and intravenous iron treatment in inflammatory bowel disease: hematological response and quality of life improvement. Inflamm Bowel Dis. 2009;15:1485–1491.
  • Zimmermann MB, Chassard C, Rohner F, et al. The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Cote d’Ivoire. Am J Clin Nutr. 2010;92:1406–1415.
  • Jaeggi T, Kortman GA, Moretti D, et al. Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants. Gut. 2015;64:731–742.
  • Jimenez K, Kulnigg-Dabsch S, Gasche C. Management of iron deficiency anemia. Gastroenterol Hepatol (N Y). 2015;11:241–250.
  • Hutchinson C, Al-Ashgar W, Liu DY, et al. Oral ferrous sulphate leads to a marked increase in pro-oxidant nontransferrin-bound iron. Eur J Clin Invest. 2004;34:782–784.
  • Dresow B, Petersen D, Fischer R, et al. Non-transferrin-bound iron in plasma following administration of oral iron drugs. Biometals. 2008;21:273–276.
  • Brissot P, Ropert M, Le Lan C, et al. Non-transferrin bound iron: a key role in iron overload and iron toxicity. Biochim Biophys Acta. 2012;1820:403–410.
  • Geisser P, Burckhardt S. The pharmacokinetics and pharmacodynamics of iron preparations. Pharmaceutics. 2011;3:12–33.
  • Kaltwasser JP, Hansen C, Oebike Y, et al. Assessment of iron availability using stable 54Fe. Eur J Clin Invest. 1991;21:436–442.
  • Schumann K, Solomons NW, Romero-Abal ME, et al. Oral administration of ferrous sulfate, but not of iron polymaltose or sodium iron ethylenediaminetetraacetic acid (NaFeEDTA), results in a substantial increase of non-transferrin-bound iron in healthy iron-adequate men. Food Nutr Bull. 2012;33:128–136.
  • Schumann K, Solomons NW, Orozco M, et al. Differences in circulating non-transferrin-bound iron after oral administration of ferrous sulfate, sodium iron EDTA, or iron polymaltose in women with marginal iron stores. Food Nutr Bull. 2013;34:185–193.
  • Santiago P. Ferrous versus ferric oral iron formulations for the treatment of iron deficiency: a clinical overview. Sci World J. 2012;2012:846824.
  • Stallmach A, Buning C. Ferric maltol (ST10): a novel oral iron supplement for the treatment of iron deficiency anemia in inflammatory bowel disease. Expert Opin Pharmacother. 2015;16:2859–2867.
  • Harvey RS, Reffitt DM, Doig LA, et al. Ferric trimaltol corrects iron deficiency anaemia in patients intolerant of iron. Aliment Pharmacol Ther. 1998;12:845–848.
  • Gasche C, Ahmad T, Tulassay Z, et al. Ferric maltol is effective in correcting iron deficiency anemia in patients with inflammatory bowel disease: results from a phase-3 clinical trial program. Inflamm Bowel Dis. 2015;21:579–588.
  • Schmidt C, Ahmad T, Tulassay Z, et al. Ferric maltol therapy for iron deficiency anaemia in patients with inflammatory bowel disease: long-term extension data from a Phase 3 study. Aliment Pharmacol Ther. 2016;44:259–270.
  • Pisani A, Riccio E, Sabbatini M, et al. Effect of oral liposomal iron versus intravenous iron for treatment of iron deficiency anaemia in CKD patients: a randomized trial. Nephrol Dial Transplant. 2015;30:645–652.
  • Mafodda A, Giuffrida D, Prestifilippo A, et al. Oral sucrosomial iron versus intravenous iron in anemic cancer patients without iron deficiency receiving darbepoetin alfa: a pilot study. Support Care Cancer. 2017.
  • Moretti D, Goede JS, Zeder C, et al. Oral iron supplements increase hepcidin and decrease iron absorption from daily or twice-daily doses in iron-depleted young women. Blood. 2015;126:1981–1989.
  • Powell JJ, Cook WB, Hutchinson C, et al. Dietary fortificant iron intake is negatively associated with quality of life in patients with mildly active inflammatory bowel disease. Nutr Metab (Lond). 2013;10:9.
  • Okam MM, Koch TA, Tran MH. Iron supplementation, response in iron-deficiency anemia: analysis of five trials. Am J Med. 2017;130:991e1–991 e8.
  • Avni T, Bieber A, Steinmetz T, et al. Treatment of anemia in inflammatory bowel disease–systematic review and meta-analysis. PLoS One. 2013;8:e75540.
  • Bonovas S, Fiorino G, Allocca M, et al. Intravenous versus oral iron for the treatment of anemia in inflammatory bowel disease: a systematic review and meta-analysis of randomized controlled trials. Medicine (Baltimore). 2016;95:e2308.
  • Lee TW, Kolber MR, Fedorak RN, et al. Iron replacement therapy in inflammatory bowel disease patients with iron deficiency anemia: a systematic review and meta-analysis. J Crohns Colitis. 2012;6:267–275.
  • Gozzard D. When is high-dose intravenous iron repletion needed? Assessing new treatment options. Drug Des Devel Ther. 2011;5:51–60.
  • Toblli JE, Angerosa M. Optimizing iron delivery in the management of anemia: patient considerations and the role of ferric carboxymaltose. Drug Des Devel Ther. 2014;8:2475–2491.
  • Geisser P, Baer M, Schaub E. Structure/histotoxicity relationship of parenteral iron preparations. Arzneimittelforschung. 1992;42:1439–1452.
  • Ganzoni AM. [Intravenous iron-dextran: therapeutic and experimental possibilities]. Schweiz Med Wochenschr. 1970;100:301–303.
  • Evstatiev R, Marteau P, Iqbal T, et al. FERGIcor, a randomized controlled trial on ferric carboxymaltose for iron deficiency anemia in inflammatory bowel disease. Gastroenterology. 2011;141:846-853 e1-2.
  • Schroder O, Schrott M, Blumenstein I, et al. A study for the evaluation of safety and tolerability of intravenous high-dose iron sucrose in patients with iron deficiency anemia due to gastrointestinal bleeding. Z Gastroenterol. 2004;42:663–667.
  • Kulnigg S, Teischinger L, Dejaco C, et al. Rapid recurrence of IBD-associated anemia and iron deficiency after intravenous iron sucrose and erythropoietin treatment. Am J Gastroenterol. 2009;104:1460–1467.
  • Evstatiev R, Alexeeva O, Bokemeyer B, et al. Ferric carboxymaltose prevents recurrence of anemia in patients with inflammatory bowel disease. Clin Gastroenterol Hepatol. 2013;11:269–277.
  • Reinisch W, Altorjay I, Zsigmond F, et al. A 1-year trial of repeated high-dose intravenous iron isomaltoside 1000 to maintain stable hemoglobin levels in inflammatory bowel disease. Scand J Gastroenterol. 2015;50:1226–1233.
  • Chertow GM, Mason PD, Vaage-Nilsen O, et al. Update on adverse drug events associated with parenteral iron. Nephrol Dial Transplant. 2006;21:378–382.
  • Yessayan L, Sandhu A, Besarab A, et al. Intravenous iron dextran as a component of anemia management in chronic kidney disease: a report of safety and efficacy. Int J Nephrol. 2013;2013:703038.
  • Wang C, Graham DJ, Kane RC, et al. Comparative risk of anaphylactic reactions associated with intravenous iron products. Jama. 2015;314:2062–2068.
  • Hussain I, Bhoyroo J, Butcher A, et al. Direct comparison of the safety and efficacy of ferric carboxymaltose versus iron dextran in patients with iron deficiency anemia. Anemia. 2013;2013:169107.
  • Charytan C, Schwenk MH, Al-Saloum MM, et al. Safety of iron sucrose in hemodialysis patients intolerant to other parenteral iron products. Nephron Clin Pract. 2004;96:c63–6.
  • Lee ES, Park BR, Kim JS, et al. Comparison of adverse event profile of intravenous iron sucrose and iron sucrose similar in postpartum and gynecologic operative patients. Curr Med Res Opin. 2013;29:141–147.
  • Rottembourg J, Kadri A, Leonard E, et al. Do two intravenous iron sucrose preparations have the same efficacy? Nephrol Dial Transplant. 2011;26:3262–3267.
  • Stein J, Dignass A, Chow KU. Clinical case reports raise doubts about the therapeutic equivalence of an iron sucrose similar preparation compared with iron sucrose originator. Curr Med Res Opin. 2012;28:241–243.
  • Li X, Kshirsagar AV, Brookhart MA. Safety of intravenous iron in hemodialysis patients. Hemodial Int. 2017;21 Suppl 1:S93–S103.
  • Szebeni J, Fishbane S, Hedenus M, et al. Hypersensitivity to intravenous iron: classification, terminology, mechanisms and management. Br J Pharmacol. 2015;172:5025–5036.
  • Rampton D, Folkersen J, Fishbane S, et al. Hypersensitivity reactions to intravenous iron: guidance for risk minimization and management. Haematologica. 2014;99:1671–1676.
  • Hempel JC, Poppelaars F, Gaya Da Costa M, et al. Distinct in vitro complement activation by various intravenous iron preparations. Am J Nephrol. 2017;45:49–59.
  • (EMA). Assessment report for: iron containing intravenous (IV) medicinal products. [cited 2017 Apr 23]. http://www.ema.europa.eu/docs/en_GB/document_library/Referrals_document/IV_iron_31/WC500150771.pdf 2013.
  • Zoller H, Schaefer B, Glodny B. Iron-induced hypophosphatemia: an emerging complication. Curr Opin Nephrol Hypertens. 2017;26(4):266–275.
  • Schaefer B, Wurtinger P, Finkenstedt A, et al. Choice of high-dose intravenous iron preparation determines hypophosphatemia risk. PLoS One. 2016;11:e0167146.
  • Zoller H, Schaefer B, Glodny B. Iron-induced hypophosphatemia: an emerging complication. Curr Opin Nephrol Hypertens. 2017;26:266–275.
  • Hardy S, Vandemergel X. Intravenous iron administration and hypophosphatemia in clinical practice. Int J Rheumatol. 2015;2015:468675.
  • Farrow EG, Yu X, Summers LJ, et al. Iron deficiency drives an autosomal dominant hypophosphatemic rickets (ADHR) phenotype in fibroblast growth factor-23 (Fgf23) knock-in mice. Proc Natl Acad Sci U S A. 2011;108:E1146–55.
  • Felsenfeld AJ, Levine BS. Approach to treatment of hypophosphatemia. Am J Kidney Dis. 2012;60:655–661.
  • Goldsweig BK, Carpenter TO. Hypophosphatemic rickets: lessons from disrupted FGF23 control of phosphorus homeostasis. Curr Osteoporos Rep. 2015;13:88–97.
  • O’Connor LR, Wheeler WS, Bethune JE. Effect of hypophosphatemia on myocardial performance in man. N Engl J Med. 1977;297:901–903.
  • Geerse DA, Bindels AJ, Kuiper MA, et al. Treatment of hypophosphatemia in the intensive care unit: a review. Crit Care. 2010;14:R147.
  • National cancer institute common terminology criteria for adverse events v4.0 NCI, NIH, DHHS. NIH. https://evs.nci.nih.gov/ftp1/CTCAE/CTCAE_4.03_2010-06-14_QuickReference_5x7.pdf
  • Auerbach M, Macdougall I. The available intravenous iron formulations: history, efficacy, and toxicology. Hemodial Int. 2017;21 Suppl 1:S83–s92.
  • Schroeder SE, Reddy MB, Schalinske KL. Retinoic acid modulates hepatic iron homeostasis in rats by attenuating the RNA-binding activity of iron regulatory proteins. J Nutr. 2007;137:2686–2690.
  • Aksan A, Isik H, Radeke HH, et al. Systematic review with network meta-analysis: comparative efficacy and tolerability of different intravenous iron formulations for the treatment of iron deficiency anaemia in patients with inflammatory bowel disease. Aliment Pharmacol Ther. 2017;45:1303–1318.
  • Kalantar-Zadeh K, Regidor DL, McAllister CJ, et al. Time-dependent associations between iron and mortality in hemodialysis patients. J Am Soc Nephrol. 2005;16:3070–3080.
  • Feldman HI, Joffe M, Robinson B, et al. Administration of parenteral iron and mortality among hemodialysis patients. J Am Soc Nephrol. 2004;15:1623–1632.
  • Beguin Y, Maertens J, De Prijck B, et al. Darbepoetin-alfa and intravenous iron administration after autologous hematopoietic stem cell transplantation: a prospective multicenter randomized trial. Am J Hematol. 2013;88:990–996.
  • Bhandari S. Update of a comparative analysis of cost minimization following the introduction of newly available intravenous iron therapies in hospital practice. Ther Clin Risk Manag. 2011;7:501–509.
  • Calvet X, Ruiz MA, Dosal A, et al. Cost-minimization analysis favours intravenous ferric carboxymaltose over ferric sucrose for the ambulatory treatment of severe iron deficiency. PLoS One. 2012;7:e45604.
  • Bager P, Dahlerup JF. The health care cost of intravenous iron treatment in IBD patients depends on the economic evaluation perspective. J Crohns Colitis. 2010;4:427–430.
  • Tsiolakidou G, Koutroubakis IE. Stimulating erythropoiesis in inflammatory bowel disease associated anemia. World J Gastroenterol. 2007;13:4798–4806.
  • Silverberg DS, Wexler DOV, Iaina A, et al. Anemia, chronic renal disease and chronic heart failure: the cardiorenal anemia syndrome. Transfus Alternatives Transfus Med. 2008;10:189–196.
  • Murphy GJ, Reeves BC, Rogers CA, et al. Increased mortality, postoperative morbidity, and cost after red blood cell transfusion in patients having cardiac surgery. Circulation. 2007;116:2544–2552.
  • Mehra T, Seifert B, Bravo-Reiter S, et al. Implementation of a patient blood management monitoring and feedback program significantly reduces transfusions and costs. Transfusion. 2015;55:2807–2815.
  • Eliadou E, Kini G, Huang J, et al. Intravenous iron replacement improves quality of life in hypoferritinemic inflammatory bowel disease patients with and without anemia. Dig Dis. 2017.
  • Cekic C, Ipek S, Aslan F, et al. The effect of intravenous iron treatment on quality of life in inflammatory bowel disease patients with nonanemic iron deficiency. Gastroenterol Res Pract. 2015;2015:582163.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.