Iron deficiency across chronic inflammatory conditions: International expert opinion on definition, diagnosis, and management

American Journal of Hematology

Volumn 92, Issue 10, 2017, Pages 1068-1078

  Cappellini, Maria Domenica ^a,b   Comin Colet, Josep ^c   de Francisco, Angel ^d   Dignass, Axel ^e   Doehner, Wolfram ^f   S P Lam, Carolyn ^g   Macdougall, Iain C ^h   Rogler, Gerhard ⁱ   Camaschella, Clara ^j   Kadir, Rezan ^k   Kassebaum, Nicholas J ^l   Spahn, Donat R ^m   Taher, Ali T ⁿ   Musallam, Khaled M ^o  

^a FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^d UNIVERSITY OF CANTABRIA   (Spain)

^e AGAPLESION MARKUS KRANKENHAUS   (Germany)

^f CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^g DUKE NUS MEDICAL SCHOOL   (Singapore)

^h KING S COLLEGE HOSPITAL   (United Kingdom)

ⁱ UNIVERSITY OF ZURICH   (Switzerland)

^j SAN RAFFAELE HOSPITAL   (Italy)

^k ROYAL FREE HOSPITAL   (United Kingdom)

^l UNIVERSITY OF WASHINGTON   (United States)

^m UNIVERSITY HOSPITAL ZURICH   (Switzerland)

ⁿ AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

^o International Network of Hematology   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

IRON; ANTIANEMIC AGENT;

CHRONIC INFLAMMATION; CHRONIC KIDNEY FAILURE; CLINICAL OUTCOME; DISEASE ASSOCIATION; HEART FAILURE; HUMAN; INFLAMMATORY BOWEL DISEASE; IRON DEFICIENCY; IRON THERAPY; PRACTICE GUIDELINE; PRIORITY JOURNAL; QUALITY OF LIFE; REVIEW; ANEMIA, IRON-DEFICIENCY; BLOOD; CHRONIC DISEASE; DEFICIENCY; DIFFERENTIAL DIAGNOSIS; DISEASE MANAGEMENT; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INTRAVENOUS DRUG ADMINISTRATION; ORAL DRUG ADMINISTRATION; RENAL INSUFFICIENCY, CHRONIC;

ADMINISTRATION, ORAL; ANEMIA, IRON-DEFICIENCY; CHRONIC DISEASE; DIAGNOSIS, DIFFERENTIAL; DISEASE MANAGEMENT; HEART FAILURE; HEMATINICS; HUMANS; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INJECTIONS, INTRAVENOUS; IRON; RENAL INSUFFICIENCY, CHRONIC;

EID: 85022062254     PISSN: 03618609     EISSN: 10968652     Source Type: Journal    
DOI: 10.1002/ajh.24820     Document Type: Review

References (117)

1. Henriques C. Vifor supports efforts to make public more aware of iron deficiency and its health impact (28 November). IBD News Today 2016. Available at: https://ibdnewstoday.com/2016/11/28/vifor-pharma-supports-efforts-to-raise-awareness-of-iron-deficiency-in-ibd-patients-others/.
2. GBD 2015 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388:1545–1602.
3. Nolte E, Knai C, Saltman RB. Assessing chronic disease management in European health systems: concepts and approaches. 2014. Available at: http://www.euro.who.int/en/about-us/partners/observatory/publications/studies/assessing-chronic-disease-management-in-european-health-systems-concepts-and-approaches.
4. Peyrin-Biroulet L, Williet N, Cacoub P. Guidelines on the diagnosis and treatment of iron deficiency across indications: a systematic review. Am J Clin Nutr. 2015;102:1585–1594.
5. Jankowska EA, Rozentryt P, Witkowska A, et al. Iron deficiency: an ominous sign in patients with systolic chronic heart failure. Eur Heart J. 2010;31:1872–1880.
6. Klip IT, Comin-Colet J, Voors AA, et al. Iron deficiency in chronic heart failure: an international pooled analysis. Am Heart J. 2013;165:575–582.
7. Okonko DO, Mandal AK, Missouris CG, Poole-Wilson PA. Disordered iron homeostasis in chronic heart failure: prevalence, predictors, and relation to anemia, exercise capacity, and survival. J Am Coll Cardiol. 2011;58:1241–1251.
8. McClellan W, Aronoff SL, Bolton WK, et al. The prevalence of anemia in patients with chronic kidney disease. Curr Med Res Opin. 2004;20:1501–1510.
9. Yeo TJ, Yeo PS, Ching-Chiew WR, et al. Iron deficiency in a multi-ethnic Asian population with and without heart failure: prevalence, clinical correlates, functional significance and prognosis. Eur J Heart Fail. 2014;16:1125–1132.
10. Wessling-Resnick M. Iron homeostasis and the inflammatory response. Annu Rev Nutr. 2010;30:105–122.
11. Wang J, Pantopoulos K. Regulation of cellular iron metabolism. Biochem J. 2011;434:365–381.
12. Macdougall IC, Canaud B, de Francisco AL, et al. Beyond the cardiorenal anaemia syndrome: recognizing the role of iron deficiency. Eur J Heart Fail. 2012;14:882–886.
13. Lopez A, Cacoub P, Macdougall IC, Peyrin-Biroulet L. Iron deficiency anaemia. Lancet. 2016;387:907–916.
14. Kassebaum NJ. The global burden of anemia. Hematol Oncol Clin North Am. 2016;30:247–308.
15. Ganz T. Systemic iron homeostasis. Physiol Rev. 2013;93:1721–1741.
16. Ganz T, Nemeth E. The hepcidin-ferroportin system as a therapeutic target in anemias and iron overload disorders. Hematology Am Soc Hematol Educ Program. 2011;2011:538–542.
17. Avni T, Leibovici L, Gafter-Gvili A. Iron supplementation for the treatment of chronic heart failure and iron deficiency: systematic review and meta-analysis. Eur J Heart Fail. 2012;14:423–429.
18. 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.
19. Camaschella C. Iron-deficiency anemia. N Engl J Med. 2015;372:1832–1843.
20. Weiss G, Goodnough LT. Anemia of chronic disease. N Engl J Med. 2005;352:1011–1023.
21. Weiss G. Anemia of chronic disorders: new diagnostic tools and new treatment strategies. Semin Hematol. 2015;52:313–320.
22. 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.
23. Himmelfarb J. Iron regulation. J Am Soc Nephrol. 2007;18:379–381.
24. Ganz T. Iron in innate immunity: starve the invaders. Curr Opin Immunol. 2009;21:63–67.
25. Cherayil BJ. The role of iron in the immune response to bacterial infection. Immunol Res. 2011;50:1–9.
26. Hentze MW, Muckenthaler MU, Andrews NC. Balancing acts: molecular control of mammalian iron metabolism. Cell. 2004;117:285–297.
27. Gasche C, Lomer MC, Cavill I, Weiss G. Iron, anaemia, and inflammatory bowel diseases. Gut. 2004;53:1190–1197.
28. Jankowska EA, von Haehling S, Anker SD, et al. Iron deficiency and heart failure: diagnostic dilemmas and therapeutic perspectives. Eur Heart J. 2013;34:816–829.
29. Tsagalis G. Renal anemia: a nephrologist's view. Hippokratia. 2011;15:39–43.
30. Maeder MT, Khammy O, dos Remedios C, Kaye DM. Myocardial and systemic iron depletion in heart failure implications for anemia accompanying heart failure. J Am Coll Cardiol. 2011;58:474–480.
31. World Health Organization. Iron deficiency anaemia. Assessment, prevention and control: a guide for programme managers. 2001. Available at: http://whqlibdoc.who.int/hq/2001/WHO_NHD_01.3.pdf.
32. Keating GM. Ferric carboxymaltose: a review of its use in iron deficiency. Drugs. 2015;75:101–127.
33. von Haehling S, Jankowska EA, van Veldhuisen DJ, et al. Iron deficiency and cardiovascular disease. Nat Rev Cardiol. 2015;12:659–669.
34. Pratt JJ, Khan KS. Non-anaemic iron deficiency—a disease looking for recognition of diagnosis: a systematic review. Eur J Haematol. 2016;96:618–628.
35. Koduru P, Abraham BP. The role of ferric carboxymaltose in the treatment of iron deficiency anemia in patients with gastrointestinal disease. Therap Adv Gastroenterol. 2016;9:76–85.
36. Goldberg ND. Iron deficiency anemia in patients with inflammatory bowel disease. Clin Exp Gastroenterol. 2013;6:61–70.
37. Borgna-Pignatti C, Zanella S. Pica as a manifestation of iron deficiency. Expert Rev Hematol. 2016;9:1075–1080.
38. Trenkwalder C, Allen R, Hogl B, et al. Restless legs syndrome associated with major diseases: a systematic review and new concept. Neurology. 2016;86:1336–1343.
39. McDonagh T, Macdougall IC. Iron therapy for the treatment of iron deficiency in chronic heart failure: intravenous or oral?. Eur J Heart Fail. 2015;17:248–262.
40. Brownlie T, Utermohlen V, Hinton PS, et al. Marginal iron deficiency without anemia impairs aerobic adaptation among previously untrained women. Am J Clin Nutr. 2002;75:734–742.
41. Haas JD, Brownlie T. Iron deficiency and reduced work capacity: a critical review of the research to determine a causal relationship. J Nutr. 2001;131:676S–688S.
42. Jankowska EA, Malyszko J, Ardehali H, et al. Iron status in patients with chronic heart failure. Eur Heart J. 2013;34:827–834.
43. Jankowska EA, Rozentryt P, Witkowska A, et al. Iron deficiency predicts impaired exercise capacity in patients with systolic chronic heart failure. J Card Fail. 2011;17:899–906.
44. Enjuanes C, Bruguera J, Grau M, et al. Iron status in chronic heart failure: impact on symptoms, functional class and submaximal exercise capacity. Rev Esp Cardiol (Engl Ed). 2016;69:247–255.
45. Anker SD, Comin CJ, Filippatos G, et al. Ferric carboxymaltose in patients with heart failure and iron deficiency. N Engl J Med. 2009;361:2436–2448.
46. Ponikowski P, van Veldhuisen DJ, Comin-Colet J, et al. Beneficial effects of long-term intravenous iron therapy with ferric carboxymaltose in patients with symptomatic heart failure and iron deficiencydagger. Eur Heart J. 2015;36:657–658.
47. van Veldhuisen DJ, Ponikowski P, Metra M, et al. Effect of Ferric Carboxymaltose on Exercise Capacity in Patients with Iron Deficiency and Chronic Heart Failure (EFFECT-HF): a Randomized, Controlled Study (NCT01394562). New Orleans, LA, USA: American Heart Association 2016 Scientific Sessions; 2016.
48. Ponikowski P, van Veldhuisen DJ, Comin-Colet J, et al. Rationale and design of the CONFIRM-HF study: a double-blind, randomized, placebo-controlled study to assess the effects of intravenous ferric carboxymaltose on functional capacity in patients with chronic heart failure and iron deficiency. ESC Heart Failure. 2014;1:52–58.
49. Enjuanes C, Klip IT, Bruguera J, et al. Iron deficiency and health-related quality of life in chronic heart failure: results from a multicenter European study. Int J Cardiol. 2014;174:268–275.
50. Toblli JE, Lombrana A, Duarte P, Di Gennaro F. Intravenous iron reduces NT-pro-brain natriuretic peptide in anemic patients with chronic heart failure and renal insufficiency. J Am Coll Cardiol. 2007;50:1657–1665.
51. Filippatos G, Farmakis D, Colet JC, et al. Intravenous ferric carboxymaltose in iron-deficient chronic heart failure patients with and without anaemia: a subanalysis of the FAIR-HF trial. Eur J Heart Fail. 2013;15:1267–1276.
52. Jankowska EA, Tkaczyszyn M, Suchocki T, et al. Effects of intravenous iron therapy in iron-deficient patients with systolic heart failure: a meta-analysis of randomized controlled trials. Eur J Heart Fail. 2016;18:786–795.
53. Horl WH. Non-erythropoietin-based anaemia management in chronic kidney disease. Nephrol Dial Transplant. 2002;17(Suppl 11):35–38.
54. Wish JB. Assessing iron status: beyond serum ferritin and transferrin saturation. Clin J Am Soc Nephrol. 2006;1(Suppl 1):S4–S8.
55. Leaf DE, Goldfarb DS. Interpretation and review of health-related quality of life data in CKD patients receiving treatment for anemia. Kidney Int. 2009;75:15–24.
56. Drueke TB, Locatelli F, Clyne N, et al. Normalization of hemoglobin level in patients with chronic kidney disease and anemia. N Engl J Med. 2006;355:2071–2084.
57. Dowling TC. Prevalence, etiology, and consequences of anemia and clinical and economic benefits of anemia correction in patients with chronic kidney disease: an overview. Am J Health Syst Pharm. 2007;64:S3–S7.
58. Finkelstein FO, Story K, Firanek C, et al. Health-related quality of life and hemoglobin levels in chronic kidney disease patients. Clin J Am Soc Nephrol. 2009;4:33–38.
59. Kovesdy CP, Trivedi BK, Kalantar-Zadeh K, Anderson JE. Association of anemia with outcomes in men with moderate and severe chronic kidney disease. Kidney Int. 2006;69:560–564.
60. Singh AK, Szczech L, Tang KL, et al. Correction of anemia with epoetin alfa in chronic kidney disease. N Engl J Med. 2006;355:2085–2098.
61. Keith DS, Nichols GA, Gullion CM, et al. Longitudinal follow-up and outcomes among a population with chronic kidney disease in a large managed care organization. Arch Intern Med. 2004;164:659–663.
62. Pfeffer MA, Burdmann EA, Chen CY, et al. A trial of darbepoetin alfa in type 2 diabetes and chronic kidney disease. N Engl J Med. 2009;361:2019–2032.
63. Thorp ML, Johnson ES, Yang X, et al. Effect of anaemia on mortality, cardiovascular hospitalizations and end-stage renal disease among patients with chronic kidney disease. Nephrology (Carlton). 2009;14:240–246.
64. Guagnozzi D, Lucendo AJ. Anemia in inflammatory bowel disease: a neglected issue with relevant effects. World J Gastroenterol. 2014;20:3542–3551.
65. Ott C, Liebold A, Takses A, et al. High prevalence but insufficient treatment of iron-deficiency anemia in patients with inflammatory bowel disease: results of a population-based cohort. Gastroenterol Res Pract. 2012;2012:595970.
66. Jelsness-Jorgensen LP, Bernklev T, Henriksen M, et al. Chronic fatigue is more prevalent in patients with inflammatory bowel disease than in healthy controls. Inflamm Bowel Dis. 2011;17:1564–1572.
67. Wells CW, Lewis S, Barton JR, Corbett S. 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.
68. 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.
69. KDIGO Clinical Practice Guideline for Anemia in Chronic Kidney Disease. Kidney Int. 2012;2:279–335.
70. NICE. Anaemia management in people with chronic kidney disease. 2015. Available at: www.nice.org.uk/guidance/ng8.
71. Ponikowski P, Voors AA, Anker SD, et al. 2016 ESC guidelines for the diagnosis and treatment of acute and chronic heart failure: the Task Force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC). Developed with the special contribution of the Heart Failure Association (HFA) of the ESC. Eur Heart J. 2016;37:2129–2200.
72. Cohen-Solal A, Leclercq C, Mebazaa A, et al. Diagnosis and treatment of iron deficiency in patients with heart failure: expert position paper from French cardiologists. Arch Cardiovasc Dis. 2014;107:563–571.
73. Gasche C, Berstad A, Befrits R, et al. Guidelines on the diagnosis and management of iron deficiency and anemia in inflammatory bowel diseases. Inflamm Bowel Dis. 2007;13:1545–1553.
74. Yancy CW, Jessup M, Bozkurt B, et al. 2017 ACC/AHA/HFSA focused update of the 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology/American Heart association task force on clinical practice guidelines and the heart failure society of America. J Card Fail. 2017. doi: 10.1016/j.cardfail.2017.04.014. [Epub ahead of print]
75. National Clinical Guideline Centre (NCGC). Anaemia management in chronic kidney disease. NG8 (update). Commissioned by the National Institute for Health and Care Excellence. 2015. Available at: https://www.nice.org.uk/guidance/ng8/evidence/full-guideline-70545133.
76. Mikhail A, Shrivastava R, Richardson D. Clinical Practice Guidelines: Anemia of CKD. 5th ed., 2009–2012. UK: Renal Association; 2012.
77. Magro F, Ramos J, Correia L, et al. Portuguese consensus on the diagnosis, prevention and treatment of anemia in inflammatory bowel disease. Acta Med Port. 2016;29:144–156.
78. Goddard AF, James MW, McIntyre AS, Scott BB. Guidelines for the management of iron deficiency anaemia. Gut. 2011;60:1309–1316.
79. Levin A, Hemmelgarn B, Culleton B, et al. Guidelines for the management of chronic kidney disease. CMAJ. 2008;179:1154–1162.
80. Kliger AS, Foley RN, Goldfarb DS, et al. KDOQI US commentary on the 2012 KDIGO clinical practice guideline for anemia in CKD. Am J Kidney Dis. 2013;62:849–859.
81. Locatelli F, Barany P, Covic A, 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.
82. Manito N, Cerqueiro JM, Comin-Colet J, et al. Consensus document of the Spanish Society of Cardiology and the Spanish Society of Internal Medicine on the diagnosis and treatment of iron deficiency in heart failure. Rev Clin Esp. 2017;217:35–45.
83. Macginley R, Walker R, Irving M. KHA-CARI guideline: use of iron in chronic kidney disease patients. Nephrology (Carlton). 2013;18:747–749.
84. Hasenfuss G, Anker S, Bauersachs J, et al. Kommentar zu den Leitlinien der Europäischen Gesellschaft für Kardiologie (ESC) zur Diagnostik und Behandlung der akuten und chronischen Herzinsuffizienz]. Kardiologe. 2013;7:105–114. [
85. Krum H, Jelinek MV, Stewart S, et al. 2011 update to National Heart Foundation of Australia and Cardiac Society of Australia and New Zealand Guidelines for the prevention, detection and management of chronic heart failure in Australia, 2006. Med J Aust. 2011;194:405–409.
86. Polin V, Coriat R, Perkins G, et al. Iron deficiency: from diagnosis to treatment. Dig Liver Dis. 2013;45:803–809.
87. Mowat C, Cole A, Windsor A, et al. Guidelines for the management of inflammatory bowel disease in adults. Gut. 2011;60:571–607.
88. Fraser IS, Langham S, Uhl-Hochgraeber K. Health-related quality of life and economic burden of abnormal uterine bleeding. Expert Rev Obstet Gynecol. 2009;4:179–189.
89. Fraser IS, Mansour D, Breymann C, et al. Prevalence of heavy menstrual bleeding and experiences of affected women in a European patient survey. Int J Gynaecol Obstet. 2015;128:196–200.
90. Brownlie T, Utermohlen V, Hinton PS, Haas JD. Tissue iron deficiency without anemia impairs adaptation in endurance capacity after aerobic training in previously untrained women. Am J Clin Nutr. 2004;79:437–443.
91. Bruner AB, Joffe A, Duggan AK, et al. Randomised study of cognitive effects of iron supplementation in non-anaemic iron-deficient adolescent girls. Lancet. 1996;348:992–996.
92. Liu Z, Doan QV, Blumenthal P, Dubois RW. A systematic review evaluating health-related quality of life, work impairment, and health-care costs and utilization in abnormal uterine bleeding. Value Health. 2007;10:183–194.
93. Verdon F, Burnand B, Stubi CL, et al. Iron supplementation for unexplained fatigue in non-anaemic women: double blind randomised placebo controlled trial. BMJ. 2003;326:1124.
94. World Health Organization. Worldwide prevalence of anaemia 1993–2005: WHO Global Database on Anaemia. 2008. Available at: http://apps.who.int/iris/bitstream/10665/43894/1/9789241596657_eng.pdf.
95. Corwin EJ, Murray-Kolb LE, Beard JL. Low hemoglobin level is a risk factor for postpartum depression. J Nutr. 2003;133:4139–4142.
96. Cantwell R, Clutton-Brock T, Cooper G, et al. Saving mothers' lives: reviewing maternal deaths to make motherhood safer: 2006–2008. The Eighth Report of the Confidential Enquiries into Maternal Deaths in the United Kingdom. BJOG. 2011;118(Suppl 1):1–203.
97. Scholl TO, Hediger ML, Fischer RL, Shearer JW. Anemia vs iron deficiency: increased risk of preterm delivery in a prospective study. Am J Clin Nutr. 1992;55:985–988.
98. Colomer J, Colomer C, Gutierrez D, et al. Anaemia during pregnancy as a risk factor for infant iron deficiency: report from the Valencia Infant Anaemia Cohort (VIAC) study. Paediatr Perinat Epidemiol. 1990;4:196–204.
99. Lozoff B, Jimenez E, Smith JB. Double burden of iron deficiency in infancy and low socioeconomic status: a longitudinal analysis of cognitive test scores to age 19 years. Arch Pediatr Adolesc Med. 2006;160:1108–1113.
100. Congdon EL, Westerlund A, Algarin CR, et al. Iron deficiency in infancy is associated with altered neural correlates of recognition memory at 10 years. J Pediatr. 2012;160:1027–1033.
101. Kamangar F, Dores GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. JCO. 2006;24:2137–2150.
102. Naoum FA. Iron deficiency in cancer patients. Rev Bras Hematol Hemoter. 2016;38:325–330.
103. Musallam KM, Tamim HM, Richards T, et al. Preoperative anaemia and postoperative outcomes in non-cardiac surgery: a retrospective cohort study. Lancet. 2011;378:1396–1407.
104. Munoz M, Acheson AG, Auerbach M, et al. International consensus statement on the peri-operative management of anaemia and iron deficiency. Anaesthesia. 2017;72:233–247.
105. National Institute for Health and Care Excellence. Blood transfusion: qs138. 2016. Available at: https://www.nice.org.uk/guidance/qs138.
106. Alleyne M, Horne MK, Miller JL. Individualized treatment for iron-deficiency anemia in adults. Am J Med. 2008;121:943–948.
107. Lyseng-Williamson KA, Keating GM. Ferric carboxymaltose: a review of its use in iron-deficiency anemia. Drugs. 2009;69:739–756.
108. Morris CC. Pediatric iron poisonings in the United States. South Med J. 2000;93:352–358.
109. Geisser P, Burckhardt S. The pharmacokinetics and pharmacodynamics of iron preparations. Pharmaceutics. 2011;3:12–33.
110. Aapro M, Osterborg A, Gascon P, et al. Anaemia and cancer: oral or intravenous iron? 2012. Available at: http://orbi.ulg.ac.be/bitstream/2268/153165/1/288.pdf.
111. Qunibi WY. The efficacy and safety of current intravenous iron preparations for the management of iron-deficiency anaemia: a review. Arzneimittelforschung. 2010;60:399–412.
112. Lewis GD, Anstrom KJ, McNulty S, et al. Oral Iron Repletion Effects on Oxygen UpTake in Heart Failure (IRONOUT HF). New Orleans, LA, USA: American Heart Association 2016 Scientific Sessions; 2016.
113. Qunibi WY, Martinez C, Smith M, et al. 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.
114. Lee T, Clavel T, Smirnov K, et al. Oral versus intravenous iron replacement therapy distinctly alters the gut microbiota and metabolome in patients with IBD. Gut. 2016;66:863–871
115. Breymann C, Milman N, Mezzacasa A, et al. Ferric carboxymaltose vs. oral iron in the treatment of pregnant women with iron deficiency anemia: an international, open-label, randomized controlled trial (FER-ASAP). J Perinat Med. 2017;45:443–453.
116. Mahey R, Kriplani A, Mogili KD, et al. Randomized controlled trial comparing ferric carboxymaltose and iron sucrose for treatment of iron deficiency anemia due to abnormal uterine bleeding. Int J Gynaecol Obstet. 2016;133:43–48.
117. Borstlap WA, Buskens CJ, Tytgat KM, et al. Multicentre randomized controlled trial comparing ferric(III)carboxymaltose infusion with oral iron supplementation in the treatment of preoperative anaemia in colorectal cancer patients. BMC Surg. 2015;15:78.