Ferrous sulfate, but not iron polymaltose complex, aggravates local and systemic inflammation and oxidative stress in dextran sodium sulfate-induced colitis in rats

Drug Design, Development and Therapy

Volumn 9, Issue , 2015, Pages 2585-2597

  Toblli, Jorge E ^a   Cao, Gabriel ^a   Angerosa, Margarita ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Colonic tissue erosion; Inflammatory bowel disease; Oral iron treatment; Preclinical; Tolerability

Indexed keywords

ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; DEXTRAN SULFATE; FERRIC FERROCYANIDE; FERRITIN; FERROUS SULFATE; HEPCIDIN; INTERLEUKIN 6; IRON POLYMALTOSE; TUMOR NECROSIS FACTOR ALPHA; ANTIANEMIC AGENT; FERRIC ION; FERROUS ION;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BODY WEIGHT; CONTROLLED STUDY; DEXTRAN SODIUM SULFATE-INDUCED COLITIS; DISEASE EXACERBATION; FEMALE; INFLAMMATION; IRON DEFICIENCY; LIVER HISTOLOGY; MALE; NONHUMAN; OXIDATIVE STRESS; RAT; ANIMAL; CHEMICALLY INDUCED; COLITIS; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECTS; ORAL DRUG ADMINISTRATION; PATHOLOGY; SPRAGUE DAWLEY RAT;

ADMINISTRATION, ORAL; ANIMALS; COLITIS; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; FEMALE; FERRIC COMPOUNDS; FERROUS COMPOUNDS; HEMATINICS; INFLAMMATION; MALE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84929179175     PISSN: None     EISSN: 11778881     Source Type: Journal    
DOI: 10.2147/DDDT.S81863     Document Type: Article

References (64)

1. Bergamaschi G, Di Sabatino A, Albertini R, et al. Prevalence and pathogenesis of anemia in inflammatory bowel disease. Influence of anti-tumor necrosis factor-alpha treatment. Haematologica. 2010;95(2):199-205.
2. Gomollón F, Gisbert JP. Current management of iron deficiency anemia in inflammatory bowel diseases: A practical guide. Drugs. 2013;73(16):1761-1770.
3. Goodnough LT, Nemeth E, Ganz T. Detection, evaluation, and management of iron-restricted erythropoiesis. Blood. 2010;116(23):4754-4761.
4. Mowat C, Cole A, Windsor A, et al; IBD Section of the British Society of Gastroenterology. Guidelines for the management of inflammatory bowel disease in adults. Gut. 2011;60(5):571-607.
5. 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(12):1545-1553.
6. Evstatiev R, Gasche C. Diagnosis and management of anemia in IBD. Inflamm Bowel Dis Monit. 2011;11(4):152-159.
7. Stein J, Hartmann F, Dignass AU. Diagnosis and management of iron deficiency anemia in patients with IBD. Nat Rev Gastroenterol Hepatol. 2010;7(11):599-610.
8. Stein J, Dignass AU. Management of iron deficiency anemia in inflammatory bowel disease - a practical approach. Ann Gastroenterol. 2013;26(2):104-113.
9. Bronstein AC, Spyker DA, Cantilena LR, Green JL, Rumack BH, Giffin SL. 2008 Annual Report of the American Association of Poison Control Centers’ National Poison Data System (NPDS): 26th Annual Report. Clin Toxicol (Phila). 2009;47(10):911-1084.
10. Manoguerra AS, Erdman AR, Booze LL, et al. Iron ingestion: an evidence-based consensus guideline for out-of-hospital management. Clin Toxicol (Phila). 2005;43(6):553-570.
11. Tenenbein M, Littman C, Stimpson RE. Gastrointestinal pathology in adult iron overdose. J Toxicol Clin Toxicol. 1990;28(3):311-320.
12. Pestaner JP, Ishak KG, Mullick FG, Centeno JA. Ferrous sulfate toxicity: A review of autopsy findings. Biol Trace Elem Res. 1999;69(3):191-198.
13. Areia M, Gradiz R, Souto P, et al. Iron-induced esophageal ulceration. Endoscopy. 2007;39 Suppl 1:E326.
14. Patel JR, Sahota O, Kaye PV. Fatal esophageal perforation caused by oral iron. Scand J Gastroenterol. 2010;45(5):635-636.
15. Zhang X, Ouyang J, Wieczorek R, DeSoto F. Iron medication-induced gastric mucosal injury. Pathol Res Pract. 2009;205(8):579-581.
16. Kulnigg S, Gasche C. Systematic review: managing anaemia in Crohn’s disease. Aliment Pharmacol Ther. 2006;24(11-12):1507-1523.
17. Kawai M, Sumimoto S, Kasajima Y, Hamamoto T. A case of ulcerative colitis induced by oral ferrous sulfate. Acta Paediatr Jpn. 1992;34(4):476-478.
18. Erichsen K, Hausken T, Ulvik RJ, Svardal A, Berstad A, Berge RK. Ferrous fumarate deteriorated plasma antioxidant status in patients with Crohn disease. Scand J Gastroenterol. 2003;38(5):543-548.
19. Erichsen K, Ulvik RJ, Nysaeter G, et al. Oral ferrous fumarate or intravenous iron sucrose for patients with inflammatory bowel disease. Scand J Gastroenterol. 2005;40(9):1058-1065.
20. Dresow B, Petersen D, Fischer R, Nielsen P. Non-transferrin-bound iron in plasma following administration of oral iron drugs. Biometals. 2008;21(3):273-276.
21. Hutchinson C, Al-Ashgar W, Liu DY, Hider RC, Powell JJ, Geissler CA. Oral ferrous sulphate leads to a marked increase in pro-oxidant nontransferrin-bound iron. Eur J Clin Invest. 2004;34(11):782-784.
22. Schümann K, Kroll S, Romero-Abal ME, et al. Impact of oral iron challenges on circulating non-transferrin-bound iron in healthy Guatemalan males. Ann Nutr Metab. 2012;60(2):98-107.
23. Schümann K, Solomons NW, Romero-Abal ME, Orozco M, Weiss G, Marx J. 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(2):128-136.
24. Brissot P, Ropert M, Le Lan C, Loréal O. Non-transferrin bound iron: A key role in iron overload and iron toxicity. Biochim Biophys Acta. 2012;1820(3):403-410.
25. Koskenkorva-Frank TS, Weiss G, Koppenol WH, Burckhardt S. The complex interplay of iron metabolism, reactive oxygen species, and reactive nitrogen species: Insights into the potential of various iron therapies to induce oxidative and nitrosative stress. Free Radic Biol Med. 2013;65:1174-1194.
26. Lachili B, Hininger I, Faure H, et al. Increased lipid peroxidation in pregnant women after iron and vitamin C supplementation. Biol Trace Elem Res. 2001;83(2):103-110.
27. Schümann K, Kroll S, Weiss G, et al. Monitoring of hematological, inflammatory and oxidative reactions to acute oral iron exposure in human volunteers: preliminary screening for selection of potentially-responsive biomarkers. Toxicology. 2005;212(1):10-23.
28. King SM, Donangelo CM, Knutson MD, et al. Daily supplementation with iron increases lipid peroxidation in young women with low iron stores. Exp Biol Med (Maywood). 2008;233(6):701-707.
29. Tuomainen TP, Nyyssönen K, Porkkala-Sarataho E, et al. Oral supplementation with ferrous sulfate but not with non-ionic iron polymaltose complex increases the susceptibility of plasma lipoproteins to oxidation. Nutr Res. 1999;19(8):1121-1132.
30. Geisser P. Safety and efficacy of iron(III)-hydroxide polymaltose complex/a review of over 25 years experience. Arzneimittelforschung. 2007;57(6A):439-452.
31. Geisser P. Iron therapy, oxidative stress and immunology. In: Chandra RK, editor. Nutrition and Immunology in the 21st Century. Guragon, India: TSAR Health; 2004:54-65.
32. Toblli JE, Brignoli R. Iron(III)-hydroxide polymaltose complex in iron deficiency anemia/review and meta-analysis. Arzneimittelforschung. 2007;57(6A):431-438.
33. Erichsen K, Ulvik RJ, Grimstad T, Berstad A, Berge RK, Hausken T. 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(9):831-838.
34. Gasche C, Evstatiev R, Haas T, et al. [Diagnosis and treatment of iron deficiency and anaemia in inflammatory bowel diseases. Consensus of the Austrian IBD Working Party]. Z Gastroenterol. 2011;49(5):627-632. German.
35. Kulnigg S, Teischinger L, Dejaco C, Waldhör T, Gasche C. Rapid recurrence of IBD-associated anemia and iron deficiency after intravenous iron sucrose and erythropoietin treatment. Am J Gastroenterol. 2009;104(6):1460-1467.
36. Toblli JE, Cao G, Olivieri L, Angerosa M. Comparative study of gastrointestinal tract and liver toxicity of ferrous sulfate, iron amino chelate and iron polymaltose complex in normal rats. Pharmacology. 2008;82(2):127-137.
37. Toblli JE, Cao G, Oliveri L, Angerosa M. Effects of iron polymaltose complex, ferrous fumarate and ferrous sulfate treatments in anemic pregnant rats, their fetuses and placentas. Inflamm Allergy Drug Targets. 2013;12(3):190-198.
38. Chassaing B, Koren O, Carvalho FA, Ley RE, Gewirtz AT. AIEC pathobiont instigates chronic colitis in susceptible hosts by altering microbiota composition. Gut. 2014;63(7):1069-1080.
39. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990;98(3):694-702.
40. Carrier J, Aghdassi E, Platt I, Cullen J, Allard JP. Effect of oral iron supplementation on oxidative stress and colonic inflammation in rats with induced colitis. Aliment Pharmacol Ther. 2001;15(12):1989-1999.
41. Erichsen K, Milde AM, Arslan G, et al. Low-dose oral ferrous fumarate aggravated intestinal inflammation in rats with DSS-induced colitis. Inflamm Bowel Dis. 2005;11(8):744-748.
42. Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Institute for Laboratory Animal Research. Division on Earth and Life Studies. National Research Council. Guide for the Care and use of Laboratory Animals. 8th ed. Washington, DC: The National Academies Press, 2011.
43. Perls M. Nachweis von Eisenoxyd in gewissen Pigmenten. Virchows Arch Pathol Anat. 1867;39:42-48. German.
44. Cook HC. Manual of Histological Demonstration Techniques. London, UK: The Butterworth Group; 1974.
45. Murthy SN, Cooper HS, Shim H, Shah RS, Ibrahim SA, Sedergran DJ. Treatment of dextran sulfate sodium-induced murine colitis by intracolonic cyclosporin. Dig Dis Sci. 1993;38(9):1722-1734.
46. Onderdonk AB, Bartlett JG. Bacteriological studies of experimental ulcerative colitis. Am J Clin Nutr. 1979;32(1):258-265.
47. Toblli JE, Cao G, Angerosa M. Comparison of early gastrointestinal tract and liver toxicity of the originator iron polymaltose complex (IPC) and an IPC similar preparation in non-anemic rats. Int J Clin Pharmacol Ther. 2012;50(8):573-583.
48. Giani JF, Gironacci MM, Muñoz MC, Peña C, Turyn D, Dominici FP. Angiotensin-(17) stimulates the phosphorylation of JAK2, IRS-1 and Akt in rat heart in vivo: Role of the AT1 and Mas receptors. Am J Physiol Heart Circ Physiol. 2007;293(2):H1154-H1163.
49. Akerboom TP, Sies H. Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Methods Enzymol. 1981;77:373-382.
50. Owen JB, Butterfield DA. Measurement of oxidized/reduced glutathione ratio. Methods Mol Biol. 2010;648:269-277.
51. Rossi R, Cardaioli E, Scaloni A, Amiconi G, Di Simplicio P. Thiol groups in proteins as endogenous reductants to determine glutathione-protein mixed disulphides in biological systems. Biochim Biophys Acta. 1995;1243(2):230-238.
52. Toblli JE, Cao G, Olivieri L, Angerosa M. Comparison of the renal, cardiovascular and hepatic toxicity data of original intravenous iron compounds. Nephrol Dial Transplant. 2010;25(11):3631-3640.
53. Carrier J, Aghdassi E, Cullen J, Allard JP. Iron supplementation increases disease activity and vitamin E ameliorates the effect in rats with dextran sulfate sodium-induced colitis. J Nutr. 2002;132(10):3146-3150.
54. Seril DN, Liao J, Ho KL, Warsi A, Yang CS, Yang GY. Dietary iron supplementation enhances DSS-induced colitis and associated colorectal carcinoma development in mice. Dig Dis Sci. 2002;47(6):1266-1278.
55. Dothel G, Vasina V, Barbara G, De Ponti F. Animal models of chemically induced intestinal inflammation: Predictivity and ethical issues. Pharmacol Ther. 2013;139(1):71-86.
56. Gotardo ÉM, Ribeiro Gde A, Clemente TR, et al. Hepcidin expression in colon during trinitrobenzene sulfonic acid-induced colitis in rats. World J Gastroenterol. 2014;20(15):4345-4352.
57. Bergamaschi G, Di Sabatino A, Albertini R, et al. Serum hepcidin in inflammatory bowel diseases: Biological and clinical significance. Inflamm Bowel Dis. 2013;19(10):2166-2172.
58. Dudkowiak R, Neubauer K, Poniewierka E. Hepcidin and its role in inflammatory bowel disease. Adv Clin Exp Med. 2013;22(4):585-591.
59. Mecklenburg I, Reznik D, Fasler-Kan E, Drewe J, Beglinger C, Hruz P; Swiss IBD Cohort Study Group. Serum hepcidin concentrations correlate with ferritin in patients with inflammatory bowel disease. J Crohns Colitis. 2014;8(11):1392-1397.
60. Oustamanolakis P, Koutroubakis IE, Messaritakis I, Malliaraki N, Sfiridaki A, Kouroumalis EA. Serum hepcidin and prohepcidin concentrations in inflammatory bowel disease. Eur J Gastroenterol Hepatol. 2011;23(3):262-268.
61. Oustamanolakis P, Koutroubakis IE, Kouroumalis EA. Diagnosing anemia in inflammatory bowel disease: beyond the established markers. J Crohns Colitis. 2011;5(5):381-391.
62. Sukumaran A, James J, Janardhan HP, et al. Expression of iron-related proteins in the duodenum is up-regulated in patients with chronic inflammatory disorders. Br J Nutr. 2014;111(6):1059-1068.
63. Mitsuyama K, Sata M, Rose-John S. Interleukin-6 trans-signaling in inflammatory bowel disease. Cytokine Growth Factor Rev. 2006;17(6):451-461.
64. Geisser P, Burckhardt S. The pharmacokinetics and pharmacodynamics of iron preparations. Pharmaceutics. 2011;3(1):12-33.