Clinical, biological, and skin histopathologic effects of ionic macrocyclic and nonionic linear gadolinium chelates in a rat model of nephrogenic systemic fibrosis

Investigative Radiology

Volumn 46, Issue 2, 2011, Pages 85-93

  Fretellier, Nathalie ^a   Idée, Jean Marc ^a   Guerret, Sylviane ^b   Hollenbeck, Claire ^a   Hartmann, Daniel ^c   González, Walter ^a   Robic, Caroline ^a   Port, Marc ^a   Corot, Claire ^a  

^a Laboratoire Guerbet   (France)

^b NOVOTEC   (France)

^c UNIVERSITÉ LYON 1   (France)

Author keywords

fibroblast growth factor 23; gadodiamide; gadolinium chelates; gadoterate; nephrogenic systemic fibrosis; renal impairment

Indexed keywords

COLLAGEN FIBER; FIBROBLAST GROWTH FACTOR 23; GADODIAMIDE; GADOTERATE MEGLUMINE; GADOTERIC ACID; IRON; TRANSFERRIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLLAGEN DEGRADATION; CONTROLLED STUDY; DERMIS; DISEASE SEVERITY; EPIDERMIS; FOLLOW UP; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; NEPHROGENIC SYSTEMIC FIBROSIS; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; SKIN ULCER;

EID: 78751634456     PISSN: 00209996     EISSN: 15360210     Source Type: Journal    
DOI: 10.1097/RLI.0b013e3181f54044     Document Type: Article

References (52)

1. Cowper SE, Boyer PJ. Nephrogenic systemic fibrosis: an update. Curr Rheumatol Rep. 2006;8:151-157.
2. Cowper SE. Nephrogenic systemic fibrosis: a review and exploration of the role of gadolinium. Adv Dermatol. 2007;23:131-154.
3. Weinreb JC, Abu-Alfa AK. Gadolinium-based contrast agents and nephro-genic systemic fibrosis: why did it happen and what have we learned? J Magn Reson Imaging. 2009;30:1236-1239.
4. Port M, Idée JM, Medina C, et al. Efficiency, thermodynamic and kinetic stability of marketed gadolinium chelates and their possible clinical consequences: a critical review. Biometals. 2008;21:469-490.
5. Thomsen HS. Nephrogenic systemic fibrosis: history and epidemiology. Radiol Clin North Am. 2009;47:827-831.
6. Broome DR. Nephrogenic systemic fibrosis associated with gadolinium based contrast agents: a summary of the medical literature reporting. Eur J Radiol. 2008;66:230-234.
7. Abujudeh HH, Kaewlai R, Kagan A, et al. Nephrogenic systemic fibrosis after gadopentetate dimeglumine exposure: case series of 36 patients. Radiology. 2009;253:81-89.
8. Wertman R, Altun E, Martin DR, et al. Risk of nephrogenic systemic fibrosis: evaluation of gadolinium chelate contrast agents at four American Universities. Radiology. 2008;248:799-806.
9. Hope TA, Herfkens RJ, Denianke KS, et al. Nephrogenic systemic fibrosis in patients with chronic kidney disease who received gadopentetate dimeglu-mine. Invest Radiol. 2009;44:135-139.
10. Idée JM, Port M, Medina C, et al. Possible involvement of gadolinium chelates in the pathophysiology of nephrogenic systemic fibrosis: a critical review. Toxicology. 2008;248:77-88.
11. Morcos SK. Nephrogenic systemic fibrosis following the administration of extracellular gadolinium-based contrast agents: is the stability of the contrast agent molecule an important factor in the pathogenesis of this condition? Br J Radiol. 2007;80:73-76.
12. Perazella MA. Tissue deposition of gadolinium and development of NSF: a convergence of factors. Semin Dial. 2008;21:150-154.
13. Newton B, Jiménez SA. Mechanism of NSF: new evidence challenging the prevailing theory. J Magn Reson Imaging. 2009;30:1277-1283.
14. Pietsch H, Lengsfeld P, Steger-Hartmann T, et al. Impact of renal impairment on long-term retention of gadolinium in the rodent skin following the administration of gadolinium-based contrast agents. Invest Radiol. 2009;44: 226-233.
15. Mahl A, Heining P, Ulrich P, et al. Comparison of clinical pathology parameters with two different blood sampling techniques in rats: retrobulbar plexus versus sublingual vein. Lab Anim. 2000;34:351-361.
16. Crissman JW, Goodman DG, Hildebrandt PK, et al. Best practices guideline: toxicologic histopathology. Toxicol Pathol. 2004;32:126-131.
17. Milliken GA. Analysis of repeated measures design. In: Berry DA, ed. Statistical Methodology in the Pharmaceutical Sciences. New York, NY: Dekker; 1990:83-116.
18. Grant D, Johnsen H, Juelsrud A, et al. Effects of gadolinium contrast agents in naïve and nephrectomised rats: relevance to nephrogenic systemic fibrosis. Acta Radiol. 2009;50:156-169.
19. Haylor J, Dencausse A, Vickers M, et al. Nephrogenic gadolinium distribution and skin cellularity following a single injection of gadodiamide in the rat. Invest Radiol. 2010;45:507-512.
20. Ersoy H, Rybicki FJ. Biochemical safety profiles of gadolinium-based extracellular contrast agents and nephrogenic systemic fibrosis. J Magn Reson Imaging. 2007;26:1190-1197.
21. US Food and Drugs Administration CfDEaR. Guidance for Industry. Estimating the maximum safe starting dose in initial clinical trials for therapeutics in adult healthy volunteers; 2005. Available at: www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/ ucm078932.pdf. Accessed May 19, 2010.
22. Bousquet JC, Saini S, Stark DD, et al. Gd-DOTA: characterization of a new paramagnetic complex. Radiology. 1988;166:693-698.
23. Idée JM, Port M, Dencausse A, et al. Involvement of gadolinium chelates in the mechanism of nephrogenic systemic fibrosis: an update. Radiol Clin North Am. 2009;47:855-869.
24. Sieber MA, Pietsch H, Walter J, et al. A preclinical study to investigate the development of nephrogenic systemic fibrosis: a possible role for gadolinium-based contrast media. Invest Radiol. 2008;43:65-75.
25. Harpur ES, Worah D, Hals PA, et al. Preclinical safety assessment and pharmacokinetics of gadodiamide injection, a new magnetic resonance imaging contrast agent. Invest Radiol. 1993;28:S28-S43.
26. Prasad AS. Clinical manifestations of zinc deficiency. Annu Rev Nutr. 1985;5:341-363.
27. Pietsch H, Pering C, Lengsfeld P, et al. Evaluating the role of zinc in the occurrence of fibrosis of the skin: a preclinical study. J Magn Reson Imaging. 2009;30:374-383.
28. Idée JM, Port M, Raynal I, et al. Clinical and biological consequences of transmetallation induced by contrast agents for magnetic resonance imaging: a review. Fundam Clin Pharmacol. 2006;20:563-576.
29. Sieber MA, Steger-Hartmann T, Lengsfeld P, et al. Gadolinium-based contrast agents and NSF: evidence from animal experience. J Magn Reson Imaging. 2009;30:1268-1276.
30. Steger-Hartmann T, Hofmeister R, Ernst R, et al. A review of preclinical safety data for Magnevist (gadopentetate dimeglumine) in the context of nephrogenic systemic fibrosis. Invest Radiol. 2010;45:520-528.
31. Stratta P, Canavese C, Aime S. Gadolinium-enhanced magnetic resonance imaging, renal failure and nephrogenic systemic fibrosis/nephrogenic fibros-ing dermopathy. Curr Med Chem. 2008;15:1229-1235.
32. Bhagavathula N, DaSilva M, Aslam MN, et al. Regulation of collagen turnover in human skin fibroblasts exposed to a gadolinium-based contrast agent. Invest Radiol. 2009;44:433-439.
33. Perone PA, Weber SL, DaSilva M, et al. Collagenolytic activity is suppressed in organ-cultured human skin exposed to a gadolinium-based MRI contrast agent. Invest Radiol. 2010;45:42-48.
34. Pohlers D, Brenmoehl J, Löffler I, et al. TGF-beta and fibrosis in different organs. Molecular pathway imprint. Biochim Biophys Acta. 2009;1792:746-756.
35. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol. 2008; 214:199-210.
36. Bucala R. Fibrocytes: discovery of a circulating connective tissue cell progenitor. In: Bucala R, ed. New Insights into Tissue Repair and Systemic Fibrosis. Hackensack, NJ: World Scientific; 2008:1-18.
37. Jiménez SA, Artlette CM, Sandorfi N, et al. Dialysis-associated systemic fibrosis (nephrogenic fibrosing dermopathy). Arthritis Rheum. 2004;50:2660-2666.
38. Steger-Hartmann T, Raschke M, Riefke B, et al. The involvement of pro-inflammatory cytokines in nephrogenic systemic fibrosis. A mechanistic hypothesis based on preclinical results from a rat model treated with gadodia-mide. Exp Toxicol Pathol. 2009;61:537-552.
39. Distler JHW, Akhmetshina A, Schett G, et al. Monocyte chemoattractant proteins in the pathogenesis of systemic fibrosis. Rheumatology. 2009;48:98-103.
40. Hasegawa M, Sato S, Takehara K. Augmented production of chemokines (monocytes chemotactic protein-1 (MCP-1), macrophage inflammatory pro-tein-1alpha (MIP-1alpha) and MIP-1beta) in patients with systemic fibrosis: MCP-1 and MIP-1alpha may be involved in the development of pulmonary fibrosis. Clin Exp Immunol. 1999;117:159-165.
41. Rovin BH, Rumancik M, Tan L, et al. Glomerular expression of monocyte chemoattractant protein-1 in experimental and human glomerulonephritis. Lab Invest. 1994;71:536-542.
42. Motekaitis RJ, Sun Y, Martell AE. New synthetic, selective, high-affinity ligands for effective trivalent metal ion binding and transport. Inorg Chim Acta. 1992;198-200:421-428.
43. Niendorf HP, Dinger JC, Haustein J, et al. Tolerance data of Gd-DTPA: a review. Eur J Radiol. 1991;13:15-20.
44. Muñoz M, Villar I, García-Erce JA. An update on iron physiology. World J Gastroenterol. 2009;15:4617-4626.
45. Wollanka H, Weidenmaier W, Giersig C. NSF after Gadovist exposure: a case report and hypothesis of NSF development. Nephrol Dial Transplant. 2009; 29:3882-3884.
46. Liu S, Quarles LD. How fibroblast growth factor 23 works. J Am Soc Nephrol. 2007;18:1637-1647.
47. Mizobuchi M, Ogata H, Hatamura I, et al. Up-regulation of Cbfa1 and Pit-1 in calcified artery of uraemic rats with severe hyperphosphataemia and secondary hyperparathyroidism. Nephrol Dial Transplant. 2006;21: 911-916.
48. Leiner T, Kucharczyk W. Special issue: nephrogenic systemic fibrosis. J Magn Reson Imaging. 2009;30:1233-1235.
49. Perazella MA. Current status of gadolinium toxicity in patients with kidney disease. Clin J Am Soc Nephrol. 2009;4:461-469.
50. Penfield JG, Reilly RF. Nephrogenic systemic fibrosis risk: is there a difference between gadolinium-based contrast agents? Semin Dial. 2008;21:129-134.
51. Sieber MA, Lengsfeld P, Frenzel T, et al. Preclinical investigation to compare different gadolinium-based contrast agents regarding their propensity to release gadolinium in vivo and to trigger nephrogenic systemic-like lesions. Eur Radiol. 2008;18:2164-2173.
52. Hope TA, High WA, LeBoit PE, et al. Nephrogenic systemic fibrosis in rats treated with erythropoietin and intravenous iron. Radiology. 2009;253:390-398.