Gadolinium-containing magnetic resonance contrast media: Investigation on the possible transchelation of Gd3+ to the glycosaminoglycan heparin

Contrast Media and Molecular Imaging

Volumn 8, Issue 2, 2013, Pages 108-116

  Taupitz, Matthias ^a   Stolzenburg, Nicola ^a   Ebert, Monika ^a   Schnorr, Jörg ^a   Hauptmann, Ralf ^a   Kratz, Harald ^a   Hamm, Bernd ^a   Wagner, Susanne ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Complex stability; Contrast media; Gadolinium; Glycosaminoglycans; Magnetic resonance imaging; Nephrogenic systemic fibrosis; Transchelation; Transmetallation

Indexed keywords

CHONDROITIN SULFATE; GADOBENATE DIMEGLUMINE; GADOBUTROL; GADODIAMIDE; GADOFOSVESET; GADOLINIUM; GADOLINIUM PENTETATE MEGLUMINE; GADOTERATE MEGLUMINE; GADOTERIDOL; GADOVERSETAMIDE; GADOXETIC ACID; HEPARIN; ZINC CHLORIDE;

ARTICLE; CHELATION; CHEMICAL COMPOSITION; CONTROLLED STUDY; DRUG RETENTION; EXTRACELLULAR MATRIX; HUMAN; IN VITRO STUDY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; THERMODYNAMICS;

CHELATING AGENTS; CONTRAST MEDIA; GADOLINIUM; HEPARIN; MAGNETIC RESONANCE IMAGING;

EID: 84871664119     PISSN: 15554309     EISSN: 15554317     Source Type: Journal    
DOI: 10.1002/cmmi.1500     Document Type: Article

References (64)

1. Knopp MV, Balzer T, Esser M, Kashanian FK, Paul P, Niendorf HP. Assessment of utilization and pharmacovigilance based on spontaneous adverse event reporting of gadopentetate dimeglumine as a magnetic resonance contrast agent after 45 million administrations and 15years of clinical use. Invest Radiol 2006; 41: 491-499. DOI: 10.1097/01.rli.0000209657.16115.42
2. Kirchin MA, Pirovano G, Venetianer C, Spinazzi A. Safety assessment of gadobenate dimeglumine (MultiHance): extended clinical experience from phase I studies to post-marketing surveillance. J Magn Reson Imag 2001; 14: 281-294.
3. Aslanian V, Lemaignen H, Bunouf P, Svaland MG, Borseth A, Lundby B. Evaluation of the clinical safety of gadodiamide injection, a new nonionic MRI contrast medium for the central nervous system: a European perspective. Neuroradiology 1996; 38: 537-541.
4. Brown JJ, Kristy RM, Stevens GR, Pierro JA. The OptiMARK clinical development program: summary of safety data. J Magn Reson Imag 2002; 15: 446-455.
5. Raman SS, Leary C, Bluemke DA, Amendola M, Sahani D, McTavish JD, Brody J, Outwater E, Mitchell D, Sheafor DH, Fidler J, Francis IR, Semelka RC, Shamsi K, Gschwend S, Feldman DR, Breuer J, United States EOB Study Group. Improved characterization of focal liver lesions with liver-specific gadoxetic acid disodium-enhanced magnetic resonance imaging: a multicenter phase 3 clinical trial. J Comput Assist Tomogr 2010; 34: 163-172. DOI: 10.1097/RCT.0b013e3181c89d87
6. Shamsi K, Yucel EK, Chamberlin P. A summary of safety of gadofosveset (MS-325) at 0.03mmol/kg body weight dose: Phase II and Phase III clinical trials data. Invest Radiol 2006; 41: 822-830. DOI: 10.1097/01.rli.0000242836.25299.8f
7. Herborn CU, Honold E, Wolf M, Kemper J, Kinner S, Adam G, Barkhausen J. Clinical safety and diagnostic value of the gadolinium chelate gadoterate meglumine (Gd-DOTA). Invest Radiol 2007; 42: 58-62. DOI: 10.1097/01.rli.0000248893.01067.e5
8. Hammerstingl R, Adam G, Ayuso JR, Van Beers B, Belfiore G, Bellin MF, Bongartz G, Ernst O, Frericks B, Giuseppetti G, Heinz-Peer G, Laghi A, Martin J, Pering C, Reimer P, Richter GM, Roemer FW, Schäfer FK, Vilgrain V, Vogl TJ, Weishaupt D, Wall A, Zech CJ, Tombach B. Comparison of 1.0M gadobutrol and 0.5M gadopentetate dimeglumine-enhanced magnetic resonance imaging in five hundred seventy-two patients with known or suspected liver lesions: results of a multicenter, double-blind, interindividual, randomized clinical phase-III trial. Invest Radiol 2009; 44: 168-176. DOI: 10.1097/RLI.0b013e318198a0ae
9. Runge VM, Parker JR. Worldwide clinical safety assessment of gadoteridol injection: an update. Eur Radiol 1997; 7(suppl 5): 243-245.
10. Cowper SE, Robin HS, Steinberg SM, Su LD, Gupta S, LeBoit PE. Scleromyxoedema-like cutaneous diseases in renal-dialysis patients. Lancet 2000; 356: 1000-1001; DOI: 10.1016/S0140-6736(00)02694-5
11. Neudecker BA, Stern R, Mark LA, Steinberg S. Scleromyxedema-like lesions of patients in renal failure contain hyaluronan: a possible pathophysiological mechanism. J Cutan Pathol 2005; 32: 612-615. DOI: 10.1111/j.0303-6987.2005.00415.x
12. Grobner T. Gadolinium - a specific trigger for the development of nephrogenic fibrosing dermopathy and nephrogenic systemic fibrosis? Nephrol Dial Transplant 2006; 21: 1104-1108. DOI: 10.1093/ndt/gfk062
13. Jamboti J. Strong association between the use of gadolinium-based contrast agents with nephrogenic fibrosing dermopathy/nephrogenic systemic fibrosis. Intern Med J 2007; 37: 508-509. DOI: 10.1111/j.1445-5994.2007.01413.x
14. Idée JM, Port M, Robic C, Medina C, Sabatou M, Corot C. Role of thermodynamic and kinetic parameters in gadolinium chelate stability. J Magn Reson Imag 2009; 30: 1249-1258. DOI: 10.1002/jmri.21967
15. Frenzel T, Lengsfeld P, Schirmer H, Hütter J, Weinmann HJ. Stability of gadolinium-based magnetic resonance imaging contrast agents in human serum at 37 degrees C. Invest Radiol 2008; 43: 817-828. DOI: 10.1097/RLI.0b013e3181852171
16. Sieber MA, Lengsfeld P, Frenzel T, Golfier S, Schmitt-Willich H, Siegmund F, Walter J, Weinmann HJ, Pietsch H. Preclinical investigation to compare different gadolinium-based contrast agents regarding their propensity to release gadolinium in vivo and to trigger nephrogenic systemic fibrosis-like lesions. Eur Radiol 2008; 18: 2164-2173. DOI: 10.1007/s00330-008-0977-y
17. Sieber MA, Pietsch H, Walter J, Haider W, Frenzel T, Weinmann HJ. 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. DOI: 10.1097/RLI.0b013e31815e6277
18. Pietsch H, Lengsfeld P, Jost G, Frenzel T, Hütter J, Sieber MA. Long-term retention of gadolinium in the skin of rodents following the administration of gadolinium-based contrast agents. Eur Radiol 2009. DOI: 10.1007/s00330-008-1259-4
19. Pietsch H, Pering C, Lengsfeld P, Walter J, Steger-Hartmann T, Golfier S, Frenzel T, Hütter J, Weinmann HJ, Sieber MA. Evaluating the role of zinc in the occurrence of fibrosis of the skin: a preclinical study. J Magn Reson Imag 2009; 30: 374-383. DOI: 10.1002/jmri.21845
20. Sieber MA, Steger-Hartmann T, Lengsfeld P, Pietsch H. Gadolinium-based contrast agents and NSF: evidence from animal experience. J Magn Reson Imag 2009; 30: 1268-1276. DOI: 10.1002/jmri.21971
21. Abujudeh HH, Kaewlai R, Kagan A, Chibnik LB, Nazarian RM, High WA, Kay J. Nephrogenic systemic fibrosis after gadopentetate dimeglumine exposure: case series of 36 patients. Radiology 2009; 253: 81-89. DOI: 10.1148/radiol.2531082160
22. George SJ, Webb SM, Abraham JL, Cramer SP. Synchrotron X-ray analyses demonstrate phosphate-bound gadolinium in skin in nephrogenic systemic fibrosis. Br J Dermatol 2010; 163: 1077-1081. DOI: 10.1111/j.1365-2133.2010.09918.x
23. High WA, Ranville JF, Brown M, Punshon T, Lanzirotti A, Jackson BP. Gadolinium deposition in nephrogenic systemic fibrosis: an examination of tissue using synchrotron x-ray fluorescence spectroscopy. J Am Acad Dermatol 2010; 62: 38-44. DOI: 10.1016/j.jaad.2009.07.018
24. Christensen KN, Lee CU, Hanley MM, Leung N, Moyer TP, Pittelkow MR. Quantification of gadolinium in fresh skin and serum samples from patients with nephrogenic systemic fibrosis. J Am Acad Dermatol 2011; 64: 91-96. DOI: 10.1016/j.jaad.2009.12.044
25. Thakral C, Abraham JL. Gadolinium-induced nephrogenic systemic fibrosis is associated with insoluble Gd deposits in tissues: in vivo transmetallation confirmed by microanalysis. J Cutan Pathol 2009; 36: 1244-1254. DOI: 10.1111/j.1600-0560.2009.01283.x
26. Cowper SE. Nephrogenic Fibrosing Dermopathy [ICNSFR Website], 2001-2009. Available from: http://www.icnsfr.org (accessed 5 May2012).
27. Wang Y, Alkasab TK, Narin O, Nazarian RM, Kaewlai R, Kay J, Abujudeh HH. Incidence of nephrogenic systemic fibrosis after adoption of restrictive gadolinium-based contrast agent guidelines. Radiology 2011; 260: 105-111. DOI: 10.1148/radiol.11102340
28. US Food and Drug Administration. FDA Drug Safety Communication: New Warnings for Using Gadolinium-based Contrast Agents in Patients with Kidney Dysfunction. Available from: http://www.fda.gov/Drugs/DrugSafety/ucm223966.htm (accessed 5 May 2012).
29. European Medicines Agency. European Medicines Agency makes Recommendations to Minimise Risk of Nephrogenic Systemic Fibrosis with Gadolinium-containing Contrast Agents. Available from: http://www.esur.org/fileadmin/News/EMEA_091120_1.pdf (accessed 5 May 2012).
30. Gupta A, Shamseddin MK, Khaira A. Pathomechanisms of nephrogenic systemic fibrosis: new insights. Clin Exp Dermatol 2011; 36: 763-768. DOI: 10.1111/j.1365-2230.2011.04136.x
31. Kasokat T, Urich K. Quantification of dechelation of gadopentetate dimeglumine in rats. Arzneimittelforschung 1992; 42: 869-876.
32. 2+: a kinetic model for the prediction of the in vivo stability of [Gd(DTPA)]2-, used as a contrast agent in magnetic resonance imaging. Chemistry 2000; 6: 719-724.
33. Puttagunta NR, Gibby WA, Puttagunta VL. Comparative transmetallation kinetics and thermodynamic stability of gadolinium-DTPA bis-glucosamide and other magnetic resonance imaging contrast media. Invest Radiol 1996; 31: 619-624.
34. Puttagunta NR, Gibby WA, Smith GT. Human in vivo comparative study of zinc and copper transmetallation after administration of magnetic resonance imaging contrast agents. Invest Radiol 1996; 31: 739-742.
35. Laurent S, Elst LV, Copoix F, Muller RN. Stability of MRI paramagnetic contrast media: a proton relaxometric protocol for transmetallation assessment. Invest Radiol 2001; 36: 115-122.
36. Laurent S, Elst LV, Muller RN. Comparative study of the physicochemical properties of six clinical low molecular weight gadolinium contrast agents. Contrast Media Mol Imag 2006; 1: 128-137. DOI: 10.1002/cmmi.100
37. Laurent S, Vander Elst L, Henoumont C, Muller RN. How to measure the transmetallation of a gadolinium complex. Contrast Media Mol Imag 2010. DOI: 10.1002/cmmi.388
38. Robic C, Caroline R, Catoen S, Sarah C, De Goltstein MC, De Marie-Christine G, Idée JM, Jean-Marc I, Port M, Marc P. The role of phosphate on Omniscan(®) dechelation: an in vitro relaxivity study at pH 7. Biometals 2011; 24: 759-768. DOI: 10.1007/s10534-011-9422-9
39. Aime S, Caravan P. Biodistribution of gadolinium-based contrast agents, including gadolinium deposition. J Magn Reson Imag 2009; 30: 1259-1267. DOI: 10.1002/jmri.21969
40. Ando A, Ando I, Hiraki T, Takeshita M, Hisada K. Mechanism of tumor and liver concentration of 111 In and 169 Yb: 111 In and 169 Yb binding substances in tumor tissues and liver. Eur J Nucl Med Mol Imag 1982; 7: 298-303.
41. Doganges PT, Schubert M. The use of lanthanum to study the degradation of a proteinpolysaccharide from cartilage. J Biol Chem 1964; 239: 1498-1503.
42. Mason RM, Mayes RW. Solubilization of cartilage protein-polysaccharide with lanthanum chloride. Biochem J 1972; 128: 120P.
43. Vercruysse KP, Li H, Luo Y, Prestwich GD. Thermosensitive lanthanide complexes of hyaluronan. Biomacromolecules 2002; 3: 639-643.
44. Hällgren R, Engström-Laurent A, Nisbeth U. Circulating hyaluronate. A potential marker of altered metabolism of the connective tissue in uremia. Nephron 1987; 46: 150-154.
45. Friman C, Storgårds E, Juvani M, Kock B. The glycosaminoglycans (mucopolysaccharides) in plasma in patients with renal insufficiency. Clin Nephrol 1977; 8: 435.
46. Dong Q, Hurst DR, Weinmann HJ, Chenevert TL, Londy FJ, Prince MR. Magnetic resonance angiography with gadomer-17. An animal study original investigation. Invest Radiol 1998; 33: 699-708.
47. Ogan MD, Schmiedl U, Moseley ME, Grodd W, Paajanen H, Brasch RC. Albumin labeled with Gd-DTPA. An intravascular contrast-enhancing agent for magnetic resonance blood pool imaging: preparation and characterization. Invest Radiol 1987; 22: 665-671.
48. McBean LD, Dove JT, Halsted JA, Smith Jr JC. Zinc concentration in human tissues. Am J Clin Nutr 1972; 25: 672-676.
49. Parr RM, Taylor DM. The concentrations of cobalt, copper, iron and zinc in some normal human tissues as determined by neutron-activation analysis. Biochem J 1964; 91: 424-431.
50. Wang SC, Wikström MG, White DL, Klaveness J, Holtz E, Rongved P, Moseley ME, Brasch RC. Evaluation of Gd-DTPA-labeled dextran as an intravascular MR contrast agent: imaging characteristics in normal rat tissues. Radiology 1990; 175: 483-488.
51. Langereis S, Kooistra HA, van Genderen MH, Meijer EW. Probing the interaction of the biotin-avidin complex with the relaxivity of biotinylated Gd-DTPA. Org Biomol Chem 2004; 2: 1271-1273. DOI: 10.1039/b402917h
52. Mitra AK, Arnott S, Atkins ED, Isaac DH. Dermatan sulfate: molecular conformations and interactions in the condensed state. J Mol Biol 1983; 169: 873-901.
53. Scott JE. Supramolecular organization of extracellular matrix glycosaminoglycans, in vitro and in the tissues. FASEB J 1992; 6: 2639-2645.
54. Woodrow G, Turney JH, Davison AM, Cooper EH. Serum hyaluronan concentrations predict survival in patients with chronic renal failure on maintenance haemodialysis. Nephrol Dial Transplant 1996; 11: 98-100.
55. Gillis A, Gray M, Burstein D. Relaxivity and diffusion of gadolinium agents in cartilage. Magn Reson Med 2002; 48: 1068-1071. DOI: 10.1002/mrm.10327
56. Kimura J, Ishiguchi T, Matsuda J, Ohno R, Nakamura A, Kamei S, Ohno K, Kawamura T, Murata K. Human comparative study of zinc and copper excretion via urine after administration of magnetic resonance imaging contrast agents. Radiat Med 2005; 23: 322-326.
57. Port M, Idée JM, Medina C, Robic C, Sabatou M, Corot C. Efficiency, thermodynamic and kinetic stability of marketed gadolinium chelates and their possible clinical consequences: a critical review. Biometals 2008; 21: 469-490. DOI: 10.1007/s10534-008-9135-x
58. Kanamalla US, Boyko OB. Gadolinium diffusion into orbital vitreous and aqueous humor, perivascular space, and ventricles in patients with chronic renal disease. Am J Roentgenol 2002; 179: 1350-1352.
59. Laurent UB, Granath KA. The molecular weight of hyaluronate in the aqueous humour and vitreous body of rabbit and cattle eyes. Exp Eye Res 1983; 36: 481-492.
60. Taylor KR, Gallo RL. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J 2006; 20: 9-22. DOI: 10.1096/fj.05-4682rev
61. Rohrer M, Bauer H, Mintorovitch J, Requardt M, Weinmann HJ. Comparison of magnetic properties of MRI contrast media solutions at different magnetic field strengths. Invest Radiol 2005; 40: 715-724.
62. Pavone P, Patrizio G, Buoni C, Tettamanti E, Passariello R, Musu C, Tirone P, Felder E. Comparison of Gd-BOPTA with Gd-DTPA in MR imaging of rat liver. Radiology 1990; 176: 61-64.
63. Weinmann HJ, Schuhmann-Giampieri G, Schmitt-Willich H, Vogler H, Frenzel T, Gries H. A new lipophilic gadolinium chelate as a tissue-specific contrast medium for MRI. Magn Reson Med 1991; 22: 233-237.
64. Parmelee DJ, Walovitch RC, Ouellet HS, Lauffer RB. Preclinical evaluation of the pharmacokinetics, biodistribution, and elimination of MS-325, a blood pool agent for magnetic resonance imaging. Invest Radiol 1997; 32: 741-747.