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Late/delayed gadolinium enhancement in MRI after intravenous administration of extracellular gadolinium-based contrast agents: is it worth waiting?

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Abstract

The acquisition of images minutes or even hours after intravenous extracellular gadolinium-based contrast agents (GBCA) administration (“Late/Delayed Gadolinium Enhancement” imaging; in this review, further termed LGE) has gained significant prominence in recent years in magnetic resonance imaging. The major limitation of LGE is the long examination time; thus, it becomes necessary to understand when it is worth waiting time after the intravenous injection of GBCA and which additional information comes from LGE. LGE can potentially be applied to various anatomical sites, such as heart, arterial vessels, lung, brain, abdomen, breast, and the musculoskeletal system, with different pathophysiological mechanisms. One of the most popular clinical applications of LGE regards the assessment of myocardial tissue thanks to its ability to highlight areas of acute myocardial damage and fibrotic tissues. Other frequently applied clinical contexts involve the study of the urinary tract with magnetic resonance urography and identifying pathological abdominal processes characterized by high fibrous stroma, such as biliary tract tumors, autoimmune pancreatitis, or intestinal fibrosis in Crohn’s disease. One of the current areas of heightened research interest revolves around the possibility of non-invasively studying the dynamics of neurofluids in the brain (the glymphatic system), the disruption of which could underlie many neurological disorders.

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Abbreviations

3D:

Three dimensional

AF:

Atrial fibrillation

BBB:

Blood–brain barrier

CNS:

Central nervous system

CSF:

Cerebrospinal fluid

dGEMRIC:

Delayed gadolinium enhanced magnetic resonance imaging

dGEMRIM:

Delayed gadolinium enhanced magnetic resonance imaging of the meniscus

ECG:

Electrocardiogram

FLAIR:

Fluid attenuated inversion recovery

FLASH:

Fast low angle shot

GAG:

Glycosaminoglycan

GBCA:

Gadolinium-based contrast agents

Gd-DTPA2− :

Gadolinium diethylene triaminepentaacetic acid

GRE:

Gradient-echo

HIV:

Human immunodeficiency virus

IR:

Inversion recovery

LGE:

Late gadolinium enhancement

MRI:

Magnetic resonance imaging

MRU:

Magnetic resonance urography

PVS:

Perivascular spaces

SE:

Spin-echo

TI:

Inversion time

References

  1. Mallio CA, Quattrocchi CC, Rovira À, Parizel PM (2020) Gadolinium deposition safety: seeking the patient’s perspective. AJNR Am J Neuroradiol 41:944–946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Parillo M, Mallio CA, Van der Molen AJ, Rovira À, Ramalho J, Ramalho M, Gianolio E, Karst U, Radbruch A, Stroomberg G, Clement O, Dekkers IA, Nederveen AJ, Quattrocchi CC, ESMRMB-GREC Working Group (2023) Skin toxicity after exposure to gadolinium-based contrast agents in normal renal function, using clinical approved doses: current status of preclinical and clinical studies. Invest Radiol 58:530–538

    Article  CAS  PubMed  Google Scholar 

  3. Parillo M, Sapienza M, Arpaia F, Magnani F, Mallio CA, D’Alessio P, Quattrocchi CC (2019) A structured survey on adverse events occurring within 24 hours after intravenous exposure to gadodiamide or gadoterate meglumine: a controlled prospective comparison study. Invest Radiol 54:191–197

    Article  CAS  PubMed  Google Scholar 

  4. Quattrocchi CC, Parillo M, Spani F, Landi D, Cola G, Dianzani C, Perrella E, Marfia GA, Mallio CA (2023) Skin thickening of the scalp and high signal intensity of dentate nucleus in multiple sclerosis: association with linear versus macrocyclic gadolinium-based contrast agents administration. Invest Radiol 58:223–230

    Article  CAS  PubMed  Google Scholar 

  5. der van Molen AJ, Quattrocchi CC, Mallio CA, Dekkers IA, European Society of Magnetic Resonance in Medicine, Biology Gadolinium Research, Educational Committee (ESMRMB-GREC) (2023) Ten years of gadolinium retention and deposition: ESMRMB-GREC looks backward and forward. Eur Radiol. https://doi.org/10.1007/s00330-023-10281-3

    Article  PubMed  PubMed Central  Google Scholar 

  6. European Medicines Agency. EMA’s final opinion confirms restrictions on use of linear gadolinium agents in body scans. https://www.ema.europa.eu/en/documents/referral/gadolinium-article-31-referral-emas-final-opinion-confirms-restrictions-use-linear-gadolinium-agents-body-scans_en.pdf-0. Accessed Sept 2023

  7. Parillo M, Mallio CA, Van der Molen AJ, Rovira À, Dekkers IA, Karst U, Stroomberg G, Clement O, Gianolio E, Nederveen AJ, Radbruch A, Quattrocchi CC, ESMRMB-GREC Working Group (2023) The role of gadolinium-based contrast agents in magnetic resonance imaging structured reporting and data systems (RADS). Magma N Y N. https://doi.org/10.1007/s10334-023-01113-y

    Article  Google Scholar 

  8. Aime S, Caravan P (2009) Biodistribution of gadolinium-based contrast agents, including gadolinium deposition. J Magn Reson Imaging JMRI 30:1259–1267

    Article  PubMed  Google Scholar 

  9. Xiao Y-D, Paudel R, Liu J, Ma C, Zhang Z-S, Zhou S-K (2016) MRI contrast agents: classification and application (Review). Int J Mol Med 38:1319–1326

    Article  CAS  PubMed  Google Scholar 

  10. Freeze WM, van der Thiel M, de Bresser J, Klijn CJM, van Etten ES, Jansen JFA, van der Weerd L, Jacobs HIL, Backes WH, van Veluw SJ (2020) CSF enhancement on post-contrast fluid-attenuated inversion recovery images; a systematic review. NeuroImage Clin 28:102456

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kramer CM, Barkhausen J, Bucciarelli-Ducci C, Flamm SD, Kim RJ, Nagel E (2020) Standardized cardiovascular magnetic resonance imaging (CMR) protocols: 2020 update. J Cardiovasc Magn Reson Off J Soc Cardiovasc Magn Reson 22:17

    Google Scholar 

  12. Mahrholdt H, Wagner A, Judd RM, Sechtem U (2002) Assessment of myocardial viability by cardiovascular magnetic resonance imaging. Eur Heart J 23:602–619

    Article  CAS  PubMed  Google Scholar 

  13. Holtackers RJ, Emrich T, Botnar RM, Kooi ME, Wildberger JE, Kreitner K-F (2022) Late gadolinium enhancement cardiac magnetic resonance imaging: from basic concepts to emerging methods. ROFO Fortschr Geb Rontgenstr Nuklearmed 194:491–504

    Article  PubMed  Google Scholar 

  14. Simonetti OP, Kim RJ, Fieno DS, Hillenbrand HB, Wu E, Bundy JM, Finn JP, Judd RM (2001) An improved MR imaging technique for the visualization of myocardial infarction. Radiology 218:215–223

    Article  CAS  PubMed  Google Scholar 

  15. Kellman P, Arai AE, McVeigh ER, Aletras AH (2002) Phase-sensitive inversion recovery for detecting myocardial infarction using gadolinium-delayed hyperenhancement. Magn Reson Med 47:372–383

    Article  PubMed  PubMed Central  Google Scholar 

  16. Look DC, Locker DR (1970) Time saving in measurement of NMR and EPR relaxation times. Rev Sci Instrum 41:250–251

    Article  CAS  Google Scholar 

  17. Doltra A, Amundsen BH, Gebker R, Fleck E, Kelle S (2013) Emerging concepts for myocardial late gadolinium enhancement MRI. Curr Cardiol Rev 9:185–190

    Article  PubMed  PubMed Central  Google Scholar 

  18. McCrohon JA, Moon JCC, Prasad SK, McKenna WJ, Lorenz CH, Coats AJS, Pennell DJ (2003) Differentiation of heart failure related to dilated cardiomyopathy and coronary artery disease using gadolinium-enhanced cardiovascular magnetic resonance. Circulation 108:54–59

    Article  CAS  PubMed  Google Scholar 

  19. De Stefano D, Parillo M, Garipoli A, Beomonte Zobel B (2021) Imaging findings in a case of myo-pericarditis associated with SARS CoV-2 disease. J Cardiol Cases 24:210–214

    Article  PubMed  PubMed Central  Google Scholar 

  20. Dang Y, Hou Y (2021) The prognostic value of late gadolinium enhancement in heart diseases: an umbrella review of meta-analyses of observational studies. Eur Radiol 31:4528–4537

    Article  PubMed  Google Scholar 

  21. Toupin S, Pezel T, Bustin A, Cochet H (2022) Whole-heart high-resolution late gadolinium enhancement: techniques and clinical applications. J Magn Reson Imaging JMRI 55:967–987

    Article  PubMed  Google Scholar 

  22. Badger TJ, Adjei-Poku YA, Burgon NS, Kalvaitis S, Shaaban A, Sommers DN, Blauer JJE, Fish EN, Akoum N, Haslem TS, Kholmovski EG, MacLeod RS, Adler DG, Marrouche NF (2009) Initial experience of assessing esophageal tissue injury and recovery using delayed-enhancement MRI after atrial fibrillation ablation. Circ Arrhythm Electrophysiol 2:620–625

    Article  PubMed  Google Scholar 

  23. von Bary C, Dornia C, Kirchner G, Weber S, Fellner C, Nisenbaum D, Georgieva M, Stroszczynski C, Hamer OW (2013) Esophageal tissue injury following pulmonary vein isolation using the PVAC: assessment by endoscopy and magnetic resonance imaging. Pacing Clin Electrophysiol PACE 36:477–485

    Article  Google Scholar 

  24. Yeon SB, Sabir A, Clouse M, Martinezclark PO, Peters DC, Hauser TH, Gibson CM, Nezafat R, Maintz D, Manning WJ, Botnar RM (2007) Delayed-enhancement cardiovascular magnetic resonance coronary artery wall imaging: comparison with multislice computed tomography and quantitative coronary angiography. J Am Coll Cardiol 50:441–447

    Article  PubMed  Google Scholar 

  25. Schneeweis C, Schnackenburg B, Stuber M, Berger A, Schneider U, Yu J, Gebker R, Weiss RG, Fleck E, Kelle S (2012) Delayed contrast-enhanced MRI of the coronary artery wall in takayasu arteritis. PLoS ONE 7:e50655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Wasserman BA, Smith WI, Trout HH, Cannon RO, Balaban RS, Arai AE (2002) Carotid artery atherosclerosis: in vivo morphologic characterization with gadolinium-enhanced double-oblique MR imaging initial results. Radiology 223:566–573

    Article  PubMed  Google Scholar 

  27. Wasserman BA, Casal SG, Astor BC, Aletras AH, Arai AE (2005) Wash-in kinetics for gadolinium-enhanced magnetic resonance imaging of carotid atheroma. J Magn Reson Imaging JMRI 21:91–95

    Article  PubMed  Google Scholar 

  28. Yuan C, Kerwin WS, Ferguson MS, Polissar N, Zhang S, Cai J, Hatsukami TS (2002) Contrast-enhanced high resolution MRI for atherosclerotic carotid artery tissue characterization. J Magn Reson Imaging JMRI 15:62–67

    Article  PubMed  Google Scholar 

  29. Rantner B, Sojer M, Kremser C, Cartes-Zumelzu F, Fraedrich G, Jaschke W, Chemelli-Steingruber I (2013) Enhancement patterns in the fibro cellular tissue in different kinds of plaques of the internal carotid artery. Eur J Radiol 82:1989–1995

    Article  PubMed  Google Scholar 

  30. Yang H, Lv P, Zhang R, Fu C, Lin J (2021) Detection of mural inflammation with low b-value diffusion-weighted imaging in patients with active Takayasu Arteritis. Eur Radiol 31:6666–6675

    Article  PubMed  Google Scholar 

  31. Choe YH, Han BK, Koh EM, Kim DK, Do YS, Lee WR (2000) Takayasu’s arteritis: assessment of disease activity with contrast-enhanced MR imaging. AJR Am J Roentgenol 175:505–511

    Article  CAS  PubMed  Google Scholar 

  32. Jiang L, Li D, Yan F, Dai X, Li Y, Ma L (2012) Evaluation of Takayasu arteritis activity by delayed contrast-enhanced magnetic resonance imaging. Int J Cardiol 155:262–267

    Article  PubMed  Google Scholar 

  33. Desai MY, Stone JH, Foo TKF, Hellmann DB, Lima JAC, Bluemke DA (2005) Delayed contrast-enhanced MRI of the aortic wall in Takayasu’s arteritis: initial experience. AJR Am J Roentgenol 184:1427–1431

    Article  PubMed  Google Scholar 

  34. Liu M, Liu W, Li H, Shu X, Tao X, Zhai Z (2017) Evaluation of takayasu arteritis with delayed contrast-enhanced MR imaging by a free-breathing 3D IR turbo FLASH. Medicine (Baltimore) 96:e9284

    Article  PubMed  PubMed Central  Google Scholar 

  35. Dejaco C, Ramiro S, Bond M, Bosch P, Ponte C, Mackie SL, Bley TA, Blockmans D, Brolin S, Bolek EC, Cassie R, Cid MC, Molina-Collada J, Dasgupta B, Nielsen BD, De Miguel E, Direskeneli H, Duftner C, Hočevar A, Molto A, Schäfer VS, Seitz L, Slart RHJA, Schmidt WA. EULAR recommendations for the use of imaging in large vessel vasculitis in clinical practice: 2023 update. Ann Rheum Dis. 2023 Aug 7:ard-2023-224543. [Epub ahead of print]

  36. Yi CA, Lee KS, Han J, Chung MP, Chung MJ, Shin KM (2008) 3-T MRI for differentiating inflammation- and fibrosis-predominant lesions of usual and nonspecific interstitial pneumonia: comparison study with pathologic correlation. AJR Am J Roentgenol 190:878–885

    Article  PubMed  Google Scholar 

  37. Lavelle LP, Brady D, McEvoy S, Murphy D, Gibney B, Gallagher A, Butler M, Shortt F, McMullen M, Fabre A, Lynch DA, Keane MP, Dodd JD (2017) Pulmonary fibrosis: tissue characterization using late-enhanced MRI compared with unenhanced anatomic high-resolution CT. Diagn Interv Radiol Ank Turk 23:106–111

    Article  Google Scholar 

  38. Fleming H, Clifford SM, Haughey A, MacDermott R, McVeigh N, Healy GM, Lavelle L, Abbara S, Murphy DJ, Fabre A, McKone E, McCarthy C, Butler M, Doran P, Lynch DA, Keane MP, Dodd JD (2020) Differentiating combined pulmonary fibrosis and emphysema from pure emphysema: utility of late gadolinium-enhanced MRI. Eur Radiol Exp 4:61

    Article  PubMed  PubMed Central  Google Scholar 

  39. Absinta M, Ha S-K, Nair G, Sati P, Luciano NJ, Palisoc M, Louveau A, Zaghloul KA, Pittaluga S, Kipnis J, Reich DS (2017) Human and nonhuman primate meninges harbor lymphatic vessels that can be visualized noninvasively by MRI. Elife 6:e29738

    Article  PubMed  PubMed Central  Google Scholar 

  40. Jost G, Frenzel T, Lohrke J, Lenhard DC, Naganawa S, Pietsch H (2017) Penetration and distribution of gadolinium-based contrast agents into the cerebrospinal fluid in healthy rats: a potential pathway of entry into the brain tissue. Eur Radiol 27:2877–2885

    Article  PubMed  Google Scholar 

  41. Rasschaert M, Weller RO, Schroeder JA, Brochhausen C, Idée J-M (2020) Retention of gadolinium in brain parenchyma: pathways for speciation, access, and distribution. a critical review. J Magn Reson Imaging JMRI 52:1293–1305

    Article  PubMed  Google Scholar 

  42. Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med 4:147ra111

    Article  PubMed  PubMed Central  Google Scholar 

  43. Naganawa S, Komada T, Fukatsu H, Ishigaki T, Takizawa O (2006) Observation of contrast enhancement in the cochlear fluid space of healthy subjects using a 3D-FLAIR sequence at 3 Tesla. Eur Radiol 16:733–737

    Article  PubMed  Google Scholar 

  44. Naganawa S, Kawai H, Sone M, Nakashima T (2010) Increased sensitivity to low concentration gadolinium contrast by optimized heavily T2-weighted 3D-FLAIR to visualize endolymphatic space. Magn Reson Med Sci MRMS Off J Jpn Soc Magn Reson Med 9:73–80

    Google Scholar 

  45. Deike-Hofmann K, Reuter J, Haase R, Paech D, Gnirs R, Bickelhaupt S, Forsting M, Heußel CP, Schlemmer H-P, Radbruch A (2019) Glymphatic pathway of gadolinium-based contrast agents through the brain: overlooked and misinterpreted. Invest Radiol 54:229–237

    Article  CAS  PubMed  Google Scholar 

  46. Naganawa S, Nakane T, Kawai H, Taoka T (2018) Differences in signal intensity and enhancement on mr images of the perivascular spaces in the basal ganglia versus those in white matter. Magn Reson Med Sci MRMS 17:301–307

    Article  CAS  PubMed  Google Scholar 

  47. Naganawa S, Nakane T, Kawai H, Taoka T (2017) Gd-based contrast enhancement of the perivascular spaces in the basal Ganglia. Magn Reson Med Sci MRMS 16:61–65

    Article  CAS  PubMed  Google Scholar 

  48. Naganawa S, Yamazaki M, Kawai H, Sone M, Nakashima T (2011) Contrast enhancement of the anterior eye segment and subarachnoid space: detection in the normal state by heavily T2-weighted 3D FLAIR. Magn Reson Med Sci MRMS 10:193–199

    Article  PubMed  Google Scholar 

  49. Naganawa S, Nakane T, Kawai H, Taoka T (2019) Age dependence of gadolinium leakage from the cortical veins into the cerebrospinal fluid assessed with whole brain 3D-real inversion recovery MR imaging. Magn Reson Med Sci MRMS 18:163–169

    Article  CAS  PubMed  Google Scholar 

  50. Nakashima T, Naganawa S, Sugiura M, Teranishi M, Sone M, Hayashi H, Nakata S, Katayama N, Ishida IM (2007) Visualization of endolymphatic hydrops in patients with Meniere’s disease. Laryngoscope 117:415–420

    Article  PubMed  Google Scholar 

  51. Basura GJ, Adams ME, Monfared A, Schwartz SR, Antonelli PJ, Burkard R, Bush ML, Bykowski J, Colandrea M, Derebery J, Kelly EA, Kerber KA, Koopman CF, Kuch AA, Marcolini E, McKinnon BJ, Ruckenstein MJ, Valenzuela CV, Vosooney A, Walsh SA, Nnacheta LC, Dhepyasuwan N, Buchanan EM (2020) Clinical practice guideline: Ménière’s disease. Otolaryngol-Head Neck Surg 162:S1–S55

    PubMed  Google Scholar 

  52. Conte G, Lo Russo FM, Calloni SF, Sina C, Barozzi S, Di Berardino F, Scola E, Palumbo G, Zanetti D, Triulzi FM (2018) MR imaging of endolymphatic hydrops in Ménière’s disease: not all that glitters is gold. Acta Otorhinolaryngol Ital Organo Uff Della Soc Ital Otorinolaringol E Chir Cerv-facc 38:369–376

    CAS  Google Scholar 

  53. Hoskin JL (2022) Ménière’s disease: new guidelines, subtypes, imaging, and more. Curr Opin Neurol 35:90–97

    Article  PubMed  Google Scholar 

  54. Lee KM, Kim JH, Kim E, Choi BS, Bae YJ, Bae H-J (2016) Early stage of hyperintense acute reperfusion marker on contrast-enhanced FLAIR images in patients with acute stroke. AJR Am J Roentgenol 206:1272–1275

    Article  PubMed  Google Scholar 

  55. Ogami R, Nakahara T, Hamasaki O, Araki H, Kurisu K (2011) Cerebrospinal fluid enhancement on fluid attenuated inversion recovery images after carotid artery stenting with neuroprotective balloon occlusions: hemodynamic instability and blood–brain barrier disruption. Cardiovasc Intervent Radiol 34:936–941

    Article  PubMed  Google Scholar 

  56. van de Haar HJ, Burgmans S, Jansen JFA, van Osch MJP, van Buchem MA, Muller M, Hofman PAM, Verhey FRJ, Backes WH (2016) Blood–brain barrier leakage in patients with early Alzheimer disease. Radiology 281:527–535

    Article  PubMed  Google Scholar 

  57. Jelescu IO, Leppert IR, Narayanan S, Araújo D, Arnold DL, Pike GB (2011) Dual-temporal resolution dynamic contrast-enhanced MRI protocol for blood–brain barrier permeability measurement in enhancing multiple sclerosis lesions. J Magn Reson Imaging JMRI 33:1291–1300

    Article  CAS  PubMed  Google Scholar 

  58. Freeze WM, Schnerr RS, Palm WM, Jansen JF, Jacobs HI, Hoff EI, Verhey FR, Backes WH (2017) Pericortical enhancement on delayed postgadolinium fluid-attenuated inversion recovery images in normal aging, mild cognitive impairment, and Alzheimer disease. AJNR Am J Neuroradiol 38:1742–1747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Israeli D, Tanne D, Daniels D, Last D, Shneor R, Guez D, Landau E, Roth Y, Ocherashvilli A, Bakon M, Hoffman C, Weinberg A, Volk T, Mardor Y (2010) The application of MRI for depiction of subtle blood brain barrier disruption in stroke. Int J Biol Sci 7:1–8

    Article  PubMed  PubMed Central  Google Scholar 

  60. Berger JR, Nath A, Greenberg RN, Andersen AH, Greene RA, Bognar A, Avison MJ (2000) Cerebrovascular changes in the basal ganglia with HIV dementia. Neurology 54:921–926

    Article  CAS  PubMed  Google Scholar 

  61. Filippopulos FM, Fischer TD, Seelos K, Dunker K, Belanovic B, Crispin A, Stahl R, Liebig T, Straube A, Forbrig R (2022) Semiquantitative 3T brain magnetic resonance imaging for dynamic visualization of the glymphatic-lymphatic fluid transport system in humans: a pilot study. Invest Radiol 57:544–551

    Article  CAS  PubMed  Google Scholar 

  62. Ding X-B, Wang X-X, Xia D-H, Liu H, Tian H-Y, Fu Y, Chen Y-K, Qin C, Wang J-Q, Xiang Z, Zhang Z-X, Cao Q-C, Wang W, Li J-Y, Wu E, Tang B-S, Ma M-M, Teng J-F, Wang X-J (2021) Impaired meningeal lymphatic drainage in patients with idiopathic Parkinson’s disease. Nat Med 27:411–418

    Article  CAS  PubMed  Google Scholar 

  63. Joo B, Park M, Ahn SJ, Suh SH (2023) Assessment of meningeal lymphatics in the parasagittal dural space: a prospective feasibility study using dynamic contrast-enhanced magnetic resonance imaging. Korean J Radiol 24:444–453

    Article  PubMed  PubMed Central  Google Scholar 

  64. Zach L, Guez D, Last D, Daniels D, Grober Y, Nissim O, Hoffmann C, Nass D, Talianski A, Spiegelmann R, Cohen ZR, Mardor Y (2012) Delayed contrast extravasation MRI for depicting tumor and non-tumoral tissues in primary and metastatic brain tumors. PLoS ONE 7:e52008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Zach L, Guez D, Last D, Daniels D, Grober Y, Nissim O, Hoffmann C, Nass D, Talianski A, Spiegelmann R, Tsarfaty G, Salomon S, Hadani M, Kanner A, Blumenthal DT, Bukstein F, Yalon M, Zauberman J, Roth J, Shoshan Y, Fridman E, Wygoda M, Limon D, Tzuk T, Cohen ZR, Mardor Y (2015) Delayed contrast extravasation MRI: a new paradigm in neuro-oncology. Neuro-Oncol 17:457–465

    Article  CAS  PubMed  Google Scholar 

  66. Wagner S, Lanfermann H, Eichner G, Gufler H (2017) Radiation injury versus malignancy after stereotactic radiosurgery for brain metastases: impact of time-dependent changes in lesion morphology on MRI. Neuro-Oncol 19:586–594

    CAS  PubMed  Google Scholar 

  67. Satvat N, Korczynski O, Müller-Eschner M, Othman AE, Schöffling V, Keric N, Ringel F, Sommer C, Brockmann MA, Reder S (2022) A rapid late enhancement mri protocol improves differentiation between brain tumor recurrence and treatment-related contrast enhancement of brain parenchyma. Cancers 14:5523

    Article  PubMed  PubMed Central  Google Scholar 

  68. Knopp MV, Runge VM, Essig M, Hartman M, Jansen O, Kirchin MA, Moeller A, Seeberg AH, Lodemann K-P (2004) Primary and secondary brain tumors at MR imaging: bicentric intraindividual crossover comparison of gadobenate dimeglumine and gadopentetate dimeglumine. Radiology 230:55–64

    Article  PubMed  Google Scholar 

  69. Chen M, Wang P, Guo Y, Yin Y, Wang L, Su Y, Gong G (2022) The effect of time delay for magnetic resonance contrast-enhanced scan on imaging for small-volume brain metastases. NeuroImage: Clin 36:103223. https://doi.org/10.1016/j.nicl.2022.103223

    Article  PubMed  Google Scholar 

  70. Jeon J-Y, Choi JW, Roh HG, Moon W-J (2014) Effect of imaging time in the magnetic resonance detection of intracerebral metastases using single dose gadobutrol. Korean J Radiol 15:145–150

    Article  PubMed  PubMed Central  Google Scholar 

  71. Yuh WT, Tali ET, Nguyen HD, Simonson TM, Mayr NA, Fisher DJ (1995) The effect of contrast dose, imaging time, and lesion size in the MR detection of intracerebral metastasis. AJNR Am J Neuroradiol 16:373–380

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Cohen-Inbar O, Xu Z, Dodson B, Rizvi T, Durst CR, Mukherjee S, Sheehan JP (2016) Time-delayed contrast-enhanced MRI improves detection of brain metastases: a prospective validation of diagnostic yield. J Neurooncol 130:485–494

    Article  PubMed  Google Scholar 

  73. Pronin IN, McManus KA, Holodny AI, Peck KK, Kornienko VN (2009) Quantification of dispersion of Gd-DTPA from the initial area of enhancement into the peritumoral zone of edema in brain tumors. J Neurooncol 94:399–408

    Article  PubMed  Google Scholar 

  74. Wattjes MP, Ciccarelli O, Reich DS, Banwell B, de Stefano N, Enzinger C, Fazekas F, Filippi M, Frederiksen J, Gasperini C, Hacohen Y, Kappos L, Li DKB, Mankad K, Montalban X, Newsome SD, Oh J, Palace J, Rocca MA, Sastre-Garriga J, Tintoré M, Traboulsee A, Vrenken H, Yousry T, Barkhof F, Rovira À, Magnetic Resonance Imaging in Multiple Sclerosis study group, Consortium of Multiple Sclerosis Centres, North American Imaging in Multiple Sclerosis Cooperative MRI guidelines working group (2021) (2021) MAGNIMS-CMSC-NAIMS consensus recommendations on the use of MRI in patients with multiple sclerosis. Lancet Neurol 20:653–670

    Article  PubMed  Google Scholar 

  75. Rovira À, Doniselli FM, Auger C, Haider L, Hodel J, Severino M, Wattjes MP, van der Molen AJ, Jasperse B, Mallio CA, Yousry T, Quattrocchi CC, ESMRMB-GREC Working Group and of the ESNR Multiple Sclerosis Working Group (2023) Use of gadolinium-based contrast agents in multiple sclerosis: a review by the ESMRMB-GREC and ESNR Multiple Sclerosis Working Group. Eur Radiol. https://doi.org/10.1007/s00330-023-10151-y

    Article  PubMed  Google Scholar 

  76. Ismail MA, Elsayed NM (2023) Diffusion-weighted images and contrast-enhanced MRI in the diagnosis of different stages of multiple sclerosis of the central nervous system. Cureus 15:e41650

    PubMed  PubMed Central  Google Scholar 

  77. Hashemi H, Behzadi S, Ghanaati H, Harirchian MH, Yaghoobi M, Shakiba M, Jalali AH, Firouznia K (2014) Evaluation of plaque detection and optimum time of enhancement in acute attack multiple sclerosis after contrast injection. Acta Radiol Stockh Swed 55:218–224

    Google Scholar 

  78. Absinta M, Vuolo L, Rao A, Nair G, Sati P, Cortese ICM, Ohayon J, Fenton K, Reyes-Mantilla MI, Maric D, Calabresi PA, Butman JA, Pardo CA, Reich DS (2015) Gadolinium-based MRI characterization of leptomeningeal inflammation in multiple sclerosis. Neurology 85:18–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Parillo M, Vaccarino F, Quattrocchi CC (2023) Imaging findings in a case of leptomeningeal myelomatosis, a rare but critical central nervous system complication of multiple myeloma. Neuroradiol J. https://doi.org/10.1177/19714009221150849

    Article  PubMed  Google Scholar 

  80. Kremer S, Abu Eid M, Bierry G, Bogorin A, Koob M, Dietemann JL, Fruehlich S (2006) Accuracy of delayed post-contrast FLAIR MR imaging for the diagnosis of leptomeningeal infectious or tumoral diseases. J Neuroradiol J Neuroradiol 33:285–291

    Article  CAS  PubMed  Google Scholar 

  81. Venkatasamy A, Huynh TT, Wohlhuter N, Vuong H, Rohmer D, Charpiot A, Meyer N, Veillon F (2019) Superior vestibular neuritis: improved detection using FLAIR sequence with delayed enhancement (1 h). Eur Arch Oto-Rhino-Laryngol 276:3309–3316

    Article  Google Scholar 

  82. Fábrega-Foster K, Ghasabeh MA, Pawlik TM, Kamel IR (2017) Multimodality imaging of intrahepatic cholangiocarcinoma. Hepatobiliary Surg Nutr 6:67–78

    Article  PubMed  PubMed Central  Google Scholar 

  83. Guarise A, Venturini S, Faccioli N, Pinali L, Morana G (2006) Role of magnetic resonance in characterising extrahepatic cholangiocarcinomas. Radiol Med (Torino) 111:526–538

    Article  CAS  PubMed  Google Scholar 

  84. Masselli G, Manfredi R, Vecchioli A, Gualdi G (2008) MR imaging and MR cholangiopancreatography in the preoperative evaluation of hilar cholangiocarcinoma: correlation with surgical and pathologic findings. Eur Radiol 18:2213–2221

    Article  PubMed  Google Scholar 

  85. Leyendecker JR, Gakhal M, Elsayes KM, McDermott R, Narra VR, Brown JJ (2008) Fat-suppressed dynamic and delayed gadolinium-enhanced volumetric interpolated breath-hold magnetic resonance imaging of cholangiocarcinoma. J Comput Assist Tomogr 32:178–184

    Article  PubMed  Google Scholar 

  86. Gabata T, Matsui O, Kadoya M, Yoshikawa J, Ueda K, Kawamori Y, Takashima T, Nonomura A (1998) Delayed MR imaging of the liver: correlation of delayed enhancement of hepatic tumors and pathologic appearance. Abdom Imaging 23:309–313

    Article  CAS  PubMed  Google Scholar 

  87. Cheung HMC, Karanicolas PJ, Hsieh E, Coburn N, Maraj T, Kim JK, Elhakim H, Haider MA, Law C, Milot L (2018) Late gadolinium enhancement of colorectal liver metastases post-chemotherapy is associated with tumour fibrosis and overall survival post-hepatectomy. Eur Radiol 28:3505–3512

    Article  PubMed  PubMed Central  Google Scholar 

  88. Semelka RC, Chung JJ, Hussain SM, Marcos HB, Woosley JT (2001) Chronic hepatitis: correlation of early patchy and late linear enhancement patterns on gadolinium-enhanced MR images with histopathology initial experience. J Magn Reson Imaging JMRI 13:385–391

    Article  CAS  PubMed  Google Scholar 

  89. Yoshimitsu K, Honda H, Kaneko K, Kuroiwa T, Irie H, Ueki T, Chijiiwa K, Takenaka K, Masuda K (1997) Dynamic MRI of the gallbladder lesions: differentiation of benign from malignant. J Magn Reson Imaging JMRI 7:696–701

    Article  CAS  PubMed  Google Scholar 

  90. Irie H, Honda H, Shinozaki K, Yoshimitsu K, Aibe H, Nishie A, Nakayama T, Masuda K (2002) MR imaging of ampullary carcinomas. J Comput Assist Tomogr 26:711–717

    Article  PubMed  Google Scholar 

  91. Jia H, Li J, Huang W, Lin G (2021) Multimodel magnetic resonance imaging of mass-forming autoimmune pancreatitis: differential diagnosis with pancreatic ductal adenocarcinoma. BMC Med Imaging 21:149

    Article  PubMed  PubMed Central  Google Scholar 

  92. Choi S-Y, Kim SH, Kang TW, Song KD, Park HJ, Choi Y-H (2016) Differentiating mass-forming autoimmune pancreatitis from pancreatic ductal adenocarcinoma on the basis of contrast-enhanced MRI and DWI findings. AJR Am J Roentgenol 206:291–300

    Article  PubMed  Google Scholar 

  93. Carbognin G, Girardi V, Biasiutti C, Camera L, Manfredi R, Frulloni L, Hermans JJ, Mucelli RP (2009) Autoimmune pancreatitis: imaging findings on contrast-enhanced MR, MRCP and dynamic secretin-enhanced MRCP. Radiol Med (Torino) 114:1214–1231

    Article  CAS  PubMed  Google Scholar 

  94. Ichikawa T, Peterson MS, Federle MP, Baron RL, Haradome H, Kawamori Y, Nawano S, Araki T (2000) Islet cell tumor of the pancreas: biphasic CT versus MR imaging in tumor detection. Radiology 216:163–171

    Article  CAS  PubMed  Google Scholar 

  95. Parillo M, van der Molen AJ, Asbach P, Elsholtz FHJ, Laghi A, Ronot M, Wu JS, Mallio CA, Quattrocchi CC (2023) The role of iodinated contrast media in computed tomography structured Reporting and Data Systems (RADS): a narrative review. Quant Imaging Med Surg 13:7621–7631

    Article  PubMed  PubMed Central  Google Scholar 

  96. Mehran R, Dangas GD, Weisbord SD (2019) Contrast-associated acute kidney injury. N Engl J Med 380:2146–2155

    Article  CAS  PubMed  Google Scholar 

  97. Rouvière O, Cornelis F, Brunelle S, Roy C, André M, Bellin M-F, Boulay I, Eiss D, Girouin N, Grenier N, Hélénon O, Lapray J-F, Lefèvre A, Matillon X, Ménager J-M, Millet I, Ronze S, Sanzalone T, Tourniaire J, Rocher L, Renard-Penna R, French Society of Genitourinary Imaging Consensus group (2020) Imaging protocols for renal multiparametric MRI and MR urography: results of a consensus conference from the French Society of Genitourinary Imaging. Eur Radiol 30:2103–2114

    Article  PubMed  Google Scholar 

  98. Cornelis F, Lasserre A-S, Tourdias T, Deminière C, Ferrière J-M, Le Bras Y, Grenier N (2013) Combined late gadolinium-enhanced and double-echo chemical-shift MRI help to differentiate renal oncocytomas with high central T2 signal intensity from renal cell carcinomas. AJR Am J Roentgenol 200:830–838

    Article  PubMed  Google Scholar 

  99. Abreu-Gomez J, Udare A, Shanbhogue KP, Schieda N (2019) Update on MR urography (MRU): technique and clinical applications. Abdom Radiol N Y 44:3800–3810

    Article  Google Scholar 

  100. Park BK, Kim CK, Kim B, Kwon GY (2007) Adrenal tumors with late enhancement on CT and MRI. Abdom Imaging 32:515–518

    Article  PubMed  Google Scholar 

  101. Rimola J, Planell N, Rodríguez S, Delgado S, Ordás I, Ramírez-Morros A, Ayuso C, Aceituno M, Ricart E, Jauregui-Amezaga A, Panés J, Cuatrecasas M (2015) Characterization of inflammation and fibrosis in Crohn’s disease lesions by magnetic resonance imaging. Am J Gastroenterol 110:432–440

    Article  PubMed  Google Scholar 

  102. Mazza S, Conforti FS, Forzenigo LV, Piazza N, Bertè R, Costantino A, Fraquelli M, Coletta M, Rimola J, Vecchi M, Caprioli F (2022) Agreement between real-time elastography and delayed enhancement magnetic resonance enterography on quantifying bowel wall fibrosis in Crohn’s disease. Dig Liver Dis 54:69–75

    Article  PubMed  Google Scholar 

  103. Cheng L, Li X (2013) Breast magnetic resonance imaging: kinetic curve assessment. Gland Surg 2:50–53

    PubMed  PubMed Central  Google Scholar 

  104. Koh J, Park AY, Ko KH, Jung HK (2020) MRI diagnostic features for predicting nipple-areolar-complex involvement in breast cancer. Eur J Radiol 122:108754

    Article  PubMed  Google Scholar 

  105. Santamaría G, Bargalló X, Fernández PL, Farrús B, Caparrós X, Velasco M (2017) Neoadjuvant systemic therapy in breast cancer: association of contrast-enhanced mr imaging findings, diffusion-weighted imaging findings, and tumor subtype with tumor response. Radiology 283:663–672

    Article  PubMed  Google Scholar 

  106. Zhao C, Li J, Wang W, Gong G, Xu L, Zhang Y, Li F, Shao Q, Wang J, Liu X, Xu M (2021) DE-MR simulation imaging for prone radiotherapy after breast-conserving surgery: assessing its application in lumpectomy cavity delineation based on deformable image registration. Radiat Oncol Lond Engl 16:91

    Article  Google Scholar 

  107. de Faria Castro Fleury E, Gianini AC, Ayres V, Ramalho LC, Seleti RO, Roveda D (2017) Breast magnetic resonance imaging: tips for the diagnosis of silicone-induced granuloma of a breast implant capsule (SIGBIC). Insights Imaging 8:439–446

    Article  PubMed  PubMed Central  Google Scholar 

  108. Rajasekaran S, Babu JN, Arun R, Armstrong BRW, Shetty AP, Murugan S (2004) ISSLS prize winner: a study of diffusion in human lumbar discs: a serial magnetic resonance imaging study documenting the influence of the endplate on diffusion in normal and degenerate discs. Spine 29:2654–2667

    Article  CAS  PubMed  Google Scholar 

  109. Niinimäki JL, Parviainen O, Ruohonen J, Ojala RO, Kurunlahti M, Karppinen J, Tervonen O, Nieminen MT (2006) In vivo quantification of delayed gadolinium enhancement in the nucleus pulposus of human intervertebral disc. J Magn Reson Imaging JMRI 24:796–800

    Article  PubMed  Google Scholar 

  110. Bekkers JEJ, Bartels LW, Benink RJ, Tsuchida AI, Vincken KL, Dhert WJA, Creemers LB, Saris DBF (2013) Delayed gadolinium enhanced MRI of cartilage (dGEMRIC) can be effectively applied for longitudinal cohort evaluation of articular cartilage regeneration. Osteoarthritis Cartilage 21:943–949

    Article  CAS  PubMed  Google Scholar 

  111. Piccolo CL, Mallio CA, Vaccarino F, Grasso RF, Zobel BB (2023) Imaging of knee osteoarthritis: a review of multimodal diagnostic approach. Quant Imaging Med Surg 13:7582–7595

    Article  PubMed  PubMed Central  Google Scholar 

  112. van Tiel J, Kotek G, Reijman M, Bos PK, Bron EE, Klein S, Verhaar JAN, Krestin GP, Weinans H, Oei EHG (2014) Delayed gadolinium-enhanced MRI of the meniscus (dGEMRIM) in patients with knee osteoarthritis: relation with meniscal degeneration on conventional MRI, reproducibility, and correlation with dGEMRIC. Eur Radiol 24:2261–2270

    Article  PubMed  Google Scholar 

  113. Schwenzer NF, Kötter I, Henes JC, Schraml C, Fritz J, Claussen CD, Horger M (2010) The role of dynamic contrast-enhanced MRI in the differential diagnosis of psoriatic and rheumatoid arthritis. AJR Am J Roentgenol 194:715–720

    Article  PubMed  Google Scholar 

  114. Schraml C, Schwenzer NF, Martirosian P, Koetter I, Henes JC, Geiger K, Claussen CD, Horger M (2011) Assessment of synovitis in erosive osteoarthritis of the hand using DCE-MRI and comparison with that in its major mimic, the psoriatic arthritis. Acad Radiol 18:804–809

    Article  PubMed  Google Scholar 

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Acknowledgements

The ESMRMB-GREC (Gadolinium Research & Education Committee) is a group of multidisciplinary ESMRMB members, including clinicians, scientists, chemists, physicists, pathologists, and clinical epidemiologists who all share a common interest in the study of gadolinium-based contrast agents in a wide variety of clinical and preclinical conditions. The authors thank all the members for their insights despite their specific competence and experience. The list of authors includes the members who developed the project and those experts who have revised and approved the final version of the manuscript.

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Correspondence to Carlo Augusto Mallio.

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The ESMRMB-GREC (Gadolinium Research & Education Committee) is a group of multidisciplinary ESMRMB members, including academic experts of industries. GREC annual meetings are sponsored by the unconditional support of Bayer AG, Bracco, GE Healthcare and Guerbet.

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Parillo, M., Mallio, C.A., Dekkers, I.A. et al. Late/delayed gadolinium enhancement in MRI after intravenous administration of extracellular gadolinium-based contrast agents: is it worth waiting?. Magn Reson Mater Phy 37, 151–168 (2024). https://doi.org/10.1007/s10334-024-01151-0

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