Skip to main content
Log in

Role of Cardiac MRI Imaging of Focal and Diffuse Inflammation and Fibrosis in Cardiomyopathy Patients Who Have Pacemakers/ICD Devices

  • Myocardial Disease (A Abbate and M Merlo, Section Editors)
  • Published:
Current Cardiology Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

This focused report aims to discuss and summarize the use of conventional and emerging methods using cardiovascular magnetic resonance (CMR) imaging in cardiomyopathy patients with implanted cardiac devices to identify diffuse and focal inflammation and fibrosis.

Recent Findings

Many cardiomyopathy patients with diffuse and focal myocardial fibrosis have a unique need for cardiac imaging that is complicated by cardiovascular implantable electronic devices (CIEDs). CMR imaging can accurately image myocardial fibrosis and inflammation using T1 mapping and late gadolinium enhancement (LGE) imaging. CMR imaging in CIED patients, however, has been limited due to severe imaging artifacts associated with the devices. The emergence of wideband imaging variants of LGE and T1 mapping techniques can successfully reduce or eliminate CIED artifacts for the evaluation of myocardial substrate in cardiomyopathy patients.

Summary

Wideband imaging variants of LGE and T1 mapping techniques provide new tools for imaging focal and diffuse fibrosis and imaging in cardiomyopathy patients with implanted cardiac devices. These emerging techniques have the potential for great impact in clinical care of such patients as well as clinical research where imaging endpoints are desired.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

CIED:

Cardiovascular implantable electronic device

CMR:

Cardiovascular magnetic resonance

CVF:

Collagen volume fraction

FLASH:

Fast, low-angle shot

ICD:

Implantable cardioverter defibrillator

LGE:

Late gadolinium enhancement

MOCO:

Motion corrected

MOLLI:

Modified Look-Locker inversion recovery

MRI:

Magnetic resonance imaging

MT:

Magnetization transfer

PM:

Pacemaker

PSIR:

Phase sensitive inversion recovery

SAPPHIRE:

Saturation-pulse prepared heart-rate independent inversion recovery

SAR:

Specific absorption rate

SASHA:

Saturation recovery single-shot acquisition

shMOLLI:

Shortened modified Look-Locker inversion recovery

SR:

Saturation recovery

SSFP:

Steady-state free precession

TI:

Inversion time

WB LGE:

Wideband late gadolinium enhancement

References

Papers of particular interest, published recently, have been highlighted as: •   Of importance •• Of major importance

  1. Maass AH, Hemels MEW, Allaart CP. Magnetic resonance imaging in patients with cardiac implantable electronic devices. Neth Heart J. 2018;26:584–90.

    Article  CAS  Google Scholar 

  2. • Bhuva AN, Moralee R, Moon JC, Manisty CH. Making MRI available for patients with cardiac implantable electronic devices: growing need and barriers to change. Eur Radiol. 2020;30:1378–84. This article aims to enable healthcare providers to build MRI services urgently for cardiac device patients, so they may benefit from the same access to MRI as everyone else.

    Article  CAS  Google Scholar 

  3. Baikoussis NG, Apostolakis E, Papakonstantinou NA, Sarantitis I, Dougenis D. Safety of magnetic resonance imaging in patients with implanted cardiac prostheses and metallic cardiovascular electronic devices. Ann Thorac Surg. 2011;91:2006–11.

    Article  Google Scholar 

  4. Camacho JC, Moreno CC, Shah AD, Mittal PK, Mengistu A, Lloyd MS, El-Chami MF, Lerakis S, Saindane AM. Safety and quality of 1.5-T MRI in patients with conventional and MRI-conditional cardiac implantable electronic devices after implementation of a standardized protocol. AJR Am J Roentgenol. 2016;207:599–604.

    Article  Google Scholar 

  5. Roguin A, Zviman MM, Meininger GR, Rodrigues ER, Dickfeld TM, Bluemke DA, Lardo A, Berger RD, Calkins H, Halperin HR. Modern pacemaker and implantable cardioverter/defibrillator systems can be magnetic resonance imaging safe: in vitro and in vivo assessment of safety and function at 1.5 T. Circulation. 2004;110:475–82.

    Article  Google Scholar 

  6. Nyenhuis JA, Park SM, Kamondetdacha R, Amjad A, Shellock F, Rezai A. MRI and implanted medical devices: basic interactions with an emphasis on heating. IEEE Trans Device Mater Reliab. 2005;5:467–80.

    Article  Google Scholar 

  7. Ferreira VM, Schulz-Menger J, Holmvang G, Kramer CM, Carbone I, Sechtem U, Kindermann I, Gutberlet M, Cooper LT, Liu P, Friedrich MG. Cardiovascular magnetic resonance in nonischemic myocardial inflammation: expert recommendations. 2018;72:3158–76.

  8. Shah AD, Morris MA, Hirsh DS, Warnock M, Huang Y, Mollerus M, Merchant FM, Patel AM, Delurgio DB, Patel AU, et al. Magnetic resonance imaging safety in nonconditional pacemaker and defibrillator recipients: a meta-analysis and systematic review. Heart Rhythm. 2018;15:1001–8.

    Article  Google Scholar 

  9. Nitz WR, Oppelt A, Renz W, Manke C, Lenhart M, Link J. On the heating of linear conductive structures as guide wires and catheters in interventional MRI. J Magn Reson Imaging. 2001;13:105–14.

    Article  CAS  Google Scholar 

  10. •• Bhuva AN, Kellman P, Graham A, Ramlall M, Boubertakh R, Feuchter P, Hawkins A, Lowe M, Lambiase PD, Sekhri N, et al. Clinical impact of cardiovascular magnetic resonance with optimized myocardial scar detection in patients with cardiac implantable devices. Int J Cardiol. 2019;279:72–8. This article demonstrates that the clinical yield from CMR using optimized LGE sequence in patients with cardiac implantable electronic devices is high, hence the need for device dependent LGE imaging strategy using wideband LGE to achieve clinical utility.

    Article  Google Scholar 

  11. Pollo C, Villemure JG, Vingerhoets F, Ghika J, Maeder P, Meuli R. Magnetic resonance artifact induced by the electrode Activa 3389: an in vitro and in vivo study. Acta Neurochir (Wien). 2004;146:161–4.

    Article  CAS  Google Scholar 

  12. Kellman P, Hansen MS. T1-mapping in the heart: accuracy and precision. J Cardiovasc Magn Reson. 2014;16:2.

    Article  Google Scholar 

  13. Bloch F. The Principle of Nuclear Induction. Science. 1953;118:425–30.

    Article  CAS  Google Scholar 

  14. Haaf P, Garg P, Messroghli DR, Broadbent DA, Greenwood JP, Plein S. Cardiac T1 mapping and extracellular volume (ECV) in clinical practice: a comprehensive review. J Cardiovasc Magn Reson. 2016;18:89.

    Article  Google Scholar 

  15. Abdel-Aty H, Boyé P, Zagrosek A, Wassmuth R, Kumar A, Messroghli D, Bock P, Dietz R, Friedrich MG, Schulz-Menger J. Diagnostic performance of cardiovascular magnetic resonance in patients with suspected acute myocarditis: comparison of different approaches. J Am Coll Cardiol. 2005;45:1815–22.

    Article  Google Scholar 

  16. Trivieri MG, Spagnolo P, Birnie D, Liu P, Drake W, Kovacic JC, Baughman R, Fayad ZA, Judson MA. Challenges in cardiac and pulmonary sarcoidosis: JACC state-of-the-art review. J Am Coll Cardiol. 2020;76:1878–901.

    Article  Google Scholar 

  17. Aitken M, Chan MV, Urzua Fresno C, Farrell A, Islam N, McInnes MD, Iwanochko M, Balter M, Moayedi Y, Thavendiranathan P, et al. Diagnostic accuracy of cardiac MRI versus FDG PET for cardiac sarcoidosis: a systematic review and meta-analysis. Radiology. 2022:213170.

  18. Ranjan R, McGann CJ, Jeong EK, Hong K, Kholmovski EG, Blauer J, Wilson BD, Marrouche NF, Kim D. Wideband late gadolinium enhanced magnetic resonance imaging for imaging myocardial scar without image artefacts induced by implantable cardioverter-defibrillator: a feasibility study at 3 T. Europace. 2015;17:483–8.

    Article  Google Scholar 

  19. Rashid S, Rapacchi S, Shivkumar K, Plotnik A, Finn JP, Hu P. Modified wideband three-dimensional late gadolinium enhancement MRI for patients with implantable cardiac devices. Magn Reson Med. 2016;75:572–84.

    Article  Google Scholar 

  20. Rashid S, Rapacchi S, Vaseghi M, Tung R, Shivkumar K, Finn JP, Hu P. Improved late gadolinium enhancement MR imaging for patients with implanted cardiac devices. Radiology. 2014;270:269–74.

    Article  Google Scholar 

  21. Bhuva A, Ramlall M, Boubertakh R, Knott K, Feuchter P, Sekhri N, Schilling R, Kellman P, Moon J, Manisty C. (2017). Wideband free breathing MOCO LGE changes patient care in patients with implantable cardiac defibrillators. BMJ Publishing Group Ltd and British Cardiovascular Society.

  22. •• Singh A, Kawaji K, Goyal N, Nazir NT, Beaser A, O’Keefe-Baker V, Addetia K, Tung R, Hu P, Mor-Avi V, et al. Feasibility of cardiac magnetic resonance wideband protocol in patients with implantable cardioverter defibrillators and its utility for defining scar. Am J Cardiol. 2019;123:1329–35. This article demonstrates that the assessment of standard LGE is markedly limited by artifact in patients with ICD and the use of wideband LGE significantly improves image quality and can accurately localize myocardial scar before ventricular tachycardia ablation.

    Article  Google Scholar 

  23. Stevens SM, Tung R, Rashid S, Gima J, Cote S, Pavez G, Khan S, Ennis DB, Finn JP, Boyle N, et al. Device artifact reduction for magnetic resonance imaging of patients with implantable cardioverter-defibrillators and ventricular tachycardia: late gadolinium enhancement correlation with electroanatomic mapping. Heart Rhythm. 2014;11:289–98.

    Article  Google Scholar 

  24. Do DH, Eyvazian V, Bayoneta AJ, Hu P, Finn JP, Bradfield JS, Shivkumar K, Boyle NG. Cardiac magnetic resonance imaging using wideband sequences in patients with nonconditional cardiac implanted electronic devices. Heart Rhythm. 2018;15:218–25.

    Article  Google Scholar 

  25. Hilbert S, Weber A, Nehrke K, Börnert P, Schnackenburg B, Oebel S, Spampinato R, Rogge C, Richter S, Hindricks G, et al. Artefact-free late gadolinium enhancement imaging in patients with implanted cardiac devices using a modified broadband sequence: current strategies and results from a real-world patient cohort. Europace. 2018;20:801–7.

    Article  Google Scholar 

  26. Ibrahim EH, Runge M, Stojanovska J, Agarwal P, Ghadimi-Mahani M, Attili A, Chenevert T, den Harder C, Bogun F. Optimized cardiac magnetic resonance imaging inversion recovery sequence for metal artifact reduction and accurate myocardial scar assessment in patients with cardiac implantable electronic devices. World J Radiol. 2018;10:100–7.

    Article  Google Scholar 

  27. Ferreira VM, Piechnik SK, Dall’Armellina E, Karamitsos TD, Francis JM, Ntusi N, Holloway C, Choudhury RP, Kardos A, Robson MD, Friedrich MG. Native T1-mapping detects the location, extent and patterns of acute myocarditis without the need for gadolinium contrast agents. 2014;16:1–11.

  28. Puntmann VO, Carr-White G, Jabbour A, Yu CY, Gebker R, Kelle S, Rolf A, Zitzmann S, Peker E, D’Angelo T, Pathan F. Native T1 and ECV of noninfarcted myocardium and outcome in patients with coronary artery disease. 2018;71:766–78.

  29. Nadjiri J, Nieberler H, Hendrich E, Greiser A, Will A, Martinoff S, Hadamitzky M. Performance of native and contrast-enhanced T1 mapping to detect myocardial damage in patients with suspected myocarditis: a head-to-head comparison of different cardiovascular magnetic resonance techniques. 2017;33:539–47.

  30. Ferreira VM, Piechnik SK, Dall'Armellina E, Karamitsos TD, Francis JM, Ntusi N, Holloway C, Choudhury RP, Kardos A, Robson MD, Friedrich MG. T1 mapping for the diagnosis of acute myocarditis using CMR: comparison to T2-weighted and late gadolinium enhanced imaging. 2013;6:1048–58.

  31. Messroghli DR, Radjenovic A, Kozerke S, Higgins DM, Sivananthan MU, Ridgway JP. Modified Look-Locker inversion recovery (MOLLI) for high-resolution T1 mapping of the heart. Magn Reson Med. 2004;52:141–6.

    Article  Google Scholar 

  32. Robson MD, Piechnik SK, Tunnicliffe EM, Neubauer S. T1 measurements in the human myocardium: the effects of magnetization transfer on the SASHA and MOLLI sequences. Magn Reson Med. 2013;70:664–70.

    Article  CAS  Google Scholar 

  33. Vassiliou VS, Wassilew K, Cameron D, Heng EL, Nyktari E, Asimakopoulos G, de Souza A, Giri S, Pierce I, Jabbour A, et al. Identification of myocardial diffuse fibrosis by 11 heartbeat MOLLI T. MAGMA. 2018;31:101–13.

    Article  CAS  Google Scholar 

  34. Iles L, Pfluger H, Phrommintikul A, Cherayath J, Aksit P, Gupta SN, Kaye DM, Taylor AJ. Evaluation of diffuse myocardial fibrosis in heart failure with cardiac magnetic resonance contrast-enhanced T1 mapping. J Am Coll Cardiol. 2008;52:1574–80.

    Article  Google Scholar 

  35. Messroghli DR, Moon JC, Ferreira VM, Grosse-Wortmann L, He T, Kellman P, Mascherbauer J, Nezafat R, Salerno M, Schelbert EB, Taylor AJ. Clinical recommendations for cardiovascular magnetic resonance mapping of T1, T2, T2* and extracellular volume: a consensus statement by the Society for Cardiovascular Magnetic Resonance (SCMR) endorsed by the European Association for Cardiovascular Imaging (EACVI). 2017;19:75.

  36. Bull S, White SK, Piechnik SK, Flett AS, Ferreira VM, Loudon M, Francis JM, Karamitsos TD, Prendergast BD, Robson MD, et al. Human non-contrast T1 values and correlation with histology in diffuse fibrosis. Heart. 2013;99:932–7.

    Article  Google Scholar 

  37. Sibley CT, Noureldin RA, Gai N, Nacif MS, Liu S, Turkbey EB, Mudd JO, van der Geest RJ, Lima JA, Halushka MK, et al. T1 Mapping in cardiomyopathy at cardiac MR: comparison with endomyocardial biopsy. Radiology. 2012;265:724–32.

    Article  Google Scholar 

  38. Hamilton-Craig CR, Strudwick MW, Galloway GJ. Mapping for myocardial fibrosis by cardiac magnetic resonance relaxometry-a comprehensive technical review. Front Cardiovasc Med. 2016;3:49.

    Google Scholar 

  39. Diao KY, Yang ZG, Xu HY, Liu X, Zhang Q, Shi K, Jiang L, Xie LJ, Wen LY, Guo YK. Histologic validation of myocardial fibrosis measured by T1 mapping: a systematic review and meta-analysis. J Cardiovasc Magn Reson. 2016;18:92.

    Article  Google Scholar 

  40. Nacif MS, Turkbey EB, Gai N, Nazarian S, van der Geest RJ, Noureldin RA, Sibley CT, Ugander M, Liu S, Arai AE, et al. Myocardial T1 mapping with MRI: comparison of look-locker and MOLLI sequences. J Magn Reson Imaging. 2011;34:1367–73.

    Article  Google Scholar 

  41. Fitts M, Breton E, Kholmovski EG, Dosdall DJ, Vijayakumar S, Hong KP, Ranjan R, Marrouche NF, Axel L, Kim D. Arrhythmia insensitive rapid cardiac T1 mapping pulse sequence. Magn Reson Med. 2013;70:1274–82.

    Article  Google Scholar 

  42. Piechnik SK, Ferreira VM, Dall'Armellina E, Cochlin LE, Greiser A, Neubauer S, Robson MD. Shortened modified Look-Locker inversion recovery (ShMOLLI) for clinical myocardial T1-mapping at 1.5 and 3 T within a 9 heartbeat breathhold. J Cardiovasc Magn Reson 2010;12:69.

  43. Roujol S, Weingärtner S, Foppa M, Chow K, Kawaji K, Ngo LH, Kellman P, Manning WJ, Thompson RB, Nezafat R. Accuracy, precision, and reproducibility of four T1 mapping sequences: a head-to-head comparison of MOLLI, ShMOLLI, SASHA, and SAPPHIRE. Radiology. 2014;272:683–9.

    Article  Google Scholar 

  44. Kellman P, Herzka DA, Arai AE, Hansen MS. Influence of Off-resonance in myocardial T1-mapping using SSFP based MOLLI method. J Cardiovasc Magn Reson. 2013;15:63.

    Article  Google Scholar 

  45. Kellman P, Herzka DA, Hansen MS. Adiabatic inversion pulses for myocardial T1 mapping. Magn Reson Med. 2014;71:1428–34.

    Article  Google Scholar 

  46. Chow K, Flewitt JA, Green JD, Pagano JJ, Friedrich MG, Thompson RB. Saturation recovery single-shot acquisition (SASHA) for myocardial T(1) mapping. Magn Reson Med. 2014;71:2082–95.

    Article  Google Scholar 

  47. Heidenreich JF, Weng AM, Donhauser J, Greiser A, Chow K, Nordbeck P, Bley TA, Köstler H. T1- and ECV-mapping in clinical routine at 3 T: differences between MOLLI. ShMOLLI and SASHA BMC Med Imaging. 2019;19:59.

    Article  Google Scholar 

  48. Teixeira T, Hafyane T, Stikov N, Akdeniz C, Greiser A, Friedrich MG. Comparison of different cardiovascular magnetic resonance sequences for native myocardial T1 mapping at 3T. J Cardiovasc Magn Reson. 2016;18:65.

    Article  Google Scholar 

  49. Shao J, Rashid S, Renella P, Nguyen KL, Hu P. Myocardial T1 mapping for patients with implanted cardiac devices using wideband inversion recovery spoiled gradient echo readout. Magn Reson Med. 2017;77:1495–504.

    Article  Google Scholar 

  50. Shao J, Rapacchi S, Nguyen KL, Hu P. Myocardial T1 mapping at 3.0 tesla using an inversion recovery spoiled gradient echo readout and bloch equation simulation with slice profile correction (BLESSPC) T1 estimation algorithm. J Magn Reson Imaging. 2016;43:414–25.

    Article  Google Scholar 

  51. Weingärtner S, Akçakaya M, Basha T, Kissinger KV, Goddu B, Berg S, Manning WJ, Nezafat R. Combined saturation/inversion recovery sequences for improved evaluation of scar and diffuse fibrosis in patients with arrhythmia or heart rate variability. Magn Reson Med. 2014;71:1024–34.

    Article  Google Scholar 

  52. Puntmann VO, Valbuena S, Hinojar R, Petersen SE, Greenwood JP, Kramer CM, Kwong RY, McCann GP, Berry C, Nagel E. Society for Cardiovascular Magnetic Resonance (SCMR) expert consensus for CMR imaging endpoints in clinical research: part I-analytical validation and clinical qualification. J Cardiovasc Magn Reson. 2018;20:1–23.

    Article  Google Scholar 

  53. Ibanez B, Aletras AH, Arai AE, Arheden H, Bax J, Berry C, Bucciarelli-Ducci C, Croisille P, Dall'Armellina E, Dharmakumar R, Eitel I. Cardiac MRI endpoints in myocardial infarction experimental and clinical trials: JACC scientific expert panel. 2019;74:238–56.

Download references

Funding

This work is supported by an American Heart Association Collaborative Sciences Award 19CSL0134580004, and funding from the VCU Pauley Heart Center and the VCU Wright Center for Clinical & Translation Research (CCTR) Clinical and Translational Science Award (CTSA) UL1TR002649.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jennifer H. Jordan.

Ethics declarations

Conflict of Interest

The authors have no conflicts of interest to disclose.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Myocardial Disease

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zaman, A., Zhao, S., Kron, J. et al. Role of Cardiac MRI Imaging of Focal and Diffuse Inflammation and Fibrosis in Cardiomyopathy Patients Who Have Pacemakers/ICD Devices. Curr Cardiol Rep 24, 1529–1536 (2022). https://doi.org/10.1007/s11886-022-01770-w

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11886-022-01770-w

Keywords

Navigation