Abstract
Objectives
To explore the relationships between oxygenation signal intensity (SI) with myocardial inflammation and regional left ventricular (LV) remodeling in reperfused acute ST-segment elevation myocardial infarction (STEMI) using oxygenation-sensitive cardiovascular magnetic resonance (OS-CMR).
Methods
Thirty-three STEMI patients and 22 age- and sex-matched healthy volunteers underwent CMR. The protocol included cine function, OS imaging, precontrast T1 mapping, T2 mapping, and late gadolinium enhancement (LGE) imaging. A total of 880 LV segments were included for analysis based on the American Heart Association 16-segment model. For validation, 15 pigs (10 myocardial infarction (MI) model animals and 5 controls) received CMR and were sacrificed for immunohistochemical analysis.
Results
In the patient study, the acute oxygenation SI showed a stepwise rise among remote, salvaged, and infarcted segments compared with healthy myocardium. At convalescence, all oxygenation SI values besides those in infarcted segments with microvascular obstruction decreased to similar levels. Acute oxygenation SI was associated with early myocardial injury (T1: r = 0.38; T2: r = 0.41; all p < 0.05). Segments with higher acute oxygenation SI values exhibited thinner diastolic walls and decreased wall thickening during follow-up. Multivariable regression modeling indicated that acute oxygenation SI (β = 2.66; p < 0.05) independently predicted convalescent segment adverse remodeling (LV wall thinning). In the animal study, alterations in oxygenation SI were correlated with histological inflammatory infiltrates (r = 0.59; p < 0.001).
Conclusions
Myocardial oxygenation by OS-CMR could be used as a quantitative imaging biomarker to assess myocardial inflammation and predict convalescent segment adverse remodeling after STEMI.
Key Points
• Oxygenation signal intensity (SI) may be an imaging biomarker of inflammatory infiltration that could be used to assess the response to anti-inflammatory therapies in the future.
• Oxygenation SI early after myocardial infarction (MI) was associated with left ventricular segment injury at acute phase and could predict regional functional recovery and adverse remodeling late after acute MI.
• Oxygenation SI demonstrated a stepwise increase among remote, salvaged, and infarcted segments. Infarcted zones with microvascular obstruction demonstrated a higher oxygenation SI than those without. However, the former showed less pronounced changes over time.
Similar content being viewed by others
Abbreviations
- DWT:
-
Diastolic wall thickness
- LGE:
-
Late gadolinium enhancement
- LV:
-
Left ventricular
- MI:
-
Myocardial infarction
- MVO:
-
Microvascular obstruction
- OS-CMR:
-
Oxygenation-sensitive cardiovascular magnetic resonance
- SI:
-
Signal intensity
- STEMI:
-
ST-segment elevation myocardial infarction
- SWT:
-
Systolic wall thickness
- TR:
-
Repetition time
- Wth:
-
Wall thickening
References
Sutton MG, Sharpe N (2000) Left ventricular remodeling after myocardial infarction: pathophysiology and therapy. Circulation 101(25):2981–2988
Konstam MA, Kramer DG, Patel AR, Maron MS, Udelson JE (2011) Left ventricular remodeling in heart failure: current concepts in clinical significance and assessment. JACC Cardiovasc Imaging 4(1):98–108
Anzai T (2013) Post-infarction inflammation and left ventricular remodeling: a double-edged sword. Circ J 77(3):580–587
Frantz S, Nahrendorf M (2014) Cardiac macrophages and their role in ischaemic heart disease. Cardiovasc Res 102(2):240–248
de Waha S, Patel MR, Granger CB et al (2017) Relationship between microvascular obstruction and adverse events following primary percutaneous coronary intervention for ST-segment elevation myocardial infarction: an individual patient data pooled analysis from seven randomized trials. Eur Heart J 38(47):3502–3510
Niccoli G, Scalone G, Lerman A, Crea F (2016) Coronary microvascular obstruction in acute myocardial infarction. Eur Heart J 37(13):1024–1033
Sree Raman K, Nucifora G, Selvanayagam JB (2018) Novel cardiovascular magnetic resonance oxygenation approaches in understanding pathophysiology of cardiac diseases. Clin Exp Pharmacol Physiol 45(5):475–480
Grover S, Lloyd R, Perry R et al (2019) Assessment of myocardial oxygenation, strain, and diastology in MYBPC3-related hypertrophic cardiomyopathy: a cardiovascular magnetic resonance and echocardiography study. Eur Heart J Cardiovasc Imaging 20(8):932–938
Shah R, Parnham S, Liang Z et al (2019) Prognostic utility of oxygen-sensitive cardiac magnetic resonance imaging in diabetic and nondiabetic chronic kidney disease patients with no known coronary artery disease. JACC Cardiovasc Imaging 12(6):1107–1109
Levelt E, Rodgers CT, Clarke WT et al (2016) Cardiac energetics, oxygenation, and perfusion during increased workload in patients with type 2 diabetes mellitus. Eur Heart J 37(46):3461–3469
Luu JM, Friedrich MG, Harker J et al (2014) Relationship of vasodilator-induced changes in myocardial oxygenation with the severity of coronary artery stenosis: a study using oxygenation-sensitive cardiovascular magnetic resonance. Eur Heart J Cardiovasc Imaging 15(12):1358–1367
Mahmod M, Francis JM, Pal N et al (2014) Myocardial perfusion and oxygenation are impaired during stress in severe aortic stenosis and correlate with impaired energetics and subclinical left ventricular dysfunction. J Cardiovasc Magn Reson 16:29
Huang S, Frangogiannis NG (2018) Anti-inflammatory therapies in myocardial infarction: failures, hopes and challenges. Br J Pharmacol 175(9):1377–1400
Ibanez B, James S, Agewall S et al (2018) 2017 ESC Guidelines for the management of acute myocardial infarction in patients presenting with ST-segment elevation: the task force for the management of acute myocardial infarction in patients presenting with ST-segment elevation of the European Society of Cardiology (ESC). Eur Heart J 39(2):119–177
Yang MX, Xu HY, Zhang L et al (2021) Myocardial perfusion assessment in the infarct core and penumbra zones in an in-vivo porcine model of the acute, sub-acute, and chronic infarction. Eur Radiol 31(5):2798–2808
Ugander M, Bagi PS, Oki AJ et al (2012) Myocardial edema as detected by pre-contrast T1 and T2 CMR delineates area at risk associated with acute myocardial infarction. JACC Cardiovasc Imaging 5(6):596–603
Liu D, Borlotti A, Viliani D et al (2017) CMR native T1 mapping allows differentiation of reversible versus irreversible myocardial damage in ST-segment-elevation myocardial infarction: An OxAMI study (Oxford acute myocardial infarction). Circ Cardiovasc Imaging 10(8):e005986
Bulluck H, Hammond-Haley M, Fontana M et al (2017) Quantification of both the area-at-risk and acute myocardial infarct size in ST-segment elevation myocardial infarction using T1-mapping. J Cardiovasc Magn Reson 19(1):57
Garg P, Broadbent DA, Swoboda PP et al (2017) Extra-cellular expansion in the normal, non-infarcted myocardium is associated with worsening of regional myocardial function after acute myocardial infarction. J Cardiovasc Magn Reson 19(1):73
D’Elia N, D’hooge J, Marwick TH (2015) Association between myocardial mechanics and ischemic LV remodeling. JACC Cardiovasc Imaging 8(12):1430–1443
Anzai T (2018) Inflammatory mechanisms of cardiovascular remodeling. Circ J 82(3):629–635
Gibb AA, Hill BG (2018) Metabolic coordination of physiological and pathological cardiac remodeling. Circ Res 123(1):107–128
van Kranenburg M, Magro M, Thiele H et al (2014) Prognostic value of microvascular obstruction and infarct size, as measured by CMR in STEMI patients. JACC Cardiovasc Imaging 7(9):930–939
Robbers LF, Eerenberg ES, Teunissen PF et al (2013) Magnetic resonance imaging-defined areas of microvascular obstruction after acute myocardial infarction represent microvascular destruction and haemorrhage. Eur Heart J 34(30):2346–2353
Wu KC (2012) CMR of microvascular obstruction and hemorrhage in myocardial infarction. J Cardiovasc Magn Reson 14:68
Dall’Armellina E, Piechnik SK, Ferreira VM et al (2012) Cardiovascular magnetic resonance by noncontrast T1-mapping allows assessment of severity of injury in acute myocardial infarction. J Cardiovasc Magn Reson 14:15
Layland J, Rauhalammi S, Lee MM et al (2017) Diagnostic accuracy of 3.0-T magnetic resonance T1 and T2 mapping and T2-weighted dark-blood imaging for the infarct-related coronary artery in non-ST-segment elevation myocardial infarction. J Am Heart Assoc 6(4):e004759
Hammer-Hansen S, Ugander M, Hsu LY et al (2014) Distinction of salvaged and infarcted myocardium within the ischaemic area-at-risk with T2 mapping. Eur Heart J Cardiovasc Imaging 15(9):1048–1053
McAlindon EJ, Pufulete M, Harris JM et al (2015) Measurement of myocardium at risk with cardiovascular MR: comparison of techniques for edema imaging. Radiology 275(1):61–70
Carberry J, Carrick D, Haig C et al (2017) Persistence of infarct zone T2 hyperintensity at 6 months after acute ST-segment-elevation myocardial infarction: incidence, pathophysiology, and prognostic implications. Circ Cardiovasc Imaging 10(12):e006586
Symons R, Masci PG, Goetschalckx K, Doulaptsis K, Janssens S, Bogaert J (2015) Effect of infarct severity on regional and global left ventricular remodeling in patients with successfully reperfused ST segment elevation myocardial infarction. Radiology 274(1):93–102
Zhang L, Mandry D, Chen B et al (2018) Impact of microvascular obstruction on left ventricular local remodeling after reperfused myocardial infarction. J Magn Reson Imaging 47(2):499–510
Vadakkumpadan F, Trayanova N, Wu KC (2014) Image-based left ventricular shape analysis for sudden cardiac death risk stratification. Heart Rhythm 11(10):1693–1700
Galea N, Dacquino GM, Ammendola RM et al (2019) Microvascular obstruction extent predicts major adverse cardiovascular events in patients with acute myocardial infarction and preserved ejection fraction. Eur Radiol 29(5):2369–2377
Zaman A, Higgins DM, Motwani M et al (2015) Robust myocardial T2 and T2 * mapping at 3T using image-based shimming. J Magn Reson Imaging 41(4):1013–1020
Funding
This study has received funding by the 1–3–5 project for disciplines of excellence of West China Hospital, Sichuan University (ZYGD18013).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Guarantor
The scientific guarantor of this publication is Prof. Zhi-Gang Yang.
Conflict of Interest
The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.
Statistics and Biometry
No complex statistical methods were necessary for this paper.
Informed Consent
Written informed consent was obtained from all subjects (patients) in this study.
Ethical Approval
Institutional Review Board approval was obtained.
Methodology
• Prospective
• Experimental
• Performed at one institution
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 78.4 kb)
Rights and permissions
About this article
Cite this article
Shi, K., Ma, M., Yang, MX. et al. Increased oxygenation is associated with myocardial inflammation and adverse regional remodeling after acute ST-segment elevation myocardial infarction. Eur Radiol 31, 8956–8966 (2021). https://doi.org/10.1007/s00330-021-08032-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-021-08032-3