Volume 56, Issue 3 pp. 779-789

Research Article

A Radiomic MRI based Nomogram for Prediction of Heart Failure with Preserved Ejection Fraction in Systemic Lupus Erythematosus Patients: Insights From a Three-Center Prospective Study

Lian-Ming Wu MD, PhD,

Lian-Ming Wu MD, PhD

orcid.org/0000-0001-7381-5436

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Ruo-Yang Shi MD, PhD,

Ruo-Yang Shi MD, PhD

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Chong-Wen Wu MD,

Chong-Wen Wu MD

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Meng Jiang MD, PhD,

Meng Jiang MD, PhD

Department of Cardiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Qiang Guo MD, PhD,

Qiang Guo MD, PhD

Department of Rheumatology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Yin-Su Zhu MD,

Yin-Su Zhu MD

Department of Radiology, The First Affiliated Hospital of Nanjing Medical University, Nan Jing, Jiang Su, 210029 China

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Lang-Lang Tang MD,

Lang-Lang Tang MD

Department of Radiology, Longyan First Hospital of Fujian Medical University, Long Yan, Fu Jian, 364031 China

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Jian-Rong Xu MD, PhD,

Jian-Rong Xu MD, PhD

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Jun Pu MD, PhD,

Jun Pu MD, PhD

Department of Cardiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Yan Zhou MD, PhD,

Corresponding Author

Yan Zhou MD, PhD

[email protected]

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

Address reprint requests to: Y.Z., Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, No. 160 Pu Jian Road, Shanghai, 200127, China. E-mail: [email protected] or R.W., Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, No. 160 Pu Jian Road, Shanghai, 200127, China. E-mail: [email protected].

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Rui Wu MD, PhD,

Corresponding Author

Rui Wu MD, PhD

[email protected]

orcid.org/0000-0002-7235-8955

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Lian-Ming Wu MD, PhD,

Lian-Ming Wu MD, PhD

orcid.org/0000-0001-7381-5436

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Ruo-Yang Shi MD, PhD,

Ruo-Yang Shi MD, PhD

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Chong-Wen Wu MD,

Chong-Wen Wu MD

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Meng Jiang MD, PhD,

Meng Jiang MD, PhD

Department of Cardiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Qiang Guo MD, PhD,

Qiang Guo MD, PhD

Department of Rheumatology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Yin-Su Zhu MD,

Yin-Su Zhu MD

Department of Radiology, The First Affiliated Hospital of Nanjing Medical University, Nan Jing, Jiang Su, 210029 China

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Lang-Lang Tang MD,

Lang-Lang Tang MD

Department of Radiology, Longyan First Hospital of Fujian Medical University, Long Yan, Fu Jian, 364031 China

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Jian-Rong Xu MD, PhD,

Jian-Rong Xu MD, PhD

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Jun Pu MD, PhD,

Jun Pu MD, PhD

Department of Cardiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Yan Zhou MD, PhD,

Corresponding Author

Yan Zhou MD, PhD

[email protected]

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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Rui Wu MD, PhD,

Corresponding Author

Rui Wu MD, PhD

[email protected]

orcid.org/0000-0002-7235-8955

Department of Radiology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200127 China

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First published: 20 January 2022

https://doi.org/10.1002/jmri.28070

Lian-Ming Wu and Ruo-Yang Shi contributed equally to the paper.

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Abstract

Background

Myocardial T1 and extracellular volume (ECV) fraction values have important roles in the prognostication of heart failure with preserved ejection fraction (HFpEF). However, the traditional mean quantification of intensity levels is not sufficient.

Purpose

To evaluate a T1 map-based radiomic nomogram as a long-term prognosticator for HFpEF in systemic lupus erythematosus (SLE) patients.

Study Type

Prospective.

Population

A total of 115 SLE patients and 50 age- and gender-matched controls.

Field Strength/Sequence

A 3.0 T scanner; cine imaging, precontrast and post-contrast T1 mapping and T2 mapping sequences.

Assessment

A radiomic nomogram was developed based on precontrast T1 mapping. Three independent readers assessed and compared the ECV value and the value of the radiomic nomogram for predicting HFpEF in SLE patients.

Statistical Test

Cox proportional hazard models, Youden index for determining cut-off values for high HFpEF risk vs. low HFpEF risk classification, Kaplan–Meier analysis, intraclass correlation (ICC), and Uno C statistic test.

Results

During a median follow-up of 27 (interquartile range, 19–37) months, 31 SLE patients developed HFpEF. Patients with elevated ECV (≥31%) and a higher output (≥42.7) from the radiomic feature “S_33_sum average” of the precontrast T1 map had a significantly higher risk of developing HFpEF than those who had lower ECV (<31%) and an output <42.7. Patients with a higher “S_33_sum average” value on precontrast T1 map had a significantly increased risk for HFpEF (hazard ratio, 1.363, 95% CI, 1.130–1.645), after adjusting for covariates including ECV and LVEF. Finally, “S_33_sum average” from precontrast T1 mapping had modest but significantly incremental prognostic value over the mean ECV value (Uno C statistic comparing models, 0.860 vs. 0.835).

Data Conclusion

The precontrast T1 map-based radiomic nomogram, as a measure of diffuse myocardial fibrosis was associated with HFpEF and provided modest prognostic value for predicting HFpEF in SLE patients.

Evidence Level

Technical Efficacy

Stage 2

Supporting Information

References

1Bengtsson C, Ohman ML, Nived O, Rantapaa DS. Cardiovascular event in systemic lupus erythematosus in northern Sweden: Incidence and predictors in a 7-year follow-up study. Lupus 2012; 21: 452-459.
10.1177/0961203311425524
CAS PubMed Web of Science® Google Scholar
2Palmieri V, Migliaresi P, Orefice M, et al. High prevalence of subclinical cardiovascular abnormalities in patients with systemic lupus erythematosus in spite of a very low clinical damage index. Nutr Metab Cardiovasc Dis 2009; 19: 234-240.
10.1016/j.numecd.2008.09.009
CAS PubMed Web of Science® Google Scholar
3Manzi S, Meilahn EN, Rairie JE, et al. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: Comparison with the Framingham study. Am J Epidemiol 1997; 145: 408-415.
10.1093/oxfordjournals.aje.a009122
CAS PubMed Web of Science® Google Scholar
4Kim CH, Al-Kindi SG, Jandali B, Askari AD, Zacharias M, Oliveira GH. Incidence and risk of heart failure in systemic lupus erythematosus. Heart 2017; 103: 227-233.
10.1136/heartjnl-2016-309561
PubMed Web of Science® Google Scholar
5Chang JC, Xiao R, Knight AM, Kimmel SE, Mercer-Rosa LM, Weiss PF. A population-based study of risk factors for heart failure in pediatric and adult-onset systemic lupus erythematosus. Semin Arthritis Rheum 2020; 50: 527-533.
10.1016/j.semarthrit.2020.03.019
PubMed Web of Science® Google Scholar
6Lekavich CL, Barksdale DJ, Neelon V, Wu JR. Heart failure preserved ejection fraction (HFpEF): An integrated and strategic review. Heart Fail Rev 2015; 20: 643-653.
10.1007/s10741-015-9506-7
CAS PubMed Web of Science® Google Scholar
7Yancy CW, Jessup M, Bozkurt B, et al. 2017 ACC/AHA/HFSA focused update of the 2013 ACCF/AHA guideline for the Management of Heart Failure: A report of the American College of Cardiology/American Heart Association task force on clinical practice guidelines and the Heart Failure Society of America. Circulation 2017; 136: e137-e161.
10.1161/CIR.0000000000000509
PubMed Web of Science® Google Scholar
8Steinberg BA, Zhao X, Heidenreich PA, et al. Trends in patients hospitalized with heart failure and preserved left ventricular ejection fraction: Prevalence, therapies, and outcomes. Circulation 2012; 126: 65-75.
10.1161/CIRCULATIONAHA.111.080770
PubMed Web of Science® Google Scholar
9Shah SJ, Katz DH, Selvaraj S, et al. Phenomapping for novel classification of heart failure with preserved ejection fraction. Circulation 2015; 131: 269-279.
10.1161/CIRCULATIONAHA.114.010637
PubMed Web of Science® Google Scholar
10Kao DP, Lewsey JD, Anand IS, et al. Characterization of subgroups of heart failure patients with preserved ejection fraction with possible implications for prognosis and treatment response. Eur J Heart Fail 2015; 17: 925-935.
10.1002/ejhf.327
PubMed Web of Science® Google Scholar
11Gartshteyn Y, Tamargo M, Fleischer S, et al. Endomyocardial biopsies in the diagnosis of myocardial involvement in systemic lupus erythematosus. Lupus 2020; 29: 199-204.
10.1177/0961203319897116
CAS PubMed Web of Science® Google Scholar
12Guo Q, Wu LM, Wang Z, et al. Early detection of silent myocardial impairment in drug-naive patients with new-onset systemic lupus erythematosus: A three-center prospective study. Arthritis Rheumatol 2018; 70: 2014-2024.
10.1002/art.40671
CAS PubMed Web of Science® Google Scholar
13Puntmann VO, D'Cruz D, Smith Z, et al. Native myocardial T1 mapping by cardiovascular magnetic resonance imaging in subclinical cardiomyopathy in patients with systemic lupus erythematosus. Circ Cardiovasc Imaging 2013; 6: 295-301.
10.1161/CIRCIMAGING.112.000151
PubMed Web of Science® Google Scholar
14Omori T, Nakamori S, Fujimoto N, et al. Myocardial native T1 predicts load-independent left ventricular chamber stiffness in patients with HFpEF. JACC Cardiovasc Imaging 2020; 13: 2117-2128.
10.1016/j.jcmg.2020.05.030
PubMed Web of Science® Google Scholar
15Rommel KP, von Roeder M, Latuscynski K, et al. Extracellular volume fraction for characterization of patients with heart failure and preserved ejection fraction. J Am Coll Cardiol 2016; 67: 1815-1825.
10.1016/j.jacc.2016.02.018
PubMed Web of Science® Google Scholar
16Gillies RJ, Kinahan PE, Hricak H. Radiomics: Images are more than pictures they are data. Radiology 2016; 278: 563-577.
10.1148/radiol.2015151169
PubMed Web of Science® Google Scholar
17Baessler B, Luecke C, Lurz J, et al. Cardiac MRI and texture analysis of myocardial T1 and T2 maps in myocarditis with acute versus chronic symptoms of heart failure. Radiology 2019; 292: 608-617.
10.1148/radiol.2019190101
PubMed Web of Science® Google Scholar
18Cheng S, Fang M, Cui C, et al. LGE-CMR-derived texture features reflect poor prognosis in hypertrophic cardiomyopathy patients with systolic dysfunction: Preliminary results. Eur Radiol 2018; 28: 4615-4624.
10.1007/s00330-018-5391-5
PubMed Web of Science® Google Scholar
19Baessler B, Luecke C, Lurz J, et al. Cardiac MRI texture analysis of T1 and T2 maps in patients with Infarctlike acute myocarditis. Radiology 2018; 289: 357-365.
10.1148/radiol.2018180411
PubMed Web of Science® Google Scholar
20Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997; 40: 1725.
10.1002/art.1780400928
CAS PubMed Web of Science® Google Scholar
21Messroghli 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: 141-146.
10.1002/mrm.20110
PubMed Web of Science® Google Scholar
22Flett AS, Hayward MP, Ashworth MT, et al. Equilibrium contrast cardiovascular magnetic resonance for the measurement of diffuse myocardial fibrosis: Preliminary validation in humans. Circulation 2010; 122: 138-144.
10.1161/CIRCULATIONAHA.109.930636
PubMed Web of Science® Google Scholar
23Szczypiński PM, Strzelecki M, Materka A, Klepaczko A. MaZda--a software package for image texture analysis. Comput Methods Programs Biomed 2009; 94: 66-76.
10.1016/j.cmpb.2008.08.005
PubMed Web of Science® Google Scholar
24Xu JW, Suzuki K. Max-AUC feature selection in computer-aided detection of polyps in CT colonography. IEEE J Biomed Health Inform 2014; 18: 585-593.
10.1109/JBHI.2013.2278023
PubMed Web of Science® Google Scholar
25Baessler B, Mannil M, Oebel S, Maintz D, Alkadhi H, Manka R. Subacute and chronic left ventricular myocardial scar: Accuracy of texture analysis on nonenhanced cine MR images. Radiology 2018; 286: 103-112.
10.1148/radiol.2017170213
PubMed Web of Science® Google Scholar
26Paulus WJ, Tschöpe C, Sanderson JE, et al. How to diagnose diastolic heart failure: A consensus statement on the diagnosis of heart failure with normal left ventricular ejection fraction by the heart failure and echocardiography associations of the European Society of Cardiology. Eur Heart J 2007; 28: 2539-2550.
10.1093/eurheartj/ehm037
PubMed Web of Science® Google Scholar
27Pencina MJ, D'Agostino RB, Pencina KM, Janssens AC, Greenland P. Interpreting incremental value of markers added to risk prediction models. Am J Epidemiol 2012; 176: 473-481.
10.1093/aje/kws207
PubMed Web of Science® Google Scholar
28Borbely A, van der Velden J, Papp Z, et al. Cardiomyocyte stiffness in diastolic heart failure. Circulation 2005; 111: 774-781.
10.1161/01.CIR.0000155257.33485.6D
PubMed Web of Science® Google Scholar
29van Heerebeek L, Borbely A, Niessen HW, et al. Myocardial structure and function differ in systolic and diastolic heart failure. Circulation 2006; 113: 1966-1973.
10.1161/CIRCULATIONAHA.105.587519
PubMed Web of Science® Google Scholar
30van Heerebeek L, Hamdani N, Falcao-Pires I, et al. Low myocardial protein kinase G activity in heart failure with preserved ejection fraction. Circulation 2012; 126: 830-839.
10.1161/CIRCULATIONAHA.111.076075
CAS PubMed Web of Science® Google Scholar
31Zile MR, Baicu CF, Ikonomidis JS, et al. Myocardial stiffness in patients with heart failure and a preserved ejection fraction: Contributions of collagen and titin. Circulation 2015; 131: 1247-1259.
10.1161/CIRCULATIONAHA.114.013215
CAS PubMed Web of Science® Google Scholar
32Duca F, Kammerlander AA, Zotter-Tufaro C, et al. Interstitial fibrosis, functional status, and outcomes in heart failure with preserved ejection fraction: Insights from a prospective cardiac magnetic resonance imaging study. Circ Cardiovasc Imaging 2016; 9:e005277.
10.1161/CIRCIMAGING.116.005277
PubMed Web of Science® Google Scholar
33Su MY, Lin LY, Tseng YH, et al. CMR-verified diffuse myocardial fibrosis is associated with diastolic dysfunction in HFpEF. JACC Cardiovasc Imaging 2014; 7: 991-997.
10.1016/j.jcmg.2014.04.022
PubMed Web of Science® Google Scholar
34Schelbert EB, Fridman Y, Wong TC, et al. Temporal relation between myocardial fibrosis and heart failure with preserved ejection fraction: Association with baseline disease severity and subsequent outcome. JAMA Cardiol 2017; 2: 995-1006.
10.1001/jamacardio.2017.2511
PubMed Web of Science® Google Scholar
35Roy C, Slimani A, de Meester C, et al. Associations and prognostic significance of diffuse myocardial fibrosis by cardiovascular magnetic resonance in heart failure with preserved ejection fraction. J Cardiovasc Magn Reson 2018; 20: 55.
10.1186/s12968-018-0477-4
PubMed Web of Science® Google Scholar
36Kanagala P, Cheng ASH, Singh A, et al. Relationship between focal and diffuse fibrosis assessed by CMR and clinical outcomes in heart failure with preserved ejection fraction. JACC Cardiovasc Imaging 2019; 12: 2291-2301.
10.1016/j.jcmg.2018.11.031
PubMed Web of Science® Google Scholar
37Neisius U, El-Rewaidy H, Nakamori S, Rodriguez J, Manning WJ, Nezafat R. Radiomic analysis of myocardial native T(1) imaging discriminates between hypertensive heart disease and hypertrophic cardiomyopathy. JACC Cardiovasc Imaging 2019; 12: 1946-1954.
10.1016/j.jcmg.2018.11.024
PubMed Web of Science® Google Scholar
38Kotu LP, Engan K, Borhani R, et al. Cardiac magnetic resonance image-based classification of the risk of arrhythmias in post-myocardial infarction patients. Artif Intell Med 2015; 64: 205-215.
10.1016/j.artmed.2015.06.001
PubMed Web of Science® Google Scholar
39Amano Y, Suzuki Y, Yanagisawa F, Omori Y, Matsumoto N. Relationship between extension or texture features of late gadolinium enhancement and ventricular Tachyarrhythmias in hypertrophic cardiomyopathy. Biomed Res Int 2018; 2018:4092469.
10.1155/2018/4092469
PubMed Web of Science® Google Scholar

Volume56, Issue3

September 2022

Pages 779-789

Filename	Description
jmri28070-sup-0001-Tables.docxWord 2007 document , 19.7 KB	Table S1 Supporting information
jmri28070-sup-0002-supinfo.docxWord 2007 document , 15.6 KB	Appendix S1: Supporting information

A Radiomic MRI based Nomogram for Prediction of Heart Failure with Preserved Ejection Fraction in Systemic Lupus Erythematosus Patients: Insights From a Three-Center Prospective Study

Abstract

Background

Purpose

Study Type

Population

Field Strength/Sequence

Assessment

Statistical Test

Results

Data Conclusion

Evidence Level

Technical Efficacy

Supporting Information

References

References

Information

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A Radiomic MRI based Nomogram for Prediction of Heart Failure with Preserved Ejection Fraction in Systemic Lupus Erythematosus Patients: Insights From a Three-Center Prospective Study

Abstract

Background

Purpose

Study Type

Population

Field Strength/Sequence

Assessment

Statistical Test

Results

Data Conclusion

Evidence Level

Technical Efficacy

Supporting Information

References

References

Related

Information