Research Presentation Session: Cardiac

RPS 203 - Strain analysis in cardiac MRI

February 28, 09:30 - 11:00 CET

6 min
Moderator introduction
Ursula Reiter, Graz / Austria
7 min
The additive effects of coronary obstruction on right ventricular diastolic and systolic dysfunction in type 2 diabetes mellitus patients: evaluated by CMR feature tracking
Jin Wang, Chengdu / China
Author Block: J. Wang, Z-G. Yang, Y. Li, Y-K. Guo, H. Fang, W-F. Yan, Y. Jiang; Chengdu/CN
Purpose: Obstructive coronary artery disease and type 2 diabetes mellitus (T2DM) commonly coexist, and coexisting OCAD are at increased risk for adverse cardiovascular events in T2DM patients. This study aimed to investigate the impact of coronary obstruction on right ventricle (RV) systolic and diastolic function in T2DM patients, and explore independent predictors of reduced RV function.
Methods or Background: Cardiac magnetic resonance (CMR) scanning was performed on 274 T2DM patients {161 patients without OCAD [T2DM(OCAD−)] and 113 with [T2DM(OCAD+)]} and 83 control subjects. CMR-derived parameters, including RV structure, function, global strains [including systolic peak strain (PS), peak systolic (PSSR) and diastolic strain rate (PDSR) in radial, circumferential and longitudinal directions] were measured and compared among observed groups. Univariable and multivariable linear regression analyses were performed to identify independent predictors of RV dysfunction.
Results or Findings: Compared to the control subjects, T2DM (OCAD-) patients exhibited reduced RV systolic and diastolic function, as evidenced by a decrease in all RV global strains except for radial PS, PSSR, and PDSR (all P < 0.05). T2DM(OCAD+) patients showed a significantly more severe impairment of RV systolic and diastolic function than T2DM(OCAD−) patients and control subjects (all P < 0.05). The presence of OCAD was independently correlated with reduced GCPS ( β = −0.149, P < 0.05), the radial ( β = −0.204, P < 0.001) and the longitudinal PS ( β = −0.155, P < 0.05) in the context of T2DM. Among T2DM(OCAD+) patients, Gensini score was associated with decreased GCPS (β=−0.388, P < 0.001).
Conclusion: In the context of T2DM, coronary artery obstruction exacerbated RV diastolic and systolic dysfunction. The presence of OCAD and Gensini score were independent predictors of decreased RV function.
Limitations: Not applicable
Funding for this study: No funding was obtained for this study.
Has your study been approved by an ethics committee? Not applicable
Ethics committee - additional information: Not applicable
7 min
Preoperative left atrial strain predicts outcome in patients with HOCM after myectomy
Shujuan Yang, Beijing / China
Author Block: S. Yang, S. Zhao, S. Wang; Beijing/CN
Purpose: This study aims to investigate the prognostic value of preoperative FT-derived LA strain among patients with HOCM following septal myectomy.
Methods or Background: In this retrospective, single-center study, 802 adult patients with HOCM who underwent septal myectomy from January 2010 through December 2017 were included. All patients underwent preoperative CMR with complete clinical outcome follow-up. Preoperative LA phasic strains were measured using CMR-FT. Primary endpoint included all-cause mortality, heart transplantation, unscheduled hospitalization for heart failure, and stroke. Secondary endpoint included all-cause mortality and heart transplantation.
Results or Findings: Of the 802 patients in this study, 116 experienced primary endpoints, 38 experienced secondary endpoints, and 18 experienced SCD/aborted SCD during a median follow-up of 56.7 (IQR, 40.2-78.6) months. LA reservoir strain held the best performance for predicting the occurrence of adverse outcomes. Compared with the group with LA reservoir strain > 22.9% (median), the annual event rate of primary endpoint(4.2% vs. 1.7%, P < .0001), secondary endpoint (1.5% vs. 0.4%, P =.0005), and sudden cardiac death (SCD) (0.7% vs. 0.2%, P = .047) was significantly higher in the group with LA reservoir strain ≤ 22.9%. In multivariable Cox proportional hazards regression analysis, LA reservoir strain≤22.9% was independently associated with primary endpoint (HR 1.98, 95%CI 1.26-3.11, P=.003) and secondary endpoint(HR 3.71, 95%CI 1.73-7.92, P=.001). Incorporating LA reservoir strain, the performance of the 2014 HCM Risk-SCD score improved for sudden cardiac death prediction (C-statistic: from 0.62 to 0.69; log-likelihood: from -110.31 to -108.27, P=.04).
Conclusion: In patients with HOCM undergoing septal myectomy, reduced preoperative LA reservoir strain assessed by CMR-FT is independently associated with postoperative adverse outcomes.
Limitations: Selection bias and referral bias might be induced in this observational study.
Funding for this study: This study is supported by grants from the National Key Research and Development Program of China (No. 2021YFF0501404, No. 2021YFF0501400) and the key projects of the National Natural Science Foundation of China (No. 81930044).
Has your study been approved by an ethics committee? Yes
Ethics committee - additional information: The study complied with the Declaration of Helsinki and was approved by the institutional review boards of Fuwai Hospital.
7 min
Subacute and convalescent phases of Takotsubo syndrome: CMR Feature-Tracking evaluation of left atrial and ventricular involvement
Giacomo Carlo Pambianchi, Rome / Italy
Author Block: G. C. Pambianchi, L. Ruoli, G. Cundari, L. Marchitelli, C. Catalano, N. Galea; Rome/IT
Purpose: The aim of this study was to evaluate the ventricular and atrial contractile dysfunction during the subacute and convalescent phases of Takotsubo (TTS), assessing myocardial strain by Cardiac Magnetic Resonance Feature-Tracking technique (CMR-FT).
Methods or Background: We retrospectively selected 50 patients with clinical-radiological diagnoses of TTS who underwent CMR within 30 days since the onset of specific symptoms; 19 patients were studied during the subacute phase (saTTS: ≤7 days) and 31 during the convalescence (cTTS: 8–30 days). We measured the left ventricular (LV) longitudinal, circumferential, radial systolic strain (lvGLS, lvGCS, lvGRS), the left atrial (LA) reservoir (laS_r), conduit (laS_cd), and booster pump strain (laS_bp). CMR parameters were compared with those of 30 healthy subjects.
Results or Findings: All the patients were female (100%), with a mean age of 69±13 years for TTS and 63±11 years for controls. When compared to controls, TTS patients showed reduced values of LV and LA strain parameters (p<0.05 for all). The saTTS showed increased laS_bp (12.7±2.6% vs 9.8±1.9%; p<0.001), reduced lvEF (47.4±11.9% vs 54.8±9.9%; p:0.028), lvGLS (-11.9±3.9% vs 14.6±3.8%; p:0.044), as compared to cTTS. The days passed from the onset of symptoms and CMR was inversely related to laS_bp (r: -0.484; p<0.001), with a direct correlation with the lvGLS (r: 0.470; p:0.001) with Pearson. In ROC analysis, laS_bp showed the best discriminatory power between saTTS and cTTS, with an AUC of 0.815 (95% CI: 0.684-0.945, p<0.001).
Conclusion: During the early phases of the TTS LA Booster Pump, function is significantly increased and gradually decreases over time. laS_bp could be an early marker of cardiac function impairment, even better the LV Strain and EF.
Limitations: The population under analysis was numerically limited and exclusively female.
CMR follow-up of the patients wasn't included in the study. Single-centre study.
Funding for this study: No funding was obtained for this study.
Has your study been approved by an ethics committee? Yes
Ethics committee - additional information: This study was approved
7 min
Impairment of left atrial and ventricular strain as early markers of myocyte dysfunction in hereditary transthyretin (h-TTR) mutation carriers
Luca Conia, Rome / Italy
Author Block: L. Conia, L. Ruoli, G. Stancanelli, G. Cundari, C. Catalano, N. Galea; Rome/IT
Purpose: The aim of the study was to investigate left atrial and ventricular contractile function and myocardial tissue characteristics by CMR in carriers of an hereditary transthyretin (h-TTR) mutation related with cardiac amyloidosis (CA) in pre-hypertrophic phase, compared with CA patients with left ventricular hypertrophy (LVH) and healthy controls.
Methods or Background: Twenty patients with definite diagnosis of CA (myocardial biopsy and/or genetic test and/or myocardial scintigraphy) and ten subjects with h-TTR mutation related to CA without LVH, who performed CMR in a 3T scanner between 2020-2023 were enrolled and compared with ten healthy age- and sex- matched controls. CMR image analysis was performed using a dedicated software (Cvi42, circle cardiovascular imaging) and LV volumes, maximal wall thickness, native-T1, LV global longitudinal (GLS), circumferential (GCS), atrial reservoir (ARS), conduit (ACS) and booster-pump (ABPS) strain were measured.
Results or Findings: Native-T1 values were higher in patients with hypertrophic CA (1348±87 ms) compared to h-TTR-mutation carriers (1227±33 ms) and healthy controls (1225±35 ms) with a p-value < 0,0003, whereas no significant difference was found between TTR-mutation carriers and healthy controls (p-value > 0,999). ARS, GLS and GCS were higher in healthy controls (respectively 25.6±2; 20.3±2; 21.9±5 %) compared to TTR-mutation carriers (respectively 22.0±4; 15.0±5; 15.5±5 %) with p-values < 0,05; there was non significant difference of ACS and ABPS between the two groups (p-value> 0,5).
Conclusion: In h-TTR mutation carriers CMR evaluation showed no significant alterations in T1 mapping values compared to healthy subjects, whereas a significant reduction was found in atrial and ventricular strain features, indicating a potential role as early markers of myocyte dysfunction.
Limitations: Small study population. Single center study. Lack of histologically evaluations in h-TTR carriers. Lack of a clinical and CMR follow-up.
Funding for this study: No funding was obtained for this study.
Has your study been approved by an ethics committee? Yes
Ethics committee - additional information: No information provided by the submitter.
7 min
Acute cardiac injury after postoperative left-sided breast cancer radiotherapy assessed by CMR feature-tracking strain
Linlin Zheng, Chengdu / China
Author Block: L. Zheng, M-X. Yang, C. Luo, J. Xu, H. Wang, J. Li, J. Zhang, P. Zhou, J. Yin; Chengdu/CN
Purpose: Chest radiotherapy could lead to cardiac toxicities; this study aims to assess the acute cardiac injury after left-side breast cancer radiotherapy using CMR feature-tracking strain.
Methods or Background: Patients treated with breast/chest-wall radiotherapy for left-side breast cancer were prospectively enrolled, and the mean heart dose (MHD) was calculated. CMR scans, consisting of cardiac cine and T2-weighted imaging, were performed within two weeks before and after radiotherapy. Left ventricular ejection fraction (LVEF), global radial strain (GRS), global circumferential strain (GCS), global longitudinal strain (GLS), and myocardial edema were analyzed by CVI 42 post-processing software.
Results or Findings: Thirty women patients aged 46±9 years were included (16 received breast radiotherapy and 14 received chest-wall radiotherapy). The MHD in all patients was 5.33 (3.13-9.19) Gy; and the MHD of chest-wall group was higher compared with that of breast group (9.65±2.05Gy vs. 3.45±1.15Gy, P<0.001). After radiotherapy, LVEF showed no significant changes but myocardial edema was observed in nine patients in the whole cohort. Compared with baseline scan, a decrease of GCS (-20.04±1.72 vs. -18.98±2.04, P=0.029) and GLS (-15.64±2.49 vs. -14.32±2.19, P=0.001) was observed in all patients after radiotherapy, while no differences of GRS were shown. In the chest-wall group, GRS [37.67±6.89 vs. 34.97 (29.95-38.49), P=0.038], GCS (-20.33±1.29 vs. -18.61±2.59, P=0.028) and GLS (-16.29±2.68 vs. -14.41±2.46, P=0.007) all demonstrated a decrease after radiotherapy; however, no change of GRS, GCS and GLS was observed in the breast group.
Conclusion: Left-side breast cancer radiotherapy could cause acute cardiac injury, which is more pronounced in patients with higher cardiac radiation dose. CMR strain allows the sensitive detection of radiation-related cardiac dysfunction soon after radiotherapy.
Limitations: The changes of left ventricular strain after radiotherapy in long-term follow-up and its clinical significance require further studies.
Funding for this study: This study was supported by National Natural Science Foundation of China (82202094) the Science and Technology Department of Sichuan Province (2022NSFSC1600)
Has your study been approved by an ethics committee? Yes
Ethics committee - additional information: The clinical protocol in this study was approved by the institutional ethics review board of our hospital.
7 min
Unveiling subclinical myocardial changes in a cohort of treatment-naive cancer population with diffuse large B-cell lymphoma (DLBCL) and breast cancer: is advanced cancer a cardiovascular syndrome?
Costanza Lisi, Milan / Italy
Author Block: C. Lisi, S. Figliozzi, F. Catapano, R. Levi, L. Monti, M. Francone; Milan/IT
Purpose: Pre-chemotherapy patients with advanced cancer may experience myocardial alterations due to inflammation and neuro-hormonal activation. These changes could serve as subclinical indicators of latent heart dysfunction, allowing for enhanced cardiotoxicity assessment and patient management. Our study sought to explore cardiac MR (CMR) potentials in shedding light on the cancer-associated uncontrolled immune activation hypothesis and to provide early biomarkers of myocardial damage.
Methods or Background: In this prospective single-center study, we examined 70 individuals, including 35 healthy controls and 35 patients with de novo DLBCL or breast cancer. All patients underwent CMR before starting chemotherapy. Univariate and multivariate analyses were performed to detect differences in myocardial tissue characterisation and functional parameters between the two groups.
Results or Findings: Significant differences were found in native T1 mapping times (p<0.01), with oncologic T1 at 998 msec vs. healthy T1 at 979.5 msec. Global longitudinal strain (GLS) values also differed significantly (p<0.01), with oncologic GLS at 15.06 and healthy GLS at 19.9. No significant differences were found in global biventricular function ad T2 mapping.
Conclusion: Advanced cancer is a multifaceted syndrome with profound involvement of the cardiovascular system. It initiates tissue inflammation, oxidative stress, and neuro-hormonal activation, resulting in substantial myocardial tissue changes. These changes manifest as myocardial fibrosis and apoptosis, potentially accounting for the increase in native T1 values and the decrease in GLS. This preliminary study underscores the importance of early tissue modifications as subclinical biomarkers of cardio-toxicity and prompts a reconsideration of the significance attributed to chemotherapy-induced myocardial alterations.
Limitations: This study is limited by its monocentric design and the relatively small sample size.
Funding for this study: No funding was obtained for this study.
Has your study been approved by an ethics committee? Not applicable
Ethics committee - additional information: No additional info was provided by the submitter.
7 min
Atrial and ventricular strain using cardiovascular magnetic resonance in the prediction of outcomes of pericarditis patients: a pilot study
Riccardo Cau, Cagliari / Italy
Author Block: R. Cau1, F. Pisu1, G. Muscogiuri2, R. Montisci1, L. Saba1; 1Cagliari/IT, 2Milan/IT
Purpose: The aims of our study were to explore with cardiovascular magnetic resonance (CMR) the impact of left atrial (LA) and ventricular myocardial strain in patients with acute pericarditis and to investigate their possible prognostic significance for adverse outcomes.
Methods or Background: In this retrospective study, 33 consecutive patients with acute pericarditis were studied with CMR. The primary endpoint was the combination of recurrent pericarditis, constrictive pericarditis, and surgery for pericardial diseases defined as pericardial events. Atrial and ventricular strain functions were performed on conventional cine SSFP sequences.
Results or Findings: After a median follow-up time of 16 months (interquartile range [13-24]), 11 patients (eight males) acute pericarditis patients reached the primary endpoint. In multivariable Cox regression analysis, the left atrial (LA) reservoir, LA conduit, and LA conduit strain rate parameters were all independent determinants of adverse pericardial events. Adjusted models of LA conduit and LA reservoir showed strong predictive performance, achieving significantly higher time-dependent AUCs than the LA conduit rate-based model (0.848 [95% CI, 0.7 – 1.0] and 0.851 [95% CI, 0.69 – 1.0], P < 0.05), for outcome prediction at 12 months.
Conclusion: LA reservoir and conduit mechanisms on CMR are independent predictor in patients with acute pericarditis. Including atrial strain parameters in the management of acute pericarditis may improve risk stratification.
Limitations: Retrospective single-center study
Funding for this study: No funding was obtained for this study.
Has your study been approved by an ethics committee? Yes
Ethics committee - additional information: This study was ethically approved by the IRB.
7 min
Atrial and ventricular involvement in acute myocarditis patients with preserved ejection fraction
Riccardo Cau, Cagliari / Italy
Author Block: R. Cau1, F. Pisu1, G. Muscogiuri2, J. S. Suri3, R. Montisci1, L. Saba1; 1Cagliari/IT, 2Milan/IT, 3Roseville, CA/US
Purpose: To evaluate ventricular and atrial strain parameters using cardiovascular magnetic resonance (CMR) in patients with acute myocarditis (AM) and preserved ejection fraction (EF) in comparison with control subjects.
Methods or Background: This retrospective study collected 126 consecutive patients (99 males, 27 females; mean age of 44.72 ± 18.22 years) with AM that fulfilled the Lake Louise criteria and with preserved EF and 52 age- and sex-matched control subjects. Left atrial (LA) and left ventricular (LV) strain functions were assessed on conventional cine SSFP sequences.
Results or Findings: AM patients with preserved ejection fraction had impaired global longitudinal strain (LS), global radical strain (RS), and global circumferential strain (CS) in comparison with control subjects. LA reservoir and conduit were significantly reduced in the myocarditis group compared to the control group. In cardiovascular risk factors-adjusted multivariable analysis, atrial and ventricular strain mechanisms remained significantly impaired in patients with AM with preserved EF compared to control subjects. Most importantly, a combined model of atrial and ventricular functions exhibited superior discriminatory ability when compared to base models of atrial or ventricular strain alone.
Conclusion: Besides ventricular strain parameters dysfunction, patients with AM and preserved EF demonstrated impaired reservoir and conduit mechanisms. A combined analysis of both atrial and ventricular function may improve the diagnostic accuracy for patients with AM and preserved EF.
Limitations: Retrospective single-center study
Funding for this study: No funding was obtained for this study.
Has your study been approved by an ethics committee? Yes
Ethics committee - additional information: The study was approved by the IRB.
7 min
Strain analysis using feature-tracking CMR: a predictor of cardiac involvement in hypereosinophilia patients?
Christos Vasileiou Gkizas, Lille / France
Author Block: C. V. Gkizas, B. Saal, M. Dubois, A. L. Rodriguez Musso, G. Lefevre, D. Launay, B. Longere, F. Pontana; Lille/FR
Purpose: The aim of this study was to assess the role of cardiac strain analysis using feature-tracking cardiac magnetic resonance (CMR) in patients with hypereosinophilia (HE).
Methods or Background: Sixty-one consecutive patients (aged 52±18 years, 35 males) diagnosed with HE and referred for CMR were enrolled. Based on clinical evaluations, patients were classified into a “symptomatic group, Group1” (n=20), identified by evidence suggestive of potential HE-induced cardiopathy, and a “screening group, Group2” (n=41), where CMR was executed to exclude cardiac involvement despite the absence of any other cardiac abnormality. The CMR protocol included conventional cine imaging, T1 and T2 parametric mapping, and late gadolinium enhancement (LGE) imaging. Global longitudinal strain (GLS), global circumferential strain (GCS) and global radial strain (GRS) of left ventricle (LV) were measured (cvi42, Circle Cardiovascular Imaging).
Results or Findings: Despite preserved LV ejection fraction (LVEF), GLS, GCS and GRS were decreased in both groups but were more impaired in Group1 compared to Group2 (GLS= -10.2±3.9 vs -14.5±4.2, p=0.0004; GCS= -12.0±4.1 vs -14.9±4.2, p=0.015; GRS= 17.6±9.1 vs 24.1±9.6, p=0.0165). No differences were found in all strain parameters when comparing the two different patterns of LGE (ie. myocarditis or subendocardial fibrosis).
Conclusion: In symptomatic patients, strain parameters are diminished even when the LVEF remains within the normal range. Utilising feature-tracking CMR may offer a valuable tool in the early identification of cardiac abnormalities in asymptomatic HE individuals.
Limitations: Relatively small population of patients (rare disease). No endomyocardial biopsies
Funding for this study: Authors did not receive a fund for this study
Has your study been approved by an ethics committee? Yes
Ethics committee - additional information: This study was approved by the IRB: HP1907
7 min
The additive effect of metabolic syndrome on left ventricular deformation and function in patients with obstructive coronary artery disease assessed by 3.0T cardiac magnetic resonance feature tracking
Chenyan Min, Chengdu / China
Author Block: C. Min, Y. Gao, Y. Zhigang, Y. Li; Chengdu/CN
Purpose: Metabolic syndrome (MetS) can increase the risk of morbidity and mortality of cardiovascular disease and obstructive coronary artery disease (OCAD). This study aimed to explore the impact of MetS on left ventricular (LV) deformation and function in OCAD patients and investigate the independent factors of impaired LV function and deformation.
Methods or Background: One hundred and twenty one patients with OCAD and 52 sex- and age-matched controls who underwent cardiac magnetic resonance scanning were enrolled in the study. All OCAD patients were divided into two groups: OCAD with MetS [OCAD(MetS+), n = 83] and OCAD without MetS [OCAD(MetS−), n = 38]. LV functional and global strain parameters were measured and compared among the three groups. Multivariable linear regression analyses were constructed to investigate the independent factors of LV deformation and impaired LV strain in OCAD patients. The logistic regression analysis and receiver operating characteristic curve (ROC) were performed to test the prediction efficiency of MetS for LV deformation and impaired LV strain.
Results or Findings: From controls to the OCAD(MetS-)group to the OCAD(MetS+) group, LV mass (LVM) increased, and LV global function index (LVGFI) and LV global longitudinal peak strain (GLPS) decreased (all p < 0.05). Compared with the OCAD(MetS-) group, the LV GLPS declined significantly (p=0.027), the LVM increased (p=0.006), and the LVGFI decreased (p=0.043) in the OCAD(MetS+) group. MetS was an independent factor of decreased LV GLPS (β=−0.211, p=0.002) and increased LVM (β=0.221, p=0.003). The logistic multivariate regression analysis and ROC analysis showed that combined MetS improved the efficiency of predicting LV GLPS reduction (AUC = 0.88) and LVM (AUC = 0.89) increase.
Conclusion: MetS aggravated the damage of LV deformation and function in OCAD patients and was independently associated with LV deformation and impaired LV strain.
Limitations: Not applicable
Funding for this study: No funding was obtained for this study.
Has your study been approved by an ethics committee? Not applicable
Ethics committee - additional information: Not applicable for this study.
7 min
Biventricular dysfunction and ventricular interdependence in patients with pulmonary hypertension: a 3.0 T cardiac MRI feature tracking study
Han Fang, Chengdu / China
Author Block: H. Fang, J. Li, Z-G. Yang; Chengdu/CN
Purpose: The objective of this study was to explore the right ventricular (RV) and left ventricular (LV) dysfunction and the ventricular interdependence in patients with pulmonary hypertension (PH), using cardiac MRI feature tracking (MRI-FT).
Methods or Background: One hundred and seven PH patients (mean pulmonary artery pressure >20 mm Hg) and 72 age- and sex- matched controls were recruited. Strains were compared between controls, PH patients with preserved RV ejection fractions (EF) (≥ 40%, n = 48) and PH patients with reduced RVEF (<40%, n = 59) and multivariable linear regression analysis were performed to explore the RV-LV interdependence in patients with PH.
Results or Findings: RV strain decreased sequentially from controls, through PH with preserved RVEF, to PH with reduced RVEF. PH patients with reduced RVEF had significantly lower LV strain, especially septal strain and LV peak diastolic strain rate compared with both controls and PH patients with preserved RVEF. Multivariable analyses showed that RVEF was independently correlated with LV strain, furthermore, independent of RVEF, RV strain was significantly correlated with LV strain(LVGRS: β = 0.416; LVGCS: β = −0.371; LVGLS: β = 0.283).
Conclusion: Subclinical impairment of RV function was found in PH with preserved RVEF. LV strain was impaired when RV was dysfunctional, which was associated with worsening RV strain. Therefore, while focusing on improving RV function, LV dysfunction in PH patients should also be monitored and treated early in order to slow the progression of the disease.
Limitations: First, this was a single-centre and cross-sectional study conducted in a large tertiary care hospital, and there might be potential selection bias. Second, because our study was a retrospective study, the inherent design limitations hindered our ability to consider changes in biventricular interdependence at different stages of PH.
Funding for this study: This work was supported by the 1·3·5 project for disciplines of excellence, West China Hospital, Sichuan University (ZYGD18013).
Has your study been approved by an ethics committee? Yes
Ethics committee - additional information: The current study received approval from the Biomedical Research Ethics Committee of West China Hospital, Sichuan University: 2019-648.

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