Diastolic Cardiac Function by MRI: History
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El-Sayed Ibrahim

Most cardiac studies focus on evaluating left ventricular (LV) systolic function. However, the assessment of diastolic cardiac function is becoming more appreciated, especially with the increasing prevalence of pathologies associated with diastolic dysfunction like heart failure with preserved ejection fraction (HFpEF). Diastolic dysfunction is an indication of abnormal mechanical properties of the myocardium, characterized by slow or delayed myocardial relaxation, abnormal LV distensibility, and/or impaired LV filling.

  • heart
  • diastolic cardiac function
  • MRI
  • HFpEF

1. Introduction

The left ventricle (LV) of the heart fills via two separate mechanisms. In early-diastole, the LV fills passively through active relaxation. In late-diastole, the remaining blood contributing to the total end-diastolic volume enters the ventricle via active contraction of the left atrium (LA). During isovolumetric relaxation, LV volume increases due to alterations in principal strains and untwisting of the ventricles [1]. Complete appreciation of impaired diastolic function as it relates to cardiovascular disease requires detailed analysis of myocardial tissue deformation during diastole, e.g., using magnetic resonance imaging (MRI) strain imaging. While diastolic shear strain rates are coupled to the prior systolic shear strain constituents, torsional recoil is independent of end-systolic factors [2].
Diastolic dysfunction is an indication of abnormal mechanical properties of the myocardium, characterized by slow or delayed myocardial relaxation, abnormal LV distensibility, and/or impaired LV filling [3]. Diastolic dysfunction has been shown to be associated with age and other cardiovascular risk factors such as hypertension and diabetes mellitus [4]. In addition, several cardiovascular diseases cause adverse LV remodeling, which leads to diastolic dysfunction. Especially, heart failure with preserved ejection fraction (HFpEF) is a clinical syndrome where patients have normal LV systolic function, and evidence of diastolic dysfunction [5]. HFpEF has distinct causes and differential pathophysiology from those with systolic heart failure and nearly 50% of patients presenting with symptoms of heart failure (HF) have diastolic dysfunction. HFpEF is more prevalent than heart failure with reduced ejection fraction (HFrEF) among women and in those with elevated systemic blood pressure [6]. Additionally, patients presenting with HFpEF suffer from vascular changes and ventricular remodeling that could affect the physiological relationships between afterload and diastole and cause ischemia induced by supply-demand imbalance [7]. Furthermore, HFpEF is correlated to substantial morbidity and mortality. Unfortunately, accurate non-invasive diagnosis of LV diastolic dysfunction remains difficult, leading to challenges in the diagnosis and treatment of HFpEF [8].
Heart catheterization is the current gold standard for demonstrating the characteristics of diastolic heart failure, but due to the risks and costs involved with invasive hemodynamic evaluation, it is not practical for the diagnosis of diastolic dysfunction. Echocardiography, with significantly less risk compared to heart catheterization, is currently the method of choice for diagnosing diastolic dysfunction. Nevertheless, echocardiography has limitations related to poor acoustic windows, geometric assumptions, suboptimal spatial resolution, and high dependency on the operator’s skills. Some of these limitations restrict the technique’s ability to accurately measure annular velocities and assess diastolic function if regional dysfunction is present [9]. Cardiac MRI measurements, however, are superior to echocardiography in accuracy for the evaluation of diastolic function. This makes cardiac MRI a valuable imaging modality for the analysis of diastolic function in patients with cardiovascular diseases such as hypertrophic cardiomyopathy, hypertension, aortic valve stenosis, coronary artery disease, and congestive heart failure [10]. Regarding this review, the authors conducted an advanced search of the PubMed database using the following keywords: cardiac/heart, MRI/magnetic resonance, diastole/diastolic, which resulted in >40 papers that are covered in this comprehensive review, where different studies are grouped based on cardiovascular diseases and implemented techniques. Table 1 summarizes key studies in which MRI was used for evaluating diastolic heart function [10].
Table 1. MRI and diastolic function: applications in cardiac disease.
Type of Disease MRI Technique n Principal Findings
HCM [11] GRE 31 Impairment of regional relaxation
HCM [12] Spectroscopy 8 Decreased PCr/ATP in symptomatic patients
HCM [13] Spectroscopy 8 Decreased PCr/ATP in asymptomatic patients
HCM [14] Tagging 17 Smaller circumferential curvatures in hypertrophy
AS [15] Tagging 12 Prolonged and delayed untwisting
AS [16] Phase contrast 9 Volumetric mitral flow correlates with Doppler
LVH [17] GRE 9 Early detection of filling abnormalities
AS [18] Tagging 13 Prolonged and delayed untwisting
Hypertensive HD [19] Spectroscopy 11 Decreased PCr/ATP correlates with impaired relaxation
Previous MI [20] Phase contrast 11 Early diastolic filling velocities correlate with Doppler
Previous MI [21] Tagging 16 Reduction of systolic strains in infarcted and remote area
Previous MI [22] Tagging 18 Nonuniform, delayed, and prolonged untwisting
CAD/previous MI [20] GRE 10/15 Reduced early diastolic long-axis velocity
Previous MI [23] Tagging 9 Reduced systolic strains in asynergic segments
Fallot [24] Phase contrast 19 Restrictive flow is associated with decreased exercise
Mustard/Senning [25] Phase contrast 12 Restrictive tricuspid flow
Fallot [26] GRE 10 Impaired ventricular filling correlates with exercise
RVPO [14] Tagging 9 Heterogeneity in strain
Single ventricle [27] Tagging 10 Regional decrease in systolic strains

AS, Aortic stenosis; ATP, adenosine triphosphate; CAD, coronary artery disease; GRE, gradient echo; HCM, hypertrophic cardiomyopathy; HD, heart disease; LVH, left ventricular hypertrophy; MI, myocardial infarction; PCr, phosphocreatine; RVPO, right ventricular pressure overload; Spectroscopy, 31P-MR spectroscopy. Table reproduced with permission from [10]. Copyright 2002 Elsevier.

2. Cardiac MRI Techniques

Different MRI techniques are currently available for evaluation of diastolic cardiac function, such as cine imaging for global function analysis, phase contrast (PC) imaging for flow analysis, and myocardial tagging for regional function analysis. Simple measurements, such as longitudinal fractional shortening, can be measured quickly and easily by MRI, which has reliably identified echocardiography-evidenced diastolic dysfunction in patients with preserved LV EF [5]. Assessment of myocardial contractility pattern using other MRI methods, such as strain-encoded (SENC), displacement encoding with stimulated echoes (DENSE), and MRI feature-tracking (MRI-FT), contribute to further evaluation of regional diastolic function. Moreover, recent advances in MRI techniques have enabled non-invasive assessment of vascular compliance and elastic properties of the vessel wall using pulse wave velocity (PWV) measurements, PC MRI, and MRI tagging. 31P magnetic resonance spectroscopy (MRS) is another technique for non-invasively quantifying the energy required for active relaxation of the myocardial tissue through calculating the ratio of myocardial phosphocreatine to adenosine triphosphate (PCr/ATP).
Global diastolic function is assessed using time-volume curves generated by tracing the epicardial and endocardial borders of the myocardium in cine MRI images throughout the cardiac cycle or from 4D flow images across atrioventricular valves (Figure 1). Studies are undergoing to create methods that would allow for efficient assessment of the diastolic cardiac function. For example, Young et al. [28] developed a three-dimensional (3D) model of cardiac function based on standard cine MRI images and showed that the developed model is equally capable of identifying diastolic dysfunction as echocardiography. The authors showed that the most useful MRI parameters for assessing LV diastolic function are E/E’ (the ratio of early-peak filling rate to early-longitudinal relaxation rate), NE (normalized early-peak filling rate, defined by early-peak filling rate divided by end-diastolic volume), and E/A (the ratio of early-peak filling rate to atrial-peak filling rate). The categorization of diastolic dysfunction was accomplished using septal and lateral measurements obtained to evaluate longitudinal shortening [29].
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Figure 1. Mitral flow analysis in (a) normal case and (b) diastolic dysfunction, showing early (E) and atrial (A) filling peaks. E/A ratio shows normal (>1) and abnormal (<1) diastolic function in normal and pathological cases, respectively. Four-dimensional (4D) flow images are shown at three timepoints in the cardiac cycle (early systole, early diastole, and late diastole), confirming the analysis findings (E & A filling peaks). White dotted line shows mitral valve plane and red arrow shows flow direction. LV, left ventricle; MV, mitral valve.

2.1. MRI Tagging

The heart function can also be studied using MRI tagging [30]. MRI tagging has advantages for evaluating diastolic heart function through excellent soft-tissue contrast and the ability to directly measure myocardial relaxation (Figure 2), in contrast to Doppler echocardiography which is load dependent and limited to indirect measures of LV function [31]. Ambale-Venkatesh et al. [32] used MRI tagging to quantify end-diastolic strain rate and strain relaxation index to predict the development of HF in patients with no prior history of cardiovascular disease. The authors used a novel index of diastolic function, the strain relaxation index, which factors in both the interval between the occurrence of peak systolic strain and post-systolic peak as well as the early-diastolic strain rate.
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Figure 2. Reduced left ventricle myocardial contractility in a rat model of lung cancer radiation therapy (experimental). Segmental circumferential strain curves in six segments (color code shown on top left) in a mid-ventricular short-axis slice in a normal rat (a) and an experimental rat (b) that received localized heart irradiation of 24 Gy. Note reduced peak systolic strain (solid arrows) and diastolic strain rate (dotted arrows) post radiation.

2.2. Complementary Spatial Modulation of Magnetization

The introduction of complementary spatial modulation of magnetization (CSPAMM) by Fischer et al. [33] helped resolve the issue of tagline fading later in the cardiac cycle in conventional tagging, and therefore allowed for analysis of heart contractility during late-diastole. CSPAMM tagging has been shown to be a reliable method for the analysis of cardiac wall motion, strain, and twist [34]. Many studies have been developed around CSPAMM to measure different parameters of global and regional ventricular function and contractility and to study the effects of aging, ischemic and structural heart diseases, and cardiomyopathies on regional cardiac function [35]. CSPAMM tagging has been used for the evaluation of hypertrophic cardiomyopathy, where it showed alterations of total systolic shortening and diastolic strain rates as well as the overlap of apical untwisting with LV filling [36][37]. Other studies used CSPAMM to evaluate the effects of aortic stenosis (AS) on ventricular function [15][18] and recovery of cardiac function following transcatheter aortic repair [38].

2.3. MRI Feature-Tracking

MRI feature-tracking (MRI-FT) is yet another technique for evaluating regional cardiac function directly from the cine images [30]. Ng et al. [39] analyzed MRI-FT-based strain parameters for their ability to identify diastolic dysfunction and assess their correlation with echocardiography indices. The results showed that LV circumferential diastolic strain rate is able to detect diastolic dysfunction with results similar to those obtained by echocardiography.

2.4. Phase-Contrast MRI

Phase-contrast (PC) MRI offers an alternative method to echocardiography for assessing vascular blood flow and myocardial tissue velocity. PC MRI has the potential to measure hemodynamic parameters that are important for assessing diastolic function in clinical routine [40] (Figure 3), with investigational studies showing promise for measuring pressure gradients. PC MRI velocity indices of diastolic function have been shown to correlate with corresponding measurements obtained by Doppler echocardiography [41]. Ashrafpoor et al. [42] demonstrated the capability of PC MRI for independently characterizing subclinical age-related variations in diastolic function among healthy volunteers. The results showed that LV remodeling index and global myocardial wall thickness have a strong correlation with diastolic parameters related to LV and myocardial relaxation, such as myocardial longitudinal peak velocity, deceleration time, and isovolumetric relaxation time [42].
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Figure 3. Grades of diastolic dysfunction (I–IV) based on trans-mitral flow pattern. E, early-diastolic flow; A, atrial/late-diastolic flow; DT, deceleration time.

2.5. Four-Dimensional Flow Cardiac MRI (4D-Flow)

Four-dimensional flow (4D-Flow) MRI is superior to Doppler echocardiography for evaluating intracardiac velocity as it is not limited by flow direction or inconsistency in transducer alignment. Previous studies using 4D-Flow MRI demonstrated significant flow reduction and end-diastolic volume and kinetic energy increase in patients with moderate-to-severe dilated cardiomyopathy [43]. The residual volume at end-diastole can be divided into four functional flow components: direct flow (blood that enters and exits the LV within the same cycle), retained inflow (blood that enters the LV but does not exit during the same cycle), delayed ejection flow (blood that had remained in the LV from the cycle before and is ejected during the current cycle), and residual volume (blood that is stagnant in the LV, not entering nor exiting during the cycle). The division of LV end-diastolic volume in this way showed that direct flow diminishes as LV volume increases and that non-ejecting volume contributing to LV end-diastolic volume (EDV) increases in patients with normal-to-mild LV remodeling and normal-to-mildly depressed LV systolic function [44].

3. Cardiovascular Measures

3.1. Temporal Resolution

While a low temporal resolution does not seem to affect accuracy in the calculation of LV systolic function, it does affect rate-based indices of LV diastolic function, resulting in underestimation of the absolute volume change of respective indices [45]. Several attempts have been made to improve MRI methods for measuring blood or tissue velocities in LV diastolic analysis, although there are some trade-offs in terms of limited quality, poor temporal resolution, long acquisition times, or sophisticated post-processing methods. By using a respiratory-triggered free-breathing cine sequence, Zhang et al. [45] achieved high temporal resolution that has the potential for evaluation of both LV systolic and diastolic functions from a single stack of cine MRI data.

3.2. Late Diastole

Understanding normal variants and pathological differences in diastolic function could be achieved through detailed study embodying the relationship between early- and late-diastolic measurements [46]. While the majority of LV filling occurs at early-diastole in normal physiological conditions, in the presence of diastolic dysfunction, impaired LV relaxation causes a shift of LV filling into late-diastole, associated with LA systolic function. MRI offers promise for early detection of diastolic dysfunction through its ability to distinguish normal from abnormal diastolic patterns. While it has been used to demonstrate characteristics of early-diastole [47], little work has been carried out to study the cardiac function in late-diastole. For example, tag lines fading toward the end of the cardiac cycle limits the usefulness of conventional MRI tagging for studying late-diastolic cardiac function [46]. However, the recent development of MRI-FT techniques offers an alternative option to study myocardial contractility during the late-diastolic phase.

3.3. Untwisting Motion

The processes of myocardial contraction and relaxation during the cardiac cycle are complex, yet organized sequences of events, which under normal function create conditions for maximal cardiac output. During systole the apex and base twist in opposite directions. At the same time, both ventricles contract to pull the atrioventricular plane toward the apex. Diastole is initiated by an instantaneous untwisting of the apex where a change in chamber volume and shape is negligible, followed by relaxation and untwisting of the remaining myocardium resulting in passive filling of the ventricle [35]. There are three components of myocardial relaxation that occur before the aortic valve closes, which produce an abrupt decline in LV pressure that initiates early filling of the LV: (1) release of torsion; (2) shear strain; and (3) radial thinning. Following aortic valve closure, and before the opening of the mitral valve, there is zero change in actual LV volume despite the seemingly increase in ventricular size observed due to distension of the LV myocardium.
Analysis of systolic and diastolic function has been conducted by quantification of torsion and recoil rate, respectively [48]. Kowallick et al. [49] demonstrated that increases in subendocardial torsion and global recoil rate coincide with increasing doses of dobutamine. The authors used MRI-FT indices, which showed to be accurate and reproducible means of quantifying myocardial torsion and recoil rates both at rest and stress. In another study, Dorfman et al. [50] demonstrated impaired diastolic untwisting in a cohort of adults after a period of post-exercise rest. Using MRI tagging to study the effect of inactive lifestyle on myocardial untwisting rate, they demonstrated a notable decline in untwisting rate in the mid-wall, slightly less significant reduction in the endocardium, and no alteration in the epicardium. The authors also showed that a lack of cardiovascular exercise leads to reduced LV mass and end-diastolic volume.
Distinct perturbations of diastolic untwisting, as demonstrated by MRI tagging, helped differentiate physiologic from pathologic hypertrophy [18]. The characteristics of ventricular rotation with clear distinction of early apical untwisting from the onset of ventricular filling showed to be the same in normal healthy hearts and hearts of endurance athletes with physiologic hypertrophy [15]. Contrarily, in patients who develop hypertrophy due to pathologic conditions such as overload or aortic stenosis, the velocity of apical rotation at end-systole is increased and the time to maximum velocity of apical untwisting is delayed, resulting in concurrent relaxation of the apex and filling of the ventricle [15]. Interruption of the normal occurrence of apical untwisting is also seen in patients with myocardial infarction (MI) [51]. However, in this case, there is no separation of apical untwisting from LV filling, and the peak velocity of apical rotation is remarkably reduced.

3.4. Vorticity

The presence of diastolic vortices within the LV contributes to the transfer of fluid kinetic energy between cardiac chambers, which indicates the presence of healthy ventricular function [52]. Decreased LV vortex formation has been demonstrated in patients with both dilated and hypertrophic cardiomyopathies [53] and in HF [54].

3.5. Left Atrium

Left atrial (LA) remodeling can occur in the setting of HF; however, little is known about the pathophysiology behind this phenomenon. Seemann et al. [55] evaluated multiple parameters of cardiac diastolic function using cine and PC MRI and demonstrated a correlation between atrial fibrosis and diastolic dysfunction. In another study, Aquaro et al. [56] showed that alteration of LA contractility parameters was present before that in the LV in diastolic dysfunction. The authors were able to create a diagnostic algorithm for diastolic dysfunction, which includes multiple calculations using measurements of LA and LV volumes, including atrial emptying fraction, isovolumetric pulmonary vein transit volume, and isovolumetric pulmonary vein transit ratio. The results confirmed that LA plays a significant role in the evolution of diastolic dysfunction and that reliable grading of diastolic dysfunction can be achieved by cardiac MRI analysis of both left-sided chambers of the heart. More recently, Kermer et al. [8] used MRI to assess cardiac structure and function in order to detect diastolic dysfunction by assessing the LV and LA functions through using tissue tracking, tagging, tissue phase mapping, and PC sequences and comparing the results to published gold standards including invasive measurements. The results showed that the MRI techniques used to calculate enlarged LA dimensions have high diagnostic accuracy and are predictive for identifying diastolic dysfunction. The results also showed that the impaired contractility pattern of the basal lateral wall is a direct sign of diastolic dysfunction.

3.6. Mitral Annulus

Not much data exists on mitral annular motion as it relates to diastolic function [40]. In one study, Wu et al. [9] used long-axis cine MRI images for mitral annular analysis using 3D mitral annular sweep volumes to determine parameters capable of detecting diastolic dysfunction. Three-dimensional (3D) volume tracking of the mitral annulus showed superiority over other methods such as MRI tagging that cannot evaluate atrial systole with the same reliability [9]. The reversal of the ratio of peak sweep rate in early-diastole to peak sweep rate in atrial systole could possibly be explained by LA dilation and subsequent enhancement of atrial contraction in concordance with the Frank–Starling law [9][57].

This entry is adapted from the peer-reviewed paper 10.3390/tomography7040075

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