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Curr Cardiovasc Imaging Rep (2012) 5:109–115DOI 10.1007/s12410-012-9122-z CARDIAC MAGNETIC RESONANCE (E NAGEL, SECTION EDITOR) Cardiovascular Magnetic Resonance of MyocardialStructure, Function, and Perfusion in Mouse and Rat Models Frank Kober & Monique Bernard & Thomas Troalen &Thibaut Capron # Springer Science+Business Media, LLC 2012 Abstract This review summarizes small-animal cardiovas- Keywords Cardiovascular magnetic resonance . MRI .
cular magnetic resonance (CMR) techniques that are being Perfusion . Self-gating . Function . Late-enhancement .
actively developed at present. Taking into account with few exceptions only literature of the past 2 years it shows thatsmall-animal CMR has become an important and versatileanalysis tool in many biomedical studies. The relatively complex signal formation and detection in magnetic reso-nance offers numerous ways of creating and modulating The years 2010–2011 were particularly rich in the field of image contrast as a function of the specific needs. Although small-animal cardiovascular magnetic resonance (CMR).
most new small-animal CMR developments are done within Indeed, not only method developments, but also preclinical the scientific MR community, the MR manufacturers have applications of more and more complex MR modalities have readily contributed in making these techniques robust and received growing attention. This article provides a compre- available for routine application studies. Unlike other car- hensive overview of new developments and applications in diovascular imaging techniques, CMR is used in many small-animal CMR over this period and outlines the reasons facets to assess morphology, global and regional function, for the rapid growth of this research field.
blood flow, myocardial structure, cell damage, metabolism,and other molecular processes for studying mouse and ratmodels of human disease as well as general biochemical Improved animal MR scanner hardware and software havebeen made available by the manufacturers and have greatlyeased standard functional imaging of the rodent heart. Theimpact of ready-to-use self-gating strategies that had been developed in the preceding years is clearly visible. Also, F. Kober (*) M. Bernard T. Troalen T. CapronCentre de Résonance Magnétique Biologique et Médicale obtaining better image quality in less time was possible by (CRMBM), UMR CNRS n 6612, Faculté de Médecine, both higher magnetic fields and commercially available parallel acquisition hardware (array coils, parallel receivers) and software (k-space acceleration), which were originally Cedex 5, Francee-mail: [email protected] set up on clinical systems. The advantages of these twostrategies have allowed not only improved cardiac functional M. Bernarde-mail: [email protected] cine-imaging, but also to perform quantitative T1 mappingfaster.
T. Troalene-mail: [email protected] The use of clinical MR operating systems combined with high-field animal magnets has offered access to more com- T. Caprone-mail: [email protected] plex base acquisition sequences serving as starting point for Curr Cardiovasc Imaging Rep (2012) 5:109–115 further developments. Efforts are being made to make myo- function assessment than in clinical CMR, in which balanced cardial diffusion MRI applicable in vivo, which is again SSFP (bright-blood) and detection arrays are used in most helped by the availability of high-performance gradient cases. In small-animal CMR, a number of acquisition setups provide images of very different contrast. Surface detectioncoils are widely used leading to spatially varying image signal content, and the flow of LV chamber blood causes strongerperturbations especially in the diastolic LV filling phase. For Self-gating is a retrospective technique using either a navi- these reasons and because small-animal CMR is a compara- gator scan preceding each acquisition or the total signal tively young technique, the number of commercially available content of the MR signal itself as physiological reference.
segmentation software packages dedicated to small-animal This reference signal is then used for reordering the acquired CMR is still low. A recent study compared LV morphological data as needed ]. Self-gating is particularly beneficial and functional parameters obtained manually and with differ- for dynamic imaging, ie, cine-CMR at high heart rates such ent segmentation algorithms [. The underlying data were as those of small rodents, and there are now commercially obtained from healthy and infarcted rats at 9.4T using a available implementations by major manufacturers. This has multi-slice gradient echo bright-blood sequence with short greatly eased standard CMR since cumbersome ECG prepa- echo-time, respiratory gating, and array-coil detection. Results rations and equipment are no longer required to perform on LV volumes were found with less than 10% error versus standard cine-imaging. But even for laboratories equipped with working ECG setups, self-gating can be an advantage.
The fact that certain mouse models such as infarction or heart failure may have strongly attenuated ECG signals gives anadvantage to the self-gating strategy. From an acquisition All different approaches to assess regional function are well point of view, the trade-off in self-gating are longer echo times known from clinical CMR, but have also been shown to be and repetition times, whereas the magnetization steady-state is feasible in small-animal MR. Whereas classical SPAMM maintained, leading to a stable signal amplitude throughout tagging [, ] and DENSE [, are methods for encoding the cardiac cycle. Bovens and coworkers [have indeed displacements and strain directly, tissue phase contrast MR found better signal-to-noise ratios with self-gating compared relies on velocity encoding by bipolar gradients.
with prospective ECG-gating, mainly owing to the uninter- All three approaches are currently developed in parallel.
One challenge in tissue phase contrast is that tissue velocitiesare comparatively small requiring strong bipolar gradients if the echo time and repetition time should not become signifi-cantly longer. On the other hand, the spatial resolution of the The continuing efforts toward using higher fields have led to strain maps corresponds to that of the raw images as opposed reduced scan times, and have made parallel detection a to classical SPAMM, in which the tagging grid spacing rep- useful addition to scanners ]. In particular, 3D func- resents a resolution limit. Animal scanners today are equipped tional assessment of the mouse heart using self-gating has with adequate gradient coils making tissue phase contrast been shown to benefit from k-space accelerated acquisition MRI feasible. Recent work on this technique has improved [•]. The two different approaches cannot be compared temporal resolution and provided all directional velocity com- straightforward, since the first one is on rats with ECG and ponents in a time-resolved manner ]. Black-blood prepa- respiratory gating at 9.4T, and the more recent one on mice ration has still been judged necessary for obtaining the best using self-gating at 4.7T. Nevertheless, an interesting obser- results. DENSE has also no intrinsic limitations by the tagging vation is that in both studies, roughly threefold scan time grid. There is no limitation in detecting small displacements reductions were shown to be possible without compromising like in tissue phase contrast. Due to the use of stimulated functional assessment quality. Both studies report imaging echoes, however, a signal loss of a factor of 2 is intrinsic. A times of less than 10 min (6 min in mice at 4.7T, 3 min in rats study using multi-phase DENSE at rest and under dobutamine at 9.4T) to cover the entire left ventricle.
stress showed improved strain calculation with respect to By acquiring more and more precise data with an increasing classical SPAMM tagging analysis and illustrated the impact number of slices across the LV, automatic cardiac segmentation of the increased cardiac workload on strain.
tools become increasingly important. Automatic segmentationfor animal CMR is more demanding and more dependent on individual experimental setups than in clinical CMR. Despitecomparable overall image quality, more variation is found for The feasibility of adenosine stress along with reasonable scanner hardware, field strength, and sequences used for global perfusion reserve values has been shown in rats under Curr Cardiovasc Imaging Rep (2012) 5:109–115 isoflurane anesthesia, and the commonly used FAIR ASL demonstrating the usefulness of k-space–accelerated acqui- approach has been confronted to microsphere MBF measure- sition for small-animal CMR. Makowski et al. •] used a ments yielding very good agreement ]. Respiratory gating k-t SENSE approach on a clinical 3T scanner. Fermi- and stability against heart-rate variations during acquisition of function deconvolution of the image signal dynamics was ASL data have been improved ], though at the expense of then used to quantify regional MBF yielding values compa- rable to previous ASL findings although no perfusion maps All small-animal myocardial ASL studies published so were calculated. The study also showed a perfusion drop in far made use of flow-sensitive alternating inversion- the infarcted myocardium, whose extent was confirmed by recovery (FAIR) as labeling technique combined with a histology. Coolen et al. [] used a four-element detection look-locker readout. This was first implemented by Belle coil and GRAPPA k-space acceleration allowing for a 64× et al. [and later improved with respect to resolution and 64 pixel image to be acquired within three heart beats, ie, a robustness to motion , ]. More recently, this FAIR temporal resolution of roughly 400 ms with a 15 ms window look-locker acquisition technique has been improved by within the cardiac cycle. Likely owing to a dedicated gradi- Vandsburger et al. [], who have used fuzzy C-means ent system with higher performance, the final temporal clustering for a more accurate calculation of inversion times resolution appears better than in the clinical system’s k-t- in a context of heart rate variations during acquisition. The accelerated approach. This study, however, did not attempt authors also used an interleaved spiral acquisition for read- absolute quantification, and therefore no literature compar- out, replacing the previously used Cartesian FLASH read- out, which as all radial approaches, has the advantage thatall signals contributing to the final image represent an equally weighted portion of k-space. Using this technique,the authors have obtained perfusion maps from mice with Beyond visualization of necrosis in myocardial infarction coronary occlusion, and the hypoperfused regions were (MI), late gadolinium-enhanced (LGE) MRI can be used to compared with late Gd-enhanced MRI. The regional delin- assess diffuse structural alterations such as fibrosis, provid- eation was found more accurate when heart rate variations ed that the longitudinal relaxation time T1 can be mapped were taken into account compared with the use of the quantitatively. As another contrast mechanism, manganese- original prospectively obtained inversion times.
enhanced MRI (MEMRI) provides interesting insights, par- ASL in rodent myocardium has relatively good sensitivity ticularly in ion transport into cells. In both contexts, accurate mainly because MBF and heart rates in rodents are roughly and rapid T1 mapping techniques dedicated to small animals five times higher than in human myocardium, and the are advantageous and have therefore been in the focus of magnetic fields used in rodent studies are generally method studies. One study obtained single-slice T1 maps strong leading to relatively long relaxation times, both with good accuracy from mice by reconsidering saturation- directly influencing the perfusion signal. These conditions recovery look-locker FLASH. The maps could be acquired and the fact that, for the same reasons, bolus tracking is more within 3 min, since no long recovery until full relaxation is difficult than in humans, have contributed to the success of the required between the inversion-recovery acquisitions [ ASL technique when applied to the rodent heart. On the other Another step toward improving T1 mapping speed was hand, ASL measurements are relatively time-consuming since made by employing self-gating and a 3D-driven equilibrium sufficient spatial and temporal resolutions are required to FLASH technique (DESPOT) with five different flip angles accurately separate the endocardial border from the left- •]. While self-gating as a retrospective technique ensured ventricular blood, whose high ASL signal would contaminate a stable steady-state, the influence of through-plane motion the MBF signal measured in the myocardium. This has until on regional saturation could be avoided by using a large now required small time windows within the cardiac cycle and excitation slab, which in 3D imaging covers more than the therefore a high number of experiment repetitions. Parallel entire heart. Each of the five 3D datasets was acquired imaging might in the future allow for scan time reductions within 10 min, and the reproducibility was shown to be without loss in spatial resolution, particularly for this If in contrast-agent studies good temporal resolution and Nevertheless, for a fast regional assessment of perfusion, acquisition efficiency is needed instead of quantitative and in infarction models in particular, first-pass bolus track- aspects, the contrast obtained with standard cine-FLASH ing might deliver sufficient information with the advantage may be sufficient. Notably black-blood contrast obtained of a faster acquisition. In the past year, two groups have by saturation pulses followed by flow spoilers has been independently reported successful myocardial first-pass per- shown to give information on manganese contrast uptake fusion measurements in mice using k-t-acceleration or ac- dynamics with good temporal resolution [Revisiting the celerated parallel detection •, •], thereby implicitly initial use of LGE for infarct size determination, a study by Curr Cardiovasc Imaging Rep (2012) 5:109–115 Protti et al. [yielded that in mice, the commonly vivo in small animals challenging. Nevertheless, the assess- employed inversion-recovery FLASH was not better than ment of cardiac high-energy phosphates such as phospho- standard cine-FLASH at a field strength of 7T, when com- creatine and adenosine triphosphate (ATP) has been setup paring infarct delineation to histology. A protocol combin- and applied to mouse models []. More recently, Gupta ing LGE and global function assessment might therefore be and coworkers ] reported the measurement of ATP accelerated by assessing both modalities with a single cine- kinetics in failing mouse hearts using a triple repetition time saturation transfer technique initially introduced in humans Since necrosis also affects tissue T2, this parameter is useful for MI characterization. In this scope, a preparation- An interesting research path has been opened by using 19 module–based T2-weighted [] sequence was developed F MRI of fluorinated compounds. Many compounds used in using an adiabatic MLEV approach with good robustness today’s biomedicine indeed contain fluorine and can be against B0 and B1 heterogeneities, which were found signifi- monitored with 19 F-MRI ]. This way, many fluorinated cant at 7T. The authors applied the sequence to a murine molecules such as perflurocarbons become an interesting infarction model and found sufficient contrast to delineate new class of contrast agents for MR with the advantage that the infarcted area with good precision. T2-weighted MRI is no non-relevant image signal is overlaid, because no native therefore a totally noninvasive alternative to LGE MRI or a 19 F background is in the body. The 19 F MR signal is complement providing supplemental characterization.
therefore qualified as robust and very specific despite lowersensitivity than the proton signal from water. As a recent example, imaging of the accumulation of emulsified per-fluorocarbons by monocytes and macrophages has been Diffusion MRI is based on MR signal weighting by the used by Flögel et al. ] to early depict allograft rejection Brownian (random) motion of molecules across an external- and to monitor rejection therapy in a heterotopic transplan- ly applied dephasing and rephasing magnetic field gradient.
tation mouse model. Another new MR application field was Since molecular motion in tissue is restricted by cell mem- opened by the possibility to increase the signal of the 13 C branes, the measured diffusion tensor is representative for nucleus by four orders of magnitude using hyperpolariza- tissue structure in general and myocardial fiber geometry in tion, and to give direct access to study metabolites relevant particular. Diffusion MRI of the heart as a moving organ has in the Krebs cycle as well as a number of derivates. 13 C been a challenge for both clinical and preclinical MR com- spectra contain information about lactate, pyruvate hydrate, munities, since the cardiac motion itself influences the mea- alanine, pyruvate, and bicarbonate. A recent study surement of the Brownian motion to a very high degree, if investigated the effect of hyperthyroidism on cardiac hyper- not compensated for appropriately. To date, the majority of trophy in a rat model using 13 C spectroscopy in vivo. From animal studies found in the literature were therefore carried their measurements, the authors calculated a twofold re- out on excised and/or fixed myocardium providing insight duced pyruvate dehydrogenase flux in hyperthyroid animals into fiber architecture and its changes mainly in mouse and versus controls and thereby showed that inhibition of glu- swine models. The main focus of fiber organization studies cose oxidation in hypertrophy is mediated by pyruvate de- has been MI and tissue remodeling, but changes in fiber hydrogenase kinase, providing a potential target for therapy.
orientation might also represent an interesting parameter for The chemical shift of certain carbon compounds is depen- studying non-ischemic cardiomyopathies. Excellent over- dent on pH and therefore represents a tool to determine views of the status of ex vivo and in vivo myocardial intracellular pH non-invasively ]. Beyond non-localized diffusion MRI in animals and humans were published re- spectroscopy, MR chemical shift imaging (CSI) is able to cently by Huang et al. [and Sosnovik et al. [who provide spatial distribution maps of metabolites, and dedi- have also been able to obtain diffusion MRI data from cated sequence development addressing the needs of hyper- polarized 13 C CSI is ongoing although recently in largeranimal models ]. A comprehensive review specifically addressing hyperpolarized MR to the heart has been pub-lished by Tyler [].
As a unique technique, MR can record and use signalscoming from other nuclei than the proton opening accessto more complex molecules implied in cell metabolism directly. Due to the comparatively low sensitivity of MRIand the low concentrations of metabolites compared to the The application field of small-animal in vivo CMR covers water used in conventional MRI, non-proton MR is limited MI, heart failure, stem-cell tracking, and the study of car- in temporal and spatial resolution, which makes its use in diovascular dysfunction in gene-manipulated mice, often Curr Cardiovasc Imaging Rep (2012) 5:109–115 associated with therapeutic monitoring. Although this review’s new growth-factor combination for heart failure treatment main objective is to give an MR method overview, and since Hiller and coworkers [] evaluated the effect of many of the method developments cited above are accompa- angiotensin-converting enzyme (ACE) inhibition by quinapril nied by a direct application, we will in the following also briefly in a mouse infarction model. They collected a complex dataset summarize a selected set of applications employing MRI with multimodal MRI including myocardial blood flow and volume, cine-imaging, as well as perfused-heart coronaryangiography, leading to the conclusion that not only function, Stem-Cell Tracking and Evaluation of Therapy but also microcirculation was improved by the ACE inhibitionapproach.
Qiao et al. have used MRI to depict SPIO-labeled em-bryonic stem cells delivered after myocardial infarction in rats.
The extent of MI in the myocardium was determined using LGE. They monitored myocardial recovery with cine-MRIand DENSE and were thereby able to demonstrate bene- In this review, we have summarized active developments for fits of the embryonic stem-cell therapy. An alternative track- small-animal CMR based on the literature over the past ing strategy was based on the use of human ferritin heavy 2 years. Not only method development, but also the interest chain as a paramagnetic reporter gene ]. The authors of the biomedical community in small-animal CMR has been modified swine cardiac stem cells to over-express this gene.
rapidly growing over the last years, confirming this technique A multi-gradient echo sequence on a clinical 1.5T system was as a powerful noninvasive research tool. Indeed, the availability used to locate the ferritin-overexpressing injected cells in rats of new methods has led to an impressive number of application with MI. Another study ] used cine-imaging to demon- studies in which small-animal in vivo MR has played a signif- strate that a novel form of microvascular stem cell graft matrix icant role. With the cited recent developments one can expect effectively preserved contractile performance after myocardial this trend to become even stronger in the future. Readers only infarction, attenuated left ventricular dilation, and decreased familiar with clinical CMR will have noticed that all clinically available magnetic resonance measurements have their equiv-alent in small-animal MRI available, but that in many cases not only specific parameters, but also sequence strategies dedicatedto the rodent’s cardiovascular system are needed. This does not In the light of the recent finding that apoptosis is reversible appear surprising when keeping in mind not only the spatial in certain circumstances, CMR as a totally non-invasive tool dimension differences of up to three orders of magnitude, but appears particularly attractive. Extremely sensitive MRI- also the differences in flow velocities and motion. Despite this, markers of apoptosis have been developed in the past ], a number of clinical method developments can be expected to and a recent study ] carried out on a 3T clinical MRI benefit from the experience made with small animal techni- system has reported successful monitoring of apoptosis in a ques, such as the setup of spin-labeling perfusion techniques.
specific heart disease rat model (doxorubicin cardiomyopa- But one also notices transfer of technology from clinical sys- thy), in which apoptosis occurs only at a moderate degree. A tems toward small-animal systems, which in turn demonstrates major result has been obtained from a rat study using MRI the active exchange between communities both ways.
for tracking iron-oxide labeled phosphorylseline-presentingliposomes that are accumulated by macrophages present in No potential conflicts of interest relevant to this article the infarct zone after MI •]. The authors used these lip- osomes to mimic apoptosis, which in turn had been shownto play a role in limiting the extent of inflammation afterinfarction.
Other MR Applications for Therapeutic Monitoringor Genetic Characterization Papers of particular interest, published recently, have beenhighlighted as: The majority of model characterization studies still relied on using cine-imaging for assessing global function [].
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