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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
AJNR Am J Neuroradiol. Author manuscript; available in PMC Jan 17, 2007.
Published in final edited form as:
PMCID: PMC1773015

High Resolution Vascular Imaging of the Rat Spine using Liposomal Blood Pool MR Agent



High resolution, vascular magnetic resonance imaging of the spine region in small animals poses several challenges. The small anatomical features, extravascular diffusion, and the low signal-to-noise ratio limit the use of conventional contrast agents. We hypothesize that a long circulating, intravascular liposomal-encapsulated MR contrast agent (liposomal-Gd) would facilitate visualization of small anatomical features of the perispinal vasculature not visible with conventional contrast agent (Gd-DTPA).


In this study, high-resolution magnetic resonance angiography (MRA) of the spine region was performed in a rat model using a liposomal-Gd, which is known to remain within the bloodpool for an extended period. The imaging characteristics of this agent were compared to a conventional, Gd-DTPA.


The liposomal-Gd enabled acquisition of high quality angiograms with high signal-to-noise ratio. Several important vascular features such as radicular arteries, posterior spinal vein and epidural venous plexus were visualized in the angiograms obtained with the liposomal agent. The MR angiograms obtained with conventional Gd-DTPA did not demonstrate these vessels clearly due to marked extravascular soft-tissue enhancement that obscured the vasculature.


This study demonstrates the potential benefit of long circulating liposomal-Gd as a MR contrast agent for high-resolution vascular imaging applications.


Compromised vasculature is implicated in a number of spine pathologies (1,2). Moreover, demonstration of perispinal vasculature is important for presurgical planning (3). Imaging of mid and large vascular structures is aided by the use of exogenous contrast agents that are typically imaged on first-pass through the arterial circuit using a fast acquisition, which is referred to as Contrast Enhanced Magnetic Resonance Angiography or CE-MRA (4,5,6). Unfortunately, the role of CE-MRA has been limited in the evaluation of smaller vessels, due to the long scan times required and the resulting venous contamination.

Rodent models are commonly used to study spinal cord pathologies, particularly spinal cord injury (SCI) (7,8,9,10,11,12). Magnetic resonance angiography of the spine in rodents however, presents unique challenges because of the small size of the blood vessels (approximately 100–300 μm). Visualization of these vessels with high signal-to-noise ratio (SNR) requires significant signal averaging and involves relatively long acquisition times.

In the present work, we report the use of gadolinium-encapsulated long circulating liposomes (liposomal-Gd) for high resolution MR imaging of the rat spinal vasculature. Although there is some variability in the literature, we define high resolution MRA as imaging at spatial resolution of approximately 100 μm, and use it as such in the present context. Long circulating liposomes are nanoparticles (~ 100 nm) bearing hydrophilic polyethylene glycol (PEG) chains on their external surface. The PEG coating prevents opsonization, and prolongs circulation half-life to around 18 hours (13). The long intra-vascular half-life of this agent results in stable levels of contrast agent within the blood pool for many hours, thus enabling a longer image-acquisition time window. Beyond this, there is relative lack of enhancement of the adjacent extravascular tissue that results in a high contrast-to-noise ratio. We therefore hypothesize that a long circulating, intravascular liposomal-encapsulated MR contrast agent (liposomal-Gd) would facilitate visualization of small anatomical features of the perispinal vasculature in a rat model not visible with conventional contrast agent (Gd-DTPA).


Liposomal-Gd Preparation

Liposomal-Gd was prepared by modification of methods described previously (14, 15). Briefly, a lipid mixture consisting of 1,2-Dipalmitoyl-sn-glycero-3-phosphocholine (DPPC) (Genzyme, MA), Cholesterol (Sigma, St Louis, MO) and 1,2-distearoyl-sn-glycero-3-phosphoethanolamine-N-[methoxy(poly(ethylene glycol))-2000] (mPEG2000-DSPE) (Genzyme, MA) in the ratio 55:40:5 was dissolved in ethanol at 60°C. The ethanol solution was then hydrated with 0.5 M gadodiamide (Omniscan® - Gd-DTPA BMA) solution and stirred for 1 hr at 60°C. The resulting liposomal solution was sequentially extruded at 60°C on Lipex Thermoline extruder (Northern Lipids, Vancouver, Canada) with three passes through 0.4 μm Nuclepore membrane (Waterman, Newton, MA), five passes through 0.2 μm Nuclepore membrane and eight passes through 0.1 μm Nuclepore membrane. The external phase was then cleaned and the liposomes simultaneously concentrated by diafiltration using MicroKros modules (Spectrum Laboratories, CA) of 50 nm cutoff. The size of the resultant liposomal formulations obtained was determined by dynamic light scattering (DLS) using a Brookhaven Instruments BI-9000AT Digital Autocorrelator, a BI-200SM goniometer (JDS Uniphase; San Jose, CA) and a Hamamatsu photomultiplier (supplied by Brookhaven, Long Island, NY). The resultant size of liposomes in the formulation as determined using DLS was 105 nm with a polydispersity index of 0.107.

The concentration of gadolinium in the liposomal-Gd formulation was determined by inductively coupled plasma atomic emission spectroscopy (ICP-AES). The average concentration of Gd in the formulation was found to be 90 mM. To determine the in-vitro molar T1 relaxivity of the liposomal-Gd formulation, samples with Gd concentrations ranging between 0.5 mM – 2 mM (4 samples) were prepared by diluting the original liposomal formulation with phosphate buffered saline. The T1 relaxation times of the samples were then determined on a 7 Tesla Bruker scanner using a multi-spin multi-echo (MSME) sequence with the following parameters: TE = 9 ms, TR was varied from 40 – 16000 ms. A plot of the T1 relaxation rates versus Gd concentrations yielded a straight line with the slope as the in-vitro T1 relaxivity of the formulation, which was found to be 0.8 (mM.s)−1.

Animal Preparation

All animal studies were performed under a protocol approved by the Animal Welfare Committee of the University of Texas – Houston Health Science Center. Five Sprague–Dawley rats weighing between 350–390 g were used in this study. After spontaneous inhalation of 4% isoflurane, the animal was intubated and maintained under anesthesia by ventilating a mixture of 2% isoflurane, 30% oxygen and air with a vaporizer (Isotec3, Ohmeda, UK) and administered through a Harvard rodent ventilator (South Natick, MA). The left jugular vein was cannulated for intravenous delivery of the contrast agent, as described previously (16). A rectangular coil (11 × 35 mm) was implanted in the back of the animal and centered at the T7 level and inductively coupled to an external surface coil (30 × 40 mm) for improved image quality (17). The animal was placed in the supine position over the external coil on a custom-built Plexiglas sled and the entire assembly was inserted into the bore of the magnet. The body temperature was maintained at 37°C by circulating warm water through the animal bed throughout the MRI scan.

MRI Protocol

All MR studies were performed on a 7 Tesla Bruker scanner, 70/30 URS (Bruker Biospec, Karlsruhe, Germany) using a 116-mm shielded gradient insert that is capable of producing a maximum gradient amplitude of 400 mT/m with 80-μs rise time. Following the acquisition of orthogonal scout image for animal positioning, anatomical images were obtained using T1-weighted spin echo sequence with TE/TR = 10.4/500 ms, 26 mm field of view, and 20 interleaved contiguous axial slices, each 1 mm thick. Preliminary scans were performed for optimizing the scan parameters (echo time, repetition time and flip angle) for MRA, and the same parameters were utilized for all the subsequent scans.

Standard Resolution Studies

Pre-contrast, post-liposomal-Gd and post-Gd-DTPA images were acquired as described below. Separate animals were used to evaluate Gd-DTPA and liposomal-Gd to avoid confounding issues that could result from interactions between the two contrast agents. The images were acquired using a flow compensated fast 3D gradient-echo (GE) sequence with the following parameters: TR/TE = 18.3/2.8 ms, flip angle = 30 degrees, image matrix = 128 × 128 × 64, FOV = 41 mm × 28 mm × 25 mm, and bandwidth = 200 KHz. The data was acquired with one signal average, thus resulting in a scan time of 2.5 minutes. Signal from the surrounding tissue was reduced by incorporating a 1 ms long magnetization transfer pulse with a frequency offset of 1500 Hz. For the Gd-DTPA study, pre-contrast images were acquired followed by administration of Gd-DTPA at a dose of 0.1 mmol/kg. The data acquisition for post- Gd-DTPA images was started immediately and subsequent images were acquired over the next 30 minutes. For the liposomal-Gd study, pre-contrast images were acquired followed by administration of liposomal-Gd at a dose of 0.1 mmol/kg. Post- liposomal-Gd images were acquired at 30 minutes post-liposomal administration. Images for MRA were acquired without cardiac or respiratory gating. Maximum intensity projections (MIP) (generated using Paravision 3.0.2 software or NIH Image J software) were used to visualize the angiograms. Contrast-to-noise ratios (CNR) were calculated for regions of interest (ROI) in the aorta, epidural venous plexus, intercostal arteries and hemi-azygous vein. The contrast-to-noise ratio was calculated by subtracting the average signal intensity in the surrounding tissues from the average signal intensity within the blood vessel and then dividing this difference by the standard deviation of the signal intensity within the background (air).

High-Resolution Studies

A high spatial resolution acquisition was performed following the injection of 0.1 mmol/kg of Gd in the form of liposomal-Gd through the jugular vein using the previously implanted catheter. Imaging was performed using a flow compensated fast 3D gradient-echo (GE) sequence with the following parameters: TR/TE = 18.3/2.8 ms, flip angle = 30 degrees, image matrix = 256 × 256 × 256, FOV = 41 mm × 28 mm × 25 mm, and bandwidth = 200 KHz. A voxel size of 160 μm × 09 μm × 98 μm was achieved using the above parameters. The number of signal averages was set to 3. The scan time for one signal average was 20 minutes. Signal from the surrounding tissue was reduced by incorporating a 1 ms long magnetization transfer pulse with a frequency offset of 1500 Hz. Images for MRA were acquired without cardiac or respiratory gating. Maximum intensity projections (MIP) (generated using Paravision 3.0.2 software or NIH Image J software) were used to visualize the angiograms. Using the method described above, contrast-to-noise ratios (CNR) were calculated for regions of interest in the posterior spinal vein, epidural venous plexus, anterior spinal artery and radicular artery (of Adamkiewicz).


For the standard resolution study, maximum intensity projection (MIP) images of the thoracic spinal region in the coronal plane were generated from acquisitions obtained prior to and following the administration of liposomal-Gd and Gd-DTPA (Figure 1). The descending aorta (Ao) and some of the intercostal arteries (IA) are visible on the pre-contrast image. The Gd-DTPA post-contrast image shows relatively poor image-contrast between the vasculature and the surrounding tissue, due to enhancement of the extravascular tissues, presumably due to diffusion of the Gd-DTPA into the extracellular space. The scans acquired over the next 30 minutes did not show any improvement in image quality. Conversely, the post-liposomal-Gd images showed clear vessel enhancement and negligible tissue enhancement. Given this good target-to-background contrast, more perispinal vasculature is demonstrable on the post liposomal-Gd images. In fact, the intravascular enhancement observed is greater for the post-Gd-DTPA study, than for the post-liposomal-Gd study. However the contrast-to-noise ratios for Gd-DTPA images were lower than liposomal-Gd images (Table 1). (Subtle differences in image orientation in the post-contrast images in Figures 1 are of secondary importance compared to slice-selection differences between the datasets which were acquired using two different animals.)

Figure 1
Coronal MIP images of the thoraco-lumbar spine region acquired (a) pre-contrast, (b) post- liposomal-Gd and (c) post- Gd-DTPA. The images were acquired using the following parameters: TR/TE = 18.3/2.8 ms, flip angle = 30 degrees, image matrix = 128 × ...
Table 1
Contrast-to-noise ratio (CNR) for anatomical features in standard-resolution images obtained with Gd-DTPA to images obtained with liposomal-Gd.

For the high-resolution study, MIP images of the thoracic spinal region were generated in the coronal plane before and after administration of liposomal-Gd (Figure 2). The post-contrast images demonstrate several small blood vessels in the vicinity of the spinal cord, the epidural venous plexus (VP), and the posterior spinal vein (PSV) along the dorsal surface of the spinal cord. The contrast-to-noise ratios for liposomal-Gd images were higher than pre-contrast images. (Table 2).

Figure 2
Coronal MIP images of the thoraco-lumbar spine region acquired before (left) and after (right) administration of liposomal-Gd. The images were acquired using the following parameters: TR/TE = 18.3/2.8 ms, flip angle = 30 degrees, image matrix = 256 × ...
Table 2
Contrast-to-noise ratio (CNR) for anatomical features in high-resolution images obtained pre-contrast and after administration of liposomal-Gd.

Axial images from the post-liposomal Gd volume acquisition of the mid thoracic spine were also reviewed (Figure 3). The hemiazygous vein (HV) is clearly seen in this image. The descending aorta and a section of the inferior vena cava are also visible. In addition, unnamed perforating vessels are identified penetrating the ventral spinal cord (Figure 3b, 3d). Artifacts due to the presence of the surgically-implanted radio-frequency coil within the soft tissues of the back are also visible in all the images. The posterior spinal vein (PSV), anterior spinal artery (ASA), and radicular arteries (including presumably the artery of Adamkiewicz (AA) with its characteristic hairpin turn) are identified on the MIP images generated in the coronal plane (Figure 4).

Figure 3
Pre-contrast (top row) and post-contrast (bottom row) axial slices at different locations through the thoraco-lumbar spine region showing several important vascular features (aorta- Ao; inferior vena cava– IVC; hemi-azygous vein – HV). ...
Figure 4
Coronal MIP images of the thoraco-lumbar spine region obtained with liposomal-Gd. The posterior spinal vein (PSV) is clearly seen in figure 4a (arrows). The anterior spinal artery (arrowheads), the artery of Adamkiewicz (AA) and an accessory anterior ...


Small animal vascular MR imaging of the spine poses several challenges. The majority of the perispinal vessels are ≤ 300 μm in size (18), and the vessels within the spinal cord are ≤150 μm in size. Imaging these micro-vessels necessitates a large image acquisition matrix size (small voxel size) to achieve the required high spatial resolution. Unfortunately, this results in a concomitant reduction in the SNR. To overcome this penalty in SNR imposed by the acquisition matrix, data have to be acquired with several signal averages that, unfortunately comes at the cost of longer acquisition times.

The majority of studies of rodent spinal vasculature done to date have therefore been based on invasive imaging. Tveten et al. investigated the vasculature of the rat spinal region using microangiographic and stereomicroscopic techniques (19,20). Koyangi et al. have analyzed the rat spinal cord vasculature with scanning electron microscope examination of a vascular corrosion cast (17). MRI techniques have not yet yielded sufficient information on the vasculature. For instance, Bilgen et al. studied spinal MRA at 9.4 T without the use of any exogenous contrast agent and in conjunction with the time-of-flight technique (21). Although some of the intercostal arteries were visible, the lack of contrast agent within the vasculature for a sustained interval prevented high-resolution studies, and also precluded visualization of intra-cord vasculature. Yet, the promise of high resolution, non-invasive imaging is alluring and motivates the current work.

An ideal contrast agent for this type of data acquisition (long-duration, large image matrix) should have the following characteristics: (1) the contrast agent must remain confined to the vasculature, and (2) maintain a relatively constant concentration (low elimination, dilution and redistribution during the period of the data acquisition). If the contrast agent exits the intravascular space during the acquisition period, the CE-MRA images are degraded for two reasons. First, the relaxation time of blood is increased and the signal from blood is reduced at short TR. Second, the contrast agent diffuses into the surrounding tissue and reduces the relaxation time, resulting in increased signal from the surrounding tissue. As a result, the image-contrast between blood vessels and the surrounding tissues (target-to-background) is reduced and compromises the quality of MRA. Thus, as demonstrated in the current studies, conventional low molecular-weight agents such as Gd-DTPA are not well suited for high resolution MRA. Another important parameter that determines the quality of angiograms is the blood elimination rate of contrast agent. The conventional contrast agents are eliminated rapidly from blood circulation through renal clearance. Although they do not penetrate the blood spinal cord barrier (BSCB), the rapid clearance of these contrast agents from blood circulation limits their use in acquiring angiograms with long scan times.

Liposomal-Gd has several advantages over conventional low molecular-weight gadolinium chelates. The long intravascular half-life of liposomal-Gd allows for stable opacification of the blood vessels for the duration required for acquisition of high-resolution images. Furthermore, the nano-size of these agents restricts their circulation to the vascular compartment, in regions of low capillary leak, and limits diffusion away from the vasculature in regions of high vascular permeability. The result of these two features is to limit the amount of enhancement of the extravascular tissues. Although the vascular signal intensities in the post- Gd-DTPA images were higher than in liposomal-Gd images, the contrast-to-noise ratios obtained with liposomal-Gd were higher than Gd-DTPA (Table 1). Rapid diffusion of Gd-DTPA into the extravascular compartment is likely responsible for the enhancement of the extravascular soft tissues that results in poor contrast between the vessels and the surrounding tissues. Acquiring high-resolution images with Gd-DTPA would therefore be expected to result in even more indistinct angiograms due to: 1) significant extravascular diffusion during long scan times, and 2) elimination from systemic circulation due to renal clearance.

The high-resolution angiograms obtained with liposomal-Gd demonstrated very good microvessel conspicuity (Figure 2). The posterior spinal vein, anterior spinal artery and radicular arteries were clearly demonstrated in the MIP images (Figure 4). The intravascular nature of the liposomal-Gd agent also enabled visualization of the epidural venous plexus. The epidural venous plexus, which consists of a lattice of fine venules, has an amorphous appearance, rather than discrete because the diameters of these fine venules are much smaller than the voxel size of the image acquisition. The contrast-to-noise ratios in the post-liposomal-Gd images were significantly higher than pre-contrast images (Table 2).

In addition to the liposomal-Gd agent, several other factors were critical in obtaining the high quality angiograms. A radio-frequency coil was surgically implanted within the soft tissues of the back of the animal and inductively coupled to an external surface coil. This enabled imaging with high SNR which resulted in demonstration of several perispinal microvessels (Figure 4). A short echo time was used in the gradient echo sequence to obtain a more heavily T1-weighted image. The repetition time was maintained as short as possible to reduce the overall scan time and thus allow for several signal averages.

While the current studies demonstrate extra-spinal cord vasculature with much detail, we have not been able to visualize the vessels within the spinal cord because of the resolution limitations and the low relaxivity of the liposomal-Gd agent. The ability to non-invasively visualize intra-spinal cord vasculature would greatly help in defining the vascular lesions and microvascular reorganization in spinal cord injury (22). It may also be possible to increase the image resolution by increasing the image matrix with concomitant increase in the scan time. However, this approach may be limited by morbidity and mortality associated with long anesthetic times. With the development of parallel imaging technology this limitation could be overcome to a great extent (23).

The encapsulation of Gd-DTPA within the core of the liposomes results in limited water exchange across the lipid bilayer. The molar relaxivity of gadolinium encapsulated within liposomes is far lower than that observed in unencapsulated (free) Gd-DTPA. The encapsulation of Gd-DTPA inside these liposomes also alters the pharmacokinetics of Gd-DTPA. The clearance of liposomal-Gd occurs through the organs of reticulo-endothelial system (RES), namely liver and spleen, rather than the kidneys. Further in vivo studies should be done to investigate the possible concerns associated with the altered pharmacokinetics of the agent.

A unique characteristic of long circulating liposomes is the ability to extravasate only from abnormal, leaky vessels. This property has been extensively exploited to deliver chemotherapeutic agents to solid tumors (24). For grading and imaging solid tumors, the same characteristic of liposomal particles could therefore be utilized to overcome the confounding issues with conventional Gd-DTPA agent, which also leaks in normal micro-vasculature (25). The encapsulation of gadolinium chelates within the liposomal interior also enables easy modification of the outer surface of the liposomes for actively targeting the contrast agents to specific sites (such as tumors, inflammation, injury etc).


The liposomal-Gd enabled acquisition of angiograms with higher microvessel conspicuity than conventional Gd-DTPA. This was due to the relative lack of extravascular enhancement that resulted in improved target-to-background contrast. In addition, the prolonged intravascular residence time of liposomal-Gd allowed for longer scans, thus facilitating high-resolution angiograms.


The authors would like to acknowledge Dr. Shi-Jie Liu, Pallavi Ahobila-Vajjula and Tessy Chacko for their help in animal handling and preparation.


Grant Support: Partial support for these studies was provided by NSF BES 0201891 (A.V.A.), NIH RO1 NS30821 (P.A.N.), Chandran Family Foundation (S.M.) and the American Roentgen Ray Society (S.M.).


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