Parallel Imaging in Inﬂ ammatory Bowel Disease 23

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K. A. Herrmann, MD

Department of Clinical Radiology, University Hospitals – Gross hadern, Ludwig Maximilian University of Munich, Marchioni nistr. 15, 81377 Munich, Germany

C O N T E N T S

23.1 Introduction 247

23.2 Technical Considerations of Small-Bowel Imaging with MRI 247 23.3 Clinical Applications of MRE 248 23.4 MRE in Crohn’s Disease 249

23.5 Parallel Imaging Techniques and MRE 249 23.6 3D-TrueFISP with 2D Parallel Imaging 250 23.7 Clinical Impact of High-Resolution

3D-TrueFISP and 3D Post-Processing 251 23.8 Future Improvement and Perspectives of SB

Imaging with MRE and Parallel MRI 251

References 253

Parallel Imaging in Inﬂ ammatory Bowel Disease 23

Karin A. Herrmann

surface. Overlay of structures due to the projection technique may limit the diagnostic quality of the examination, and mural and extramural processes are not depicted with this imaging modality.

MRI is suitable for overcoming most of these problems of conventional projection radiography and provides additional advantages: representing a multi-planar cross-sectional imaging modality, MRI readily depicts both intra-luminal mucosal as well as submucosal, mural and extramural pathology. In this quality, MRI currently competes with upcoming multi-planar multi-detector computed tomography of the bowel (Maglinte et al. 2003; Furukawa et al.

2004), yet, MRI is not related to radiation exposure.

Furthermore, it offers additional tissue characterization due to its high soft-tissue contrast properties.

Over the past 5 years, considerable progress has been made in the technical development of ultra-fast imaging sequences in MRI, providing short acquisition times and breath-hold examination for abdominal imaging in general and for bowel imaging in particular. This may be why MRI of the small and large bowel has been fostered with increasing at- tention and great success, ﬁ rst and foremost in the imaging of Crohn’s disease (Maglinte et al. 2003;

Gourtsoyiannis et al. 2002).

23.2

Technical Considerations of Small-Bowel Imaging with MRI

Formerly, MRI of the small and large bowel has suffered from signiﬁ cant technical limitations related to respiratory movements, bowel motility and the tortuous course of this tubular organ within the abdominal cavity. The break-through for MRI of the intestinal tract was linked to the advent of fast and ultra-fast imaging sequences in the early 1990s (Nitz 2002; Papanikolaou et al. 2002;

23.1

Introduction

Small-bowel (SB) imaging, thus far, has been the domain of radiological and ﬂ uoroscopic imaging techniques such as small-bowel follow-through and barium-sul- fate double-contrast enteroclysis, both representing the gold standard for SB imaging (Maglinte et al. 1992;

Maglinte et al. 1996). They provide dynamic information on SB motility and morphologic information on the intra-luminal mucosal surface and the SB lumen.

Yet, these techniques require the exposure to ionizing radiation and, as they are pure “luminograms,” they are restricted to imaging the lumen and the mucosal

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Gourtsoyiannis and Papanikolaou 2005), compris- ing single-shot turbo-spin-echo sequences (e.g., SSFSE, HASTE or FIESTA), steady-state free-precession sequences (e.g., FISP, True FISP, FFE, GRASS) and gradient-echo sequences with low ﬂ ip angles (GRE, FLASH) as well as fast-spin-echo or turbo-spin-echo sequences (FSE and TSE) (Nitz 2002; Papanikolaou et al. 2002;

Gourtsoyiannis and Papanikolaou 2005; Nitz 1999). Mainly due to their robustness against motility artefacts, these ultra-fast sequences helped to realize high-quality imaging of the abdominal organs and the bowel, and can, by now, be considered state-of-the-art sequences for this purpose.

When performing MRI of the SB, further distinct challenges will be encountered. As is known from well-established conventional radiological techniques (Maglinte et al. 2003), the SB lumen and wall is more reliably assessed in full bowel distension. Therefore, intra-luminal contrast media have to be administered in order to distend the bowel and to render mucosal, submucosal and mural abnormalities more conspicuous. A number of different intra-luminal contrast media are available for MRI of the SB. According to their signal characteristics in conjunction with typical imaging sequences, intra-luminal contrast media are classiﬁ ed in positive, biphasic and negative. Posi- tive intra-luminal contrast agents exhibit high signal intensity in both T1-weighted and T2-weighted imaging. Biphasic contrast media have high signal intensity on T2-weighted images and low signal on T1-weighted images. Typical representatives of the latter group are polyethylene glycol (PEG) (Gourt- soyiannis et al. 2002; Laghi et al. 2003; Prasopou- los et al. 2001), methylcellulose aqueous solution, locust bean gum solution and water (Gourtsoyian- nis et al. 2000). Negative intra-luminal contrast with both T1-weighted and T2-weighted sequences is ba- sically achieved with substances containing iron-oxide particles (Boraschi et al. 2004; Herrmann et al.

2005; Maccioni et al. 2004; Holzknecht et al. 2003).

To date, there is no common sense in the literature as to which contrast medium to prefer for adequate SB imaging.

Further controversy exists in the literature as to whether to apply these substances orally or to per- form nasojejunal intubation and direct intra-luminal infusion. Oral application is favoured in children (Laghi et al. 2003). Yet in general, MRI of the SB after oral ingestion of the contrast medium may suf- fer from incomplete and inhomogeneous distension or even collapse of segments of bowel in up to 23%

of the cases, mainly concerning the jejunum or the

terminal ileum (Born et al. 2003; Schreyer et al.

2004). With nasojejunal intubation and automatic infusion of the contrast medium, the administration of the contrast medium is constantly supervised using MR-ﬂ uoroscopy with the patient already inside the magnet. At the instant of appropriate and homogeneous distension of all SB segments, standard imaging sequences are acquired while full dilatation of the bowel is maintained using antispasmotic drugs such as butylscopolamine or glucagon. This procedure is called MR-enteroclysis (MRE) and is recommended by many authors (Laghi et al. 2003; Papanikolaou et al. 2002; Prasopoulos et al. 2001; Gourtsoyiannis et al. 2000; Herrmann et al. 2005; Herrmann et al.

2006a; Gourtsoyiannis et al. 2001) since it provides homogeneous dilatation of the entire small bowel at the instant of investigation.

Homogeneous SB distension as provided with MRE is warranted in almost all issues of SB assessment, especially if high-resolution imaging of the small bowel is attempted. In the absence of adequate active SB distension, SB may remain collapsed and appropriate diagnostic interpretation is hampered. Collapsed SB wall may be misinterpreted as thickened from inﬂ ammatory or neoplastic processes, and subtle abnormalities of the fold pattern or mucosa may be obscured. This is one major argument why MRE should be preferred to MRI after oral contrast media. Initial experiences have shown that MRE is the preferable technique to proﬁ t from the advantages of parallel imaging in SB imaging (Herrmann et al. 2006b).

23.3

Clinical Applications of MRE

Crohn’s disease (CD) of the SB is one major indica- tion for SB imaging with MRI and MRE. Its purpose is to determine the presence, extent and severity of this disease. Facing the young age of patients affected with this chronic disease, MRI seems to be preferable to CT and CT enteroclysis in this respect. Further indica- tions for MRE, though currently less well established, are the search for benign or malignant neoplasms and the identiﬁ cation of the underlying pathology in mechanical SB obstruction (Papanikolaou et al.

2002; Prassopoulos et al. 2001). In the diagnostic management of postoperative adhesions and intestinal hemorrhage or small bowel ischemia, the usefulness of MRE has not been explored so far.

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23.4

MRE in Crohn’s Disease

Crohn’s disease (CD) in its initial stages is character- ized by small superﬁ cial lesions of the mucosal surface, mucosal ﬁ ssures and ulcera. In order to establish the diagnosis of early CD and to depict these subtle mucosal lesions in imaging, high spatial resolution is required. Up to now, MRE was clearly limited in this respect, and inferior to conventional radiographic imaging techniques, the latter offering a spatial resolution of far less than 1 mm³.

In contrast, MRE has proven to be a very reliable in disclosing transmural and extramural disease. Appro- priate dilatation of the SB provided, the disruption of the mucosal fold pattern, deep mucosal ulcera, inﬂ ammatory stenosis, prestenotic dilatation, internal enteric ﬁ stulae and abscesses can easily be visualized in MRE (Prasopoulos et al. 2001; Herrmann et al. 2005;

Herrmann et al. 2006a; Maccioni et al. 2000; Rieber et al. 2000; Rieber et al. 2002). Since different stages of infl ammation in CD may be encountered in one patient, distinguishing acute infl ammatory from chronic infl ammatory and fi brotic disease is pivotal to decide subsequently for an appropriate therapy, whether surgical or medical. MRE provides this information due to its capacity of tissue characterization. Thickening of the SB wall and submucosal edema with hyperin- tense signal on T2-weighted imaging, increased contrast medium uptake of the thickened SB wall and the depiction of enlarged, contrast-enhancing mesenteric lymphadenopathies are typical signs of active infl ammatory CD in MRE (Prasopoulos et al. 2001; Gourt- soyiannis et al. 2004). In contrast, fi brotic strictures of the SB wall are slightly hypointense on T2-weighted and SSFP images, show less contrast uptake, yield marked prestenotic dilatation, but are generally not associated with wall thickening. Since their appear- ance and signal characteristics are close to normal bowel wall, active SB distension with MRE is required to unveil these lesions as strictures (Umshcaden and Gasser 2003; Umschaden et al. 2000).

Both infl ammatory stenosis and fi brotic stricture in CD result in SB obstruction. Acute and chronic transmural infl ammation with stenosis and post-infl ammatory scar formation impair SB motility. Sub- tle, sub-occlusive disease may only be revealed with an increased volume charge as is provided in MRE. To disclose disturbances of SB motility and sub-occlusive disease, time-resolved dynamic information is obtained from MR-fl uoroscopy which is implemented

in MRE using rapid repetition of ultra-fast sequences [e.g., single-shot turbo-spin-echo (HASTE) or rapid acquisition with relaxation enhancement (RARE) sequences]. This technique permits to observe the propagation of the intra-luminal contrast medium and the subsequent dilatation of the SB. To date, the named sequences are both used as a projection technique and are clearly limited in spatial resolution.

23.5

Parallel Imaging Techniques and MRE

Numerous advantages can be anticipated from parallel imaging techniques in SB-MRE. Improving spatial resolution while reducing acquisition time creates options for 3D imaging, including 3D post-processing of the bowel, and may enable and foster the assessment of mucosal lesions – still a major limitation of MRE.

Respiratory and motion artefacts may be reduced at shorter acquisition time, and overall examination time can be shortened, limiting the period of patients’ dis- comfort due to SB ﬁ lling to a minimum.

To implement SB-MRE with parallel imaging, ideally a 32-channel whole-body MRI system is required. The typical setting for SB-MRE with parallel imaging includes two 6-element phased-array body coils to cover the entire abdomen anteriorly and a 12-element spine array coil posteriorly (Fig. 23.1a).

Providing this coil setting, parallel acquisition can be performed in two dimensions by applying a parallel imaging acceleration factor of R=3 in the left-right direction (phase-encoding direction) and an accel- eration factor of R=2 in the anterior-posterior direc- tion (partition direction) (Fig. 23.1b), which results in a total nominal 2D acceleration factor of 6.

The image reconstruction in phase-encoding direction is based on the generalized partially parallel acquisition technique (GRAPPA) (Griswold et al. 2002). This reconstruction algorithm requires the measurement of a total of 24 reference lines to determine the coil proﬁ les. In the anterior-posterior direction, the image reconstruction is performed in the image domain using a SENSE-like algorithm and a total of 64 reference lines. The integrated acquisition of the reference lines reduces the effective acceleration of parallel imaging in both the phase- encoding and the partition direction. Thus, the effective acceleration factor in phase-encoding direction is 2.53 (nominal acceleration factor R=3); in partition

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direction it is 1.24 (nominal acceleration factor R=2).

Hence, under these conditions with 2D parallel imag- ing, a total effective acceleration factor of R_eff=3.13 can be achieved. One of the ﬁ rst sequences for abdominal MRI that employs parallel imaging in two dimensions with acceleration factors greater than 3 is the recently introduced 3D-TrueFISP sequence.

23.6

3D-TrueFISP with 2D Parallel Imaging

Steady-state free-precession sequences such as TrueFISP are particularly valuable and have been recommended for SB imaging with MRE (Gourtsoyiannis et al. 2002;

Prasopoulos et al. 2001; Gourtsoyiannis et al. 2000), since they have a very distinct signal behavior with both T1 and T2 signal properties and an individual intrinsic chemical-shift effect (also called “ink artefacts”), result-

ing in an excellent soft tissue contrast (Prasopoulos et al. 2001). Therefore, the introduction of a 3D-TrueFISP sequence with parallel imaging is of particular importance for SB imaging and MRE, opening promising options of image quality improvement.

High-resolution 3D-TrueFISP imaging with 2D parallel imaging at a nominal acceleration factor of 6 can be performed within one single breath-hold of 18 s, covering the entire abdomen and providing an isotropic spatial resolution of 1.8×1.8×1.8 mm³ (Fig. 23.2). Due to the isotropic properties of this 3D-TrueFISP sequence, 3D post-processing tools can be applied to create maxi- mum-intensity projections (MIP), multi-planar refor- mations (MPR) in any arbitrary plane and so-called curved reformats (CR) (Fig. 23.3a,b). Curved reformats allow transforming curvilinear, tortuous structures into virtually linear structures on two-dimensional presen- tations. For 3D post-processing, the 3D source images are transferred to a commercially available dedicated post-processing workstation (e.g., Leonardo, Siemens Medical systems, Erlangen, Germany).

Fig. 23.1a,b. Coil arrangement and parallel-acquisition setup in 3D-TrueFISP imaging of the small bowel using two-dimensional parallel imaging with a nominal acceleration factor of 6:

(a) A total of 24 array coil elements arranged in four rings are used in small-bowel imaging with parallel acquisition techniques, each ring consisting of three body-array and three spine-array coil elements. (b) A parallel-imaging acceleration factor of 3 is applied in left-right direction (phase-encoding direction) and an acceleration factor of 2 in the anterior-posterior direction (partition direction) resulting in a total nominal acceleration factor of R=6

b a

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23.7

Clinical Impact of High-Resolution 3D-True- FISP and 3D Post-Processing

3D post-processing in 3D-TrueFISP imaging is dis- tinctly helpful in many issues of SB disease. Accord- ing to a recent preliminary study, 3D post-processing yields additional diagnostic information in up to 77%

of all patients (Herrmann et al. 2006b). This additional information has relevant diagnostic impact in therapeutic decision making in more than 54% of the cases. Both CR and MRP contribute to this result; the combination of both is the most effective.

In the assessment of CD on standard coronal or transverse images, the exact length of stenosis may be difﬁ cult to determine if a long segment of SB is affected and has a tortuous course within the abdominal cavity. In these cases, 3D post-processing with CRs is most helpful. An interactive tool is used to trace the course of the bowel loop manually within the 3D data set (Fig. 23.3a). The curvilinear course of the bowel segment is then virtually “straightened” and “unfold- ed” and displayed as a linear structure (Fig. 23.3B) The planar presentation of the affected bowel segment facilitates the exact measurement of the length of a stenosis (Fig. 23.3b), which may be relevant in the decision making for a potential surgical intervention.

Likewise, CRs support the assessment of mucosal ﬁ s- sures and ulcera in rendering them more conspicuous on linear planar images (Fig. 23.3b) (Herrmann et al.

2006b). Especially in the terminal ileum, applying CRs has major impact on diagnosing the presence of CD while improving the evaluation of the mucosa.

In a complex arrangement of bowel loops affected with CD, also known as “inﬂ ammatory pseudo-tumors” or “conglomerate tumors” in CD, CRs and MPRs are particularly useful and capable of adding relevant information in better depicting the local extent and involvement of adjacent structures and providing a better orientation within the abdominal cavity.

In the presence of complex internal entero-enteric fi stula, MPR can be adjusted to the course of the fi stulous tract and show the origin and the site where the fi stulous tract abuts the distal target organ. Likewise, the point of departure of complications such as abscesses may be clarifi ed more easily with appropriate orientation of MPR planes (Fig. 23.4b).

In neoplastic disease of the bowel, MPRs have proven to be useful in the assessment of the tumor extent and inﬁ ltration into adjacent structures (Her- rmann et al. 2006b). Extra-luminal inﬁ ltration into

the mesentery or other structures is best disclosed on MPRs strictly orthogonal to the bowel lumen.

To successfully apply 3D post-processing tools and obtain these results, the bowel has to be fully distend- ed. This is why the authors emphasize the importance of SB distension as an indispensable prerequisite for high-resolution imaging with 3D-TrueFISP including these options for 3D post-processing.

23.8

Future Improvement and Perspectives of SB Imaging with MRE and Parallel MRI

Parallel-imaging techniques and a higher ﬁ eld strength of 3 T are generally considered ideal mu- tual adjuncts since higher signal at 3 T compensates for the noise induced in parallel imaging techniques.

Yet, TrueFISP imaging at 3 T suffers from distinct

Fig. 23.2. High-resolution 3D-TrueFISP imaging with 2D paral- lel imaging and an acceleration factor of R=6: Coronal view of an MR-enteroclysis with biphasic intra-luminal contrast (0.5%

methyl-cellulose solution) in the small (small short arrows) and large bowel (large short arrows). The jejunal fold pattern (small short arrows) and the less pronounced ileal folds (small long arrow) are very well depicted due to the high spatial reso- lution of 1.8×1.8×1.8 mm³ with isotropic voxel size

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artefacts due to more pronounced sensitivity to sus- ceptibility effects. Therefore, the issue of TrueFISP imaging at 3 T has to be addressed before integrating SB imaging into a 3 T clinical setting.

In contrast, parallel imaging at 3 T now offers further reﬁ nement of other imaging sequences such as T1-weighted fat-saturated gradient-echo images (e.g., VIBE sequence and volume-interpolated breath-hold examination sequences), generally used for contrast-enhanced SB imaging after intra- venous application of gadolinium. These sequences can now be acquired with isotropic voxel size, so that 3D post-processing is also applicable to these

sequences. To date, 3D GRE sequences have proven their usefulness in MR-colonoscopy (Debatin and Lauenstein 2003). According to some preliminary experience, better signal-to-noise ratios and higher spatial resolution can be achieved with parallel imaging and 3 T for this application. In the future, increased spatial resolution and further improvements in terms of image quality of TrueFISP imaging holds great promise of improving the assessment of mucosal lesions in CD. MRE would then evolve to be a comprehensive diagnostic tool in the diagnostic workup of CD, covering its entire spectrum of mac- roscopic clinical presentation.

Fig. 23.3a,b. Curved reformat (CR): The tortuous and convo- luted course of a long-segment infl amed and stenosed small- bowel loop is manually traced within the 3D data set (a, yellow line) to create the CR. Most of the course of the traced small- bowel loop is outside the shown image plane but is indicated by the yellow line. The long-segment stenosis is presented in a linear planar fashion (b, proximal to distal from right to left) depicting more clearly the mucosal ulcera and cobble- stone pattern (b, small white arrows) as compared to normal mucosa. The linear planar presentation facilitates the exact measurement of the length of stenosis and of the prestenotic dilatation in the middle ileum (b, large white arrow). The small white arrowhead b indicates the air-fl uid level in the terminal ileum which, at that time, was fi lled with air.

a

b

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