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Original Research |
1 Department of Radiology, University College Hospital, Newcastle Rd., Galway,
Ireland.
2 Present address: Department of Radiological Sciences, David Geffen School of
Medicine, University of California, Los Angeles, 10945 Le Conte Ave., Peter V.
Ueberroth Bldg., Ste. 3371, Los Angeles, CA 90095-7206.
Received June 12, 2007;
accepted after revision August 22, 2007.
Address correspondence to D. G. Lohan.
Abstract
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MATERIALS AND METHODS. Over a 54-month period, 10 patients with subsequently confirmed small-bowel lymphoma were imaged using a standardized MR enterography technique. Retrospective chart review was performed to detect associated disease processes, such as celiac disease. The morphologic characteristics of each segment with lymphomatous involvement were evaluated with respect to tumor location, tumor size, mural characteristics, fold features, loop dilatation, luminal stricturing, mesenteric or antimesenteric distribution, mesenteric involvement, and signal intensity.
RESULTS. Nineteen distinct segments of lymphomatous involvement were identified in 10 patients, and underlying celiac disease was confirmed in six of the 10 patients. This patient group comprised 10 patients with non-Hodgkin's lymphoma (NHL) of various subtypes. No cases of Hodgkin's lymphoma were encountered. Analysis revealed celiac NHL enteropathy to have a tendency toward localization to a single, long (> 10 cm), smooth continuous bowel segment, often with aneurysmal loop dilatation, in the absence of a distinct mesenteric or antimesenteric distribution. Luminal stricturing was encountered in cases of low-grade lymphoma, whereas mesenteric fat infiltration represented a characteristic of high-grade disease.
CONCLUSION. We describe the characteristics of small-bowel lymphoma on MR enterography, identifying a number of key features that may help the interpreting radiologist in suggesting the underlying histologic subtype and whether the presence of underlying celiac disease is likely.
Keywords: celiac disease • imaging–histology correlation • lymphoma • MR enterography • MRI • small bowel
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Few anatomic systems have experienced the benefit of these technologic advances to the same degree as the gastrointestinal system. This is particularly the case with MR interrogation of the small bowel, a relatively inaccessible region that has eluded physicians and radiologists alike throughout medical history. Indeed, before the advent of cross-sectional imaging, the presence of small-bowel disease was inferred by its effect on the small-bowel lumen during the course of conventional small-bowel enterography or enteroclysis. MDCT offered a reasonable alternative imaging solution, although with the penalty of necessitating potentially nephrotoxic iodine-based contrast medium injection and involving considerable ionizing radiation exposure, thus precluding repeated temporal imaging and hence assessment of small-bowel peristaltic activity. As a result, the considerable attributes of MRI described have renewed interest in small-bowel imaging, with studies evaluating the utility of various potential small-bowel MR enterography contrast media and their application to a number of suspected small-bowel diseases dominating the current literature.
Tumors of the small bowel account for 1–2% of all gastrointestinal neoplasms (0.3% of all neoplasms) and as a result are usually misdiagnosed on initial presentation or diagnosed late in the disease process [1, 2]. Small-bowel lymphoma, be it of primary origin or, more commonly, a secondary feature of systemic disease, represents approximately 16% of these tumors [3]. Small-bowel lymphoma occurs most commonly as a manifestation of its non-Hodgkin's B-cell histologic subtype and is suspected to arise from mucosa-associated lymphoid tissue (MALT) [4, 5]. T-cell lymphoma, particularly that of the small bowel, is considerably less prevalent [6] and is associated with the concomitant presence of celiac disease, a condition that is endemic to the west of Ireland in most cases (enteropathy-associated T-cell lymphoma) [7].
To the best of our knowledge, the imaging characteristics of small-bowel lymphoma have not previously been described at MR enterography. We present 10 patients with small-bowel lymphoma, derived from a population in whom the underlying prevalence of celiac disease is elevated, to illustrate the features and distribution of lymphomatous involvement, while attempting to identify key morphologic traits capable of providing an association between imaging manifestation and likely histologic diagnosis.
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Examination Technique
All examinations were performed using a single protocol that was unchanged
over the protracted course of the study period. Patients, all of whom fasted
for 8 hours before the examination, were instructed to ingest a single sachet
of polyethylene glycol (Klean-Prep, Norgine) diluted in 1,000 mL of water and
a small amount of orange flavor cordial, added to optimize patient tolerance,
over a period of 45 minutes immediately before scanning.
MR enterography examinations were performed on a 1.5-T system (Magnetom Symphony, Siemens Medical Solutions) equipped with high-performance gradient coils characterized by a maximum gradient amplitude of 52 mT/m and a slew rate of 125 T/m/s. Large flexible surface coils were, in addition, used for signal optimization. Imaging parameters for coronal true fast imaging with steady-state precession (FISP) sequences were a TR/TE of 4.42/2.36; number of signal averages, 1; flip angle, 70°; base resolution, 256; phase resolution, 100; field-of-view (FOV) read, 320 mm; FOV phase, 75 mm; slice thickness, 8 mm; and distance factor, 20. For axial true FISP sequences, the imaging parameters were as follows: 4.62/2.31; number of signal averages, 1; flip angle, 70°; base resolution, 350; phase resolution, 100; FOV read, 320 mm; FOV phase, 75; slice thickness, 5 mm; and distance factor, 20. Coronal and axial 2D images encompassing the entire abdomen and pelvis were obtained with the patient in the supine position using a T2-weighted true FISP sequence. The first series of images were obtained 20 minutes after completion of contrast medium ingestion. A second series was acquired 40 minutes after ingestion, and if the oral contrast medium had not reached the cecum at that time, imaging was repeated at 20-minute intervals until an adequate amount of the contrast bolus was deemed to have passed to the colon. If necessary, additional projections and sequences were performed.
Image Analysis
The MR enterography examinations of patients with subsequent histologic
confirmation of lymphomatous involvement were evaluated by two experienced
abdominal imaging radiologists who were blinded to the patients' underlying
histologic diagnoses. Each study was analyzed for a number of qualitative and
quantitative criteria including tumor location, tumor size, mural
characteristics, fold features, loop dilatation, luminal stricturing,
mesenteric or antimesenteric distribution, mesenteric involvement, and signal
intensity. Discrepancies in morphologic characterization were settled by
consensus.
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Ten patients with histologically confirmed primary small-bowel lymphoma (four primary and six secondary) were imaged during the study period (four men and six women; mean age, 61.4 years; age range, 44–85 years) (Table 1). Nineteen distinct segments of lymphomatous involvement were identified in this patient population. The presence of celiac disease had been previously documented, with histologic confirmation, in four patients and was subsequently confirmed on endoscopic biopsy in an additional two patients for a total of six patients with celiac disease.
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Histologic Classification
This patient group comprised 10 patients with non-Hodgkin's lymphoma (NHL)
of various subtypes including those of B-cell origin seen in six patients
(low-grade NHL in four patients, including follicular NHL in two and MALT
lymphoma in one; intermediate- to high-grade follicular NHL in one patient;
and high-grade NHL in one patient) and those of T-cell origin in four
patients, all of whom were confirmed to have celiac high-grade NHL. No
instances of small-bowel Hodgkin's lymphoma were encountered. Of the six
patients with underlying celiac disease, four developed high-grade T-cell NHL
(enteropathy-associated T-cell lymphoma), with one each of low-grade
follicular and low-grade MALT lymphoma subtypes of B-cell NHL.
Location
Lymphomatous involvement was localized to a single segment of small bowel
in five of the 10 patients—namely, the duodenum in one patient and the
jejunum and ileum in two patients each. Celiac disease was an underlying
disease process in four of these patients. The additional patient reported no
clinical symptoms to suspect celiac disease, although jejunal endoscopic
evaluation and biopsy were not performed.
In the remaining five patients, multiple sites of lymphomatous infiltration were observed; a unifying feature was the presence of ileal involvement, which was seen in all cases. Only two patients (patients 5 and 6 in Table 1) with celiac disease were observed as having more than one site of involvement (Figs. 1A, 1B and 2).
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Mural Characteristics
Circumferential serosal-surface mural involvement was identified in at
least one small-bowel segment in all 10 patients. In half of these patients
(n = 5), circumferential infiltration was eccentric, with marginal
irregularity being a common accompanying feature. Notably, a smooth marginal
component was identified in six patients, all of whom were known to have
underlying celiac disease (Fig.
4A,
4B). This feature was not
identified in any patient in whom a diagnosis of celiac disease had not been
established (Fig. 5A,
5B). Furthermore, a smooth
serosal contour was identified in patients with both T-cell and B-cell NHL in
the presence of celiac disease, suggesting that this morphologic
characteristic is likely a manifestation of celiac disease rather than the
most commonly encountered lymphoma subtype in this group—namely, T-cell
NHL.
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Loop Dilatation
Aneurysmal small-bowel loop dilatation was observed in 12 segments, in
association with thickening of regional mucosal folds in 75% of instances
(n = 9) (Fig. 5A,
5B). Diffuse segmental bowel
loop dilatation was identified in seven segments in six patients, all of whom
were known to have underlying celiac disease. Furthermore, this morphologic
feature was absent in only one of nine diseased segments identified in this
patient group. Diffuse loop dilatation was not identified in the absence of
celiac disease.
Luminal Stricturing
This feature was identified in six small-bowel segments, three of which
occurred in a single individual (patient 2). Of these six segments, five were
present in patients with low-grade disease, B-cell in four and T-cell in two.
A single instance of luminal compromise occurring in the presence of
intermediate- or high-grade disease was identified in an individual with
celiac T-cell NHL (patient 10) (Fig.
6).
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Mesenteric Involvement
Mesenteric lymphadenopathy in the form of distinct nodal enlargement was
seen in only one patient. Discrete nodal masses were seen in two additional
patients, measuring 9.4 and 6.5 cm in long-axis diameter, respectively (Fig.
8A,
8B). Another three patients
were identified as having adjacent lymphomatous mesenteric fat infiltration in
the absence of distinct soft-tissue deposition (Fig.
9A,
9B). Interestingly, mesenteric
fat infiltration was identified only in patients with high-grade NHL, B-cell
subtype in one patient and T-cell subtype in two patients.
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The mean signal intensity of B-cell NHL lesions was 134 ± 40.5 AU, whereas that for T-cell NHL lesions was 178 ± 80.8 AU; the difference between these mean values failed to reach statistical significance (p = 0.3). In addition, the signal intensity difference between lesions occurring in patients with and without concurrent celiac disease was not of statistical significance (p = 0.45).
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Analysis of the varying morphologic characteristics observed yields a number of interesting findings, many of which pertain to patients with NHL and underlying celiac disease, representing 60% of the cases in this series. NHL was T-cell subtype and was high grade in four of these six patients, reflecting the predilection of this histologic subtype to develop in patients with celiac disease. As illustrated, celiac NHL enteropathy had a tendency toward localization to a single small-bowel segment, representing four of six such cases in our patient population. The extent of continuous segmental involvement also differed considerably between those with and those without underlying celiac sprue, with a tendency toward longer segmental involvement in the presence of this disease state. Indeed, the use of a cutoff criterion of at least one segment with 10 cm of continuous pathologic abnormality at MR enterography yields 100% accuracy and positive and negative predictive values for the presence of celiac disease.
An association was also observed between certain mural characteristics and the presence of celiac disease, most notably that of a smooth marginal component, being observed in at least one diseased segment in each patient with this condition in our patient population. Diffuse segmental small-bowel loop dilatation was identified in seven segments in six patients in our patient group, all of whom were known to have underlying celiac disease. Significantly, neither a smooth mural component nor aneurysmal loop dilatation was observed in a single segment in the absence of concurrent celiac disease, likely a reflection of the generalized hypotonia known to exist in the presence of this condition. The pattern of disease distribution was also seen to be of value in assessing the potential for underlying celiac disease: The absence of a distinct mesenteric or antimesenteric predominance had a 100% positive predictive value and 88.8% negative predictive value for underlying celiac disease in this patient population.
Luminal stricturing, as described earlier, was identified in six small-bowel segments, five of which were present in patients with low-grade disease of both B- and T-cell subtypes. However, three of the six segments occurred in a single patient. Nonetheless, these findings suggest that this entity may perhaps be regarded as a manifestation of indolent, slow-growing disease with associated subclinical or chronic symptoms and resultant delay in diagnosis.
Mesenteric involvement, be it in the form of diffuse fat infiltration or distinct nodal or masslike deposition, is a relatively common accompanying feature of systemic lymphoma. Indeed, only four of 10 patients in our series showed no evidence to suggest some form of mesenteric involvement. Although discrete or diffuse lymphadenopathy proved to be of little value in determination of disease subtype, mesenteric fat infiltration was seen in 30%, all of whom had histologically confirmed high-grade NHL.
The signal intensity of small-bowel NHL proved consistently and significantly higher than that of adjacent psoas muscle on unenhanced T2 steady-state free precession (SSFP) imaging. No such statistical difference was observed when the signal intensity of diseased segments was compared with that of spleen, although such a comparison may be flawed by the presence of occult splenic lymphomatous involvement, thus influencing the signal intensity of the spleen. Therefore, we suggest comparing the signal intensity of diseased small bowel with that of psoas muscle for the greatest diagnostic accuracy; however, bear in mind that, although extremely rare, skeletal muscle involvement by systemic lymphoma has been reported in the literature [9].
A number of key conclusions can be drawn on the basis of the imaging features described. The feasibility of accurate depiction of small-bowel abnormalities—irrespective of anatomic location, extent, and morphologic distortion—has been repeatedly shown [10, 11]. Indeed, the role of MRI in the detection of celiac disease and the MR enterography appearances of celiac disease in the absence of concomitant lymphoma have recently been described [12, 13]. Our findings, which are based on high-resolution diagnostic-quality studies obtained in all cases, echo those of these studies. MR enterography allows concurrent evaluation of luminal integrity, mural deformity, and distant extraluminal disease extent. The orally ingested contrast preparation was well tolerated by all patients, and no significant adverse effect was seen. However, we propose that this imaging technique may be of value in suggesting the potential histologic grade and the likely presence or absence of concomitant celiac disease. As we discussed, we have observed a correlation between small-bowel luminal stricturing and the presence of low-grade disease, be it of the B- or T-cell subtype. Furthermore, mesenteric fat infiltration in the absence of discrete lymphadenopathy was observed in relation to the presence of high-grade NHL. Evaluation of larger patient populations is required in the future for further elucidation of these suggested associations.
Our proposals are perhaps more compelling with regard to the diagnosis of underlying celiac disease in patients with small-bowel lymphoma. Involvement of a single small-bowel segment, particularly when exceeding a longitudinal distance of 10 cm, appears highly predictive of celiac disease. Smooth mural contour, diffuse segmental bowel loop aneurysmal dilatation, and absence of a distinct mesenteric or antimesenteric distribution, as described, are highly suggestive of the presence of lymphoma occurring on a background of celiac sprue.
We recognize the limitations in our study design—namely, the absence of upper gastrointestinal endoscopic exclusion of celiac disease in all cases, low patient numbers, and lack of gadolinium contrast administration. However, detailed clinical histories were obtained and physical examinations were performed in all patients, and endoscopic evaluation was performed at the discretion of the referring clinician based on the index of suspicion for the presence of celiac disease. Furthermore, small-bowel lymphoma, be it primary or secondary, is a rare entity, thus impacting the potential for large patient series and precluding derivation of definite pathologic diagnosis based on the imaging features encountered. However, the purpose of this study was to describe findings of potential value in the suggestion of likely histologic diagnosis rather than to find a replacement of the gold standard biopsy in the characterization of a pathologic lesion. Also, in most centers, routine MR enterography examinations do not involve IV contrast administration, as is our departmental policy.
In conclusion, MR enterography is a versatile, highly diagnostic, and accurate technique in the evaluation of small-bowel lymphoma that allows confident regional and mesenteric assessment. Certain morphologic characteristics, as described, may be of value in the suggestion of likely histologic subtype, although ultimately confirmation of the presence of this disease and of the cellular characteristics of this disease process continues to rest with histologic analysis.
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