Normal small bowel wall characteristics on MR enterography

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European Journal of Radiology 75 (2010) 207–211

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European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad

Normal small bowel wall characteristics on MR enterography Carmel G. Cronin ∗ , Eithne Delappe, Derek G. Lohan, Clare Roche, Joseph M. Murphy Department of Radiology, University College Hospital, Galway, Ireland

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Article history: Received 29 September 2008 Received in revised form 24 April 2009 Accepted 24 April 2009 Keywords: MR enterography MR small bowel follow through Small bowel Normal small bowel diameter

a b s t r a c t Purpose: To assess the normal small bowel parameters, namely bowel diameter, bowel wall thickness, number of folds (valvulae connivientes) per 2.5 cm (in.), fold thickness and interfold distance per small bowel segment (duodenum, jejunum, proximal ileum, distal ileum and terminal ileum) on MR enterography. Materials and methods: Between September 2003 and January 2008, 280 MR enterography examinations were performed for investigation of known or suspected small bowel pathology. 120 of these examinations were normal. Sixty-five (m = 29, f = 36, mean age = 34 years, range = 17–73 years) of 120 examinations without a prior small bowel diagnosis, with no prior or subsequent abnormal radiology or endoscopy examinations, no prior small bowel surgery and with a minimum 3 years follow-up demonstrating normality were retrospectively evaluated for the described small bowel parameters. Results: We found the mean diameter of the duodenum to be 24.8 mm (S.D. = 4.5 mm), jejunum to be 24.5 mm (S.D. = 4.2 mm), proximal ileum to be 19.5 mm (S.D. = 3.6 mm), distal ileum to be 18.9 mm (S.D. = 4.2 mm) and terminal ileum to be 18.7 mm (S.D. = 3.6 mm). The number of folds per 2.5 cm varied from 4.6 in the jejunum to 1.5 in the terminal ileum. The fold thickness varied from 2.1 mm in the duodenum to 1.8 mm in the terminal ileum. The small bowel parameters gradually decreased in size from the duodenum to the smallest measurements which were in the terminal ileum. The bowel wall is similar in size throughout the small bowel measuring 1.5 ± 0.5 mm. Conclusion: These results provide the mean, range of normality and standard deviation of the small bowel parameters per segment on the current population on MR enterography. From our experience, knowledge of these parameters is extremely helpful and essential in the everyday assessment of MR enterography studies. © 2009 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Diseases of the small bowel manifest as bowel dilation, small bowel wall thickening and fold (valvulae connivientes) abnormalities such as thickening, separation, blunting, flattening and straightening [1]. Most of the known small bowel pathologies can occur in any small bowel segment and can result in a number of morphological changes. This highlights the importance of a detailed understanding of the normal small bowel anatomy and establishment of the normal small bowel parameter measurements for each small bowel segment to aid small bowel assessment and decipher normal from abnormal bowel. Traditionally conventional enteroclysis (CE) was the gold standard for evaluating the small bowel. With advances in MR technology and faster imaging sequences, MR steady state free pre-

∗ Corresponding author. Tel.: +353 91 544857; fax: +353 91 521197. E-mail address: [email protected] (C.G. Cronin). 0720-048X/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2009.04.066

cession (SSFP) imaging can be performed in seconds with a short total imaging duration. MR enterography/MR small bowel follow through is an evolving, promising diagnostic tool for the evaluation of the small bowel and offers a number of distinct advantages over its projectional and cross-sectional alternatives, including absence of associated ionizing radiation exposure, multiplanar imaging capabilities, superb contrast and temporal resolution and facilitation of sequential imaging over prolonged periods of time. The normal small bowel jejunum [2] and ileal diameters and small bowel fold appearances were established on conventional barium study radiographs a numbers of years ago [3,4]. However these plain radiographic measurements are subjected to a 30% magnification error and thus cannot be directly applied to MR enterography imaging. To our knowledge these normal small bowel mural and fold parameters have not been previously described in each small bowel segment to date. From our experience with MR enterography [10], knowledge of normal values and range of normality is extremely helpful and essential in the everyday assessment of MR enterography examinations, making this paper a valuable addition to the literature.

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2. Materials and methods Institutional review board approval was obtained. 2.1. Study population Between September 2003 and January 2008, 280 MR enterography examinations were performed for investigation of known or suspected small bowel pathology. Retrospective chart analysis was also performed, gathering information regarding patient symptoms, indication for the MR enterography examination, pre-existing conditions and correlating investigational results in 120 patients with normal examinations. Sixty-five (m = 29, f = 36, mean age = 34 years, range = 17–73 years) of 120 patient examinations who were normal (no prior small bowel diagnosis, no prior small bowel surgery, no prior or subsequent abnormal radiology or endoscopy examination), with a minimum 3 years follow-up demonstrating normality and studies of diagnostic quality were retrospectively evaluated for assessment of the described small bowel parameters. The currently analyzed group is from a similar database to previous papers [5–10] however this study is unique in its objective of assessing normal small bowel parameters.

Fig. 1. Axial MR enterography image demonstrating a well distended duodenum. The duodenal wall, lumen and fold pattern are visualized.

2.2. Patient preparation 2.4. Image analysis All patients are instructed to fast from the preceding midnight. No bowel preparation, medications to promote gastric emptying, bowel relaxation or paramagnetic contrast agents were administered prior to or during image acquisition. Bowel distension was achieved using a previously described technique [5–9] involving oral ingestion of a single packet of polyethylene glycol (PEG) solution (Klean Prep, Norgine, Middlesex, UK) diluted in 1000 mL of water and a small amount of orange flavoring, added to render the mixture more palatable. This solution was ingested over a 10–15-min period, as permitted by patient tolerance. PEG is a highosmolarity, non-absorbed contrast medium that provides exquisite intraluminal contrast and luminal distension (PEG Macrogol 3350 59.0 g, anhydrous sodium sulphate 5.685 g; sodium bicarbonate 1.685 g; sodium chloride 1.465 g; potassium chloride 0.7425 g). All patients are provided with an information sheet detailing the procedure and the potential risk of diarrhea due to PEG prior to their appointment. 2.3. Imaging technique Initial images are obtained 20 min after contrast ingestion [5–9]. Delayed repeat imaging was performed as required until the contrast bolus has passed to the colon. Study ‘completion’ is defined as the presence of a contrast medium bolus within the cecum or further distally, having achieved prior diagnostic-quality distension of the small bowel throughout its length. All studies were performed on a single Symphony 1.5 T MRI System (Siemens Medical Solutions, Erlangen, Germany) 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). A phased array body coil was also employed for optimization of signal reception. Multiplanar rapid localizers were followed by 2D steady state free precession (SSFP – true-FISP) sequences, acquired in the coronal and axial planes and encompassing from the diaphragmatic apex to the groins in craniocaudal extent. These true-FISP acquisitions incorporated the following parameters: repetition time (TR)/echo time (TE) 4.6 ms/2.3 ms, flip angle 70◦ , matrix 205 × 256, field of view 400 mm × 400 mm. A slice thickness of 5 mm enabled 19 sections to be obtained within 21 s. Breath holding was not required.

The images were reviewed on a PACS (Picture Achieving and Communication System, Agfa, Belgium)-workstation without compression. Images were blindly and qualitatively evaluated with regard to degree of small bowel distention using a Visual Assessment Grading Scale that ranged from 1 to 3, as validated in prior studies [7,10,11]. A score of 1 was taken to represent poor distention, 2 moderate distention and 3 excellent small bowel distention. Scores of 2 or 3 were taken to indicate an examination of ‘diagnostic quality’—only studies of diagnostic quality were assessed for the small bowel parameter. For the purposes of data recording and analysis the small bowel was divided into five main segments: the duodenum (Fig. 1), jejunum (Fig. 2), proximal ileum (to the left of midline) (Fig. 3), distal ileum (to the right of midline) (Figs. 3 and 4) and terminal ileum (Fig. 4). We measured the small bowel diameter, bowel wall thickness, number of folds (valvulae connivientes) per 2.5 cm, fold thickness and interfold distance in each segment. The measurements were taken at right angles to the parallel margins of the

Fig. 2. Coronal MR enterography coronal image of the jejunum demonstrating a normal mucosal, mural and fold pattern which are well visualized.

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diameter measurements. Barium studies had not been performed on the patients in the same time period of the MR examination, therefore comparison with plain radiograph measurements was not possible. 2.5. Statistical analysis SPSS Version 14 was used for statistical analysis. A one sample KS (Kolmogorov–Smirov) test was used to assess if our data set was a normal data set—this test confirmed that our data were not significantly different from a normal data set. Mean, standard deviation and range values were calculated. Pearson’s correlation coefficient was used to assess if the bowel diameter measurements varied with age. A p value of less than 0.05 was considered to indicate a statistically significant difference. Inter-observer agreement was estimated by Kappa coefficient. 3. Results All examinations evaluated were of moderate to excellent distension and all were of diagnostic quality (evaluated by a radiologist). Examinations showed no morphologic abnormalities or evidence of pathology. On review of the clinical and radiological records these patients had no subsequent small bowel disorders diagnosed at follow-up which ranged from 36 to 69 months (average 43 months). Inter-observer agreement was sufficient (Ä = 0.65). Tables 1–5 outline the mean, standard deviation and range of normal values based on this imaging modality—MR enterography. We found an average diameter in the duodenum of 24.8 mm

Fig. 3. Coronal MR enterography image of the normal distal ileum with fewer folds visualized in comparison to that of the jejunum and duodenum.

bowel [2]. We used the mean value of three measurements as the measured value. The interfold distance was measured at the fold base at bowel wall. Two observers performed all the measurements. Inter-observer variability was assessed in 25% of the bowel and fold

Table 1 Mean, standard deviation and range of normal values for the duodenal parameters (duodenal diameter, duodenal wall thickness, number of folds per 2.5 cm in the duodenum, duodenal fold thickness, duodenal interfold distance) based on MR enterography (millimeters). Duodenum diameter

Duodenum wall thickness

Fold number per 2.5 cm

Duodenum fold thickness

Duodenum interfold distance

65 0

65 0

65 0

65 0

65 0

N Valid Missing Mean Std. deviation Minimum Maximum

24.842 4.5468 17.1 35.0

1.525 0.5835 0.9 3.2

4.555 0.7253 3.0 6.0

2.108 0.5727 0.9 3.3

4.700 1.5406 2.6 9.7

Table 2 Mean, standard deviation and range of normal values for the jejunum parameters (jejunum diameter, jejunum wall thickness, number of folds per 2.5 cm in the jejunum, jejunum fold thickness, and jejunum interfold distance) based on MR enterography (millimeters). Jejunum diameter

Jejunum wall thickness

Fold number per 2.5 cm

Jejunal fold thickness

Jejunal interfold distance

65 0

65 0

65 0

65 0

65 0

N Valid Missing Mean Std. deviation Minimum Maximum

24.2572 4.25 15.00 32.00

1.501 0.5455 .90 3.10

4.67 0.83 2.00 7.00

2.20 0.66 1.00 4.20

4.59 3.56 2.00 31.00

Table 3 Mean, standard deviation and range of normal values for the proximal ileum parameters (proximal ileum diameter, proximal ileum wall thickness, number of folds per 2.5 cm in the proximal ileum, proximal ileum fold thickness, and proximal ileum interfold distance) based on MR enterography (millimeters). Proximal ileum diameter

Proximal ileum wall thickness

Fold number per 2.5 cm

Proximal ileum fold thickness

Proximal ileum interfold distance

65 0

65 0

65 0

65 0

65 0

N Valid Missing Mean Std. deviation Minimum Maximum

19.51 3.61 12.50 28.00

1.61 0.466 0.9 2.70

1.85 0.63 1.00 3.00

1.95 0.521 1.00 3.10

16.8 6.75 6.10 32.80

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Table 4 Mean, standard deviation and range of normal values for the distal ileum parameters (distal ileum diameter, distal ileum wall thickness, number of folds per 2.5 cm in the distal ileum, distal ileum fold thickness, and distal ileum interfold distance) based on MR enterography (millimeters). Distal ileal diameter

Distal ileal wall thickness

Fold number per 2.5 cm

Distal ileal fold thickness

Distal ileal interfold distance

65 0

65 0

65 0

65 0

65 0

N Valid Missing Mean Std. deviation Minimum Maximum

18.95 4.26 11.00 31.00

1.44 0.48 0.80 2.50

1.604 0.56 1.00 3.00

1.808 0.501 1.00 3.40

18.5 7.183 9.00 35.50

Table 5 Mean, standard deviation and range of normal values for the terminal ileum parameters (terminal ileum diameter, terminal ileum wall thickness, number of folds per 2.5 cm in the terminal ileum, terminal ileum fold thickness, and terminal ileum interfold distance) based on MR enterography (millimeters). Terminal ileal diameter

Terminal ileal wall thickness

Fold number per 2.5 cm

Terminal ileal fold thickness

Terminal ileal interfold distance

65 0

65 0

65 0

65 0

65 0

N Valid Missing Mean Std. deviation Minimum Maximum

18.7 3.6 11.0 26.00

1.5 0.45 0.90 3.0

1.56 0.58 1.00 3.00

(S.D. = 4.5 mm), jejunum of 24.5 mm (S.D. = 4.2 mm), proximal ileum of 19.5 mm (S.D. = 3.6 mm), distal ileum of 18.9 mm (S.D. = 4.2 mm) and terminal ileum of 18.7 mm (S.D. = 3.6 mm) (Fig. 4). We found an average number of folds per 2.5 cm in the duodenum of 4.5 (S.D. = 0.7), jejunum of 4.6 (S.D. = 0.8), proximal ileum of 1.8 (S.D. = 0.6), distal ileum of 1.6 (S.D. = 0.5) and terminal ileum of 1.5 (S.D. = 0.6). We found an average fold diameter in the duodenum of 2.1 mm (S.D. = 0.6 mm), jejunum of 2.2 mm (S.D. = 0.7 mm), proximal ileum of 1.9 mm (S.D. = 0.5 mm), distal ileum of 1.9 mm (S.D. = 0.5 mm) and terminal ileum of 1.8 mm (S.D. = 0.4 mm). The duodenum and jejunum had similar bowel diameter, fold number, fold thickness and interfold distances. The bowel diameter, fold number, fold thickness and interfold distance gradually decreases in size to their smallest measurements in the terminal ileum. The proximal ileum, distal ileum and terminal ileum’s bowel diameter, fold number, fold thickness and interfold distance are not dissimilar. The small bowel wall thickness

Fig. 4. Coronal MR enterography image of the normal distal and terminal ileum with fewer folds visualized in comparison to that of the jejunum and duodenum.

1.85 0.40 1.00 3.30

17.91 7.86 8.00 35.00

is similar in size throughout the bowel measuring approximately 1.5 ± 0.5 mm. There is no statistical difference in the bowel diameter measurements over an age range from 17 to 73 which is confirmed with Pearson’s correlation (p = 0.7, 0.8, 0.8, 0.4, 0.3—Pearson’s correlation).

4. Discussion The small bowel is a common site of benign and malignant disease. Some diseases have a predilection for a particular location in the small bowel for example duodenitis, jejunitis and terminal ileitis. Other disease processes may affect any site, have a multifocal or diffuse pattern of involvement such as Crohn’s disease [8,12], celiac [3], primary malignancies and metastasis [13], lymphoma, radiation enteritis [14], pancreatitis, chronic renal failure, low albumin states and Zollinger–Ellison syndrome. Disease processes manifest as bowel dilation in mechanical obstruction, ileus and aneurismal tumor dilation. Small bowel wall and fold thickening, fold separation or fold loss occurs in tumor infiltration and inflammatory processes (Crohn’s, celiac, radiation enteritis, eosinophilic gastroenteropathy, bacteria, paracites and sclerosing encapsulating peritonitis). The overall fold pattern may be altered (thickened, separated, blunted, flattened and straightened) [1] or reversed as with ‘ileal jejenisation’ in celiac disease [3]. Pathological effects on the bowel wall and patterns of disease are an integral part of radiological diagnosis and monitoring [3,15]. Therefore knowledge of the normal bowel parameter measurements is paramount. We performed a complete analysis of the bowel wall and fold characteristics in all small bowel segments on MR SBFT imaging which to our knowledge has not been performed before. While jejunal and ileal diameter measurements have been established on plain radiographs at enteroclysis [2,4], the duodenum and terminal ileum parameters have not been measured on any modality. The ileum was previously assessed as a single unit, as there is a gradual transition in bowel features from the jejunum to the terminal ileum we divided the ileum into proximal (to the right of midline) and distal (to the left of midline) segments for a more complete evaluation.

C.G. Cronin et al. / European Journal of Radiology 75 (2010) 207–211

We found an average diameter in the duodenum of 24.9 mm (S.D. = 4.6 mm), jejunum of 24.2 mm (S.D. = 4.2 mm), proximal ileum of 19.5 mm (S.D. = 3.5 mm), distal ileum of 18.9 mm (S.D. = 4.2 mm) and terminal ileum of 18.7 mm (S.D. = 3.7 mm). Haworth et al. [2] had previously reported the jejunum to have a diameter of 23 mm on plain radiographs delineated by barium in a similar age group. This is similar to our finding. Pallotta et al. [16] assessed bowel diameter using ultrasound post-PEG ingestion. They found similar ileal diameter measurements to ours however the smaller jejenal diameter measurements. This study had less participants (n = 10) and is dissimilar to our as they used smaller volume of contrast (200–820 mL) over a longer time period for consumption (65 min). These factors may account for the difference in jejenal distension and diameters. We found no significant difference in the bowel segment diameters over the age range from 15 to 73 using Pearson’s correlation. This is similar to Haworth et al. [2] findings. Haworth et al. [2] assessed jejunal diameters at 6 months, 8 years, 15 years and adults, and found no statistical difference between the jejunal diameter measurements in a 15 year old and that of an adult. We have confirmed that there is no statistical difference in bowel diameter over the age range of 17–73 years in all small bowel segments. The mean patient age was 34 years (range 17–73). This is of importance as it outlines the young age of those requiring and undergoing small bowel investigations. The main limitation of this study is its retrospective nature. Furthermore such a study would ideally be performed on a normal cohort with out any symptoms; however we believe our population are normal as their MR studies were normal morphologically and no abnormalities’ were found on a minimum of 3 years of follow-up. 5. Conclusion These results provide the mean, standard deviation and range of normal small bowel parameters on the current population on MR enterography/MR small bowel follow through. Knowledge of the small bowel anatomy and its normal parameter values will be of benefit to each radiologist in their everyday assessments of the small bowel and will aid accurate diagnoses of bowel obstruction, bowel wall or fold thickening.

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