Hindawi Publishing Corporation

Gastroenterology Research and Practice

Volume 2012, Article ID 816920, 15 pages
doi:10.1155/2012/816920

Review Article
Crohn’s Disease Imaging: A Review

Gatta Gianluca,1 Di Grezia Graziella,1 Di Mizio Veronica,2 Landolfi Cinzia,3

Mansi Luigi,3 De Sio Ilario,4 Rotondo Antonio,1 and Grassi Roberto1
1 Radiology Department, Second University of Naples, 80138 Naples, Italy
2 San Massimo Hospital, 65017 Penne, Italy
3 Nuclear Medicine Department, Second University of Naples, 80138 Naples, Italy
4 Gastroenterology Department, Second University of Naples, 80138 Naples, Italy

Correspondence should be addressed to Di Grezia Graziella, [email protected]

Received 20 August 2011; Revised 10 October 2011; Accepted 10 October 2011

Academic Editor: P. Gionchetti

Copyright © 2012 Gatta Gianluca et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Crohn’s disease is a chronic granulomatous inflammatory disease of the gastrointestinal tract, which can involve almost any seg-
ment from the mouth to the anus. Typically, Crohn’s lesions attain segmental and asynchronous distribution with varying levels of
seriousness, although the sites most frequently involved are the terminal ileum and the proximal colon. A single gold standard for
the diagnosis of CD is not available and the diagnosis of CD is confirmed by clinical evaluation and a combination of endoscopic,
histological, radiological, and/or biochemical investigations. In recent years, many studies have been performed to investigate the
diagnostic potential of less invasive and more patient-friendly imaging modalities in the evaluation of Crohn’s disease includ-
ing conventional enteroclysis, ultrasonography, color-power Doppler, contrast-enhanced ultrasonography, multidetector CT ente-
roclysis, MRI enteroclysis, and 99mTc-HMPAO-labeled leukocyte scintigraphy. The potential diagnostic role of each imaging
modality has to be considered in different clinical degrees of the disease, because there is no single imaging technique that allows a
correct diagnosis and may be performed with similar results in every institution. The aim of this paper is to point out the advan-
tages and limitations of the various imaging techniques in patients with suspected or proven Crohn’s disease.

1. Conventional Enteroclysis (CE) Radiologic findings include irregular thickening and dis-
tortion of the valvulae conniventes, loops adhesions (mass-
Conventional enteroclysis is generally performed according like effect), or separated loops because of wall thickening and
to the technique established by Herlinger [1]. mesenteric inflammatory infiltration [5] (Figure 1).
A nasoenteric tube is placed beyond the duodenojejunal Transverse and longitudinal distribution of ulcerations
junction under fluoroscopic guidance. A standard amount can separate islands of thickened internal wall, resulting in
of barium (300 mL) and 0.5% methylcellulose solution the typical cobblestone appearance.
(1.500 mL) or air, as in our experience, is infused through Strictures are often separated by healthy bowel tracts
the nasoenteric tube, achieving optimal double-contrast and (skip lesions); impaired small bowel peristalsis is commonly
small-bowel distention. observed within rigid stenotic tracts. Extrinsic compression
Standardized compression views are obtained in all pa- may be observed, due to mesentery lymph node enlargement
tients for evaluation of the small bowel, especially of the ter- [6]. In partial obstructing stenosis, enteroclysis may provide
minal ileum [2]. higher sensitivity than enterography for detection of lesions
Crohn’s disease has been traditionally investigated with in the small bowel [7].
the use of small bowel barium enteroclysis, which detects Although it manages to accurately detect the location and
early mucosal disease (sens. 69.6%, spec. 95.8% [3]) as well as extension of Crohn’s disease (sens. 98%, spec. 97% [8]), it is
complications such as strictures, fistulae, and abscesses (diag- unable to provide information on extraluminal lesions [9],
nostic accuracy 80.3%) [3, 4]. and capsule endoscopy and double balloon enteroscopy have
2 Gastroenterology Research and Practice

(a) (b) (c)

(d) (e) (f) (g)

Figure 1: Conventional enteroclysis. (a) Conventional enteroclysis: panoramic view. (b) Mild wall thickening in the ileum. (c) Scattered
linear aphthoid lesions (arrow) in a segment of distal small bowel. (d) Mucosal ulcers (arrows). (e) Typical cobblestone-like nodular filling
defects and ulceration. (f) Fistula (arrows). (g) Stenotic loop (arrows).

replaced the enteroclysis as gold standard technique, even in Each layer does not correspond exactly to a defined his-
clinical practice [7]. tologic layer but rather an interface between adjacent layers
However, barium enteroclysis may be required as an ad- [13].
ditional test in a small group of patients with a high clinical The normal thickness of the small bowel is comprised
suspicion but a negative CT study [10]. ≤3 in the distended bowel and ≤5 mm in the nondistended
bowel.
Intestinal US allows the visualization of wall thickening
2. Ultrasonography (US) of the relevant loop, with the loss of normal stratification and
motility, lack of compressibility by the transducer, narrowing
Ultrasonography is an accurate, noninvasive, painless diag- of the lumen, conglomeration, the possible coexistence of
nostic tool with the capability of being used extensively in the mesenteric thickening, increased lymph nodes, abdominal
clinical setting. fluid and abscess, fistulas and stenoses related to dilations of
The examination consist of a global evaluation of the the upper loops [7, 11] (Figure 2).
small bowel and colon with standard resolution US (3.5– However, the accuracy of US is highly dependent on fac-
5 MHz), followed by a focused high-resolution study (7– tors such as experience level of examining physician and loca-
12 MHz). B-mode US may visualize five concentric layers tion and severity of the disease [7].
with different echogenicities [11]. When sensitivity is estimated based on disease location,
The first layer is the echogenic interface, followed by a the highest values are found for anatomic areas easily acces-
hypoechoic mucosa, an echogenic submucosa, a hypoechoic sible by US, such as terminal ileum and left colon, whereas
muscular layer, and a echogenic interface between the serosa the diagnostic accuracy is lower for upper small bowel and
and the adjacent fatty mesentery [12]. rectum [14].
Gastroenterology Research and Practice 3

(a) (b)

(c) (d)

Figure 2: US. (a) Wall thickening without stratification and hyperecoic lumen. Regular outer margin of the loop. Mesenteric fat hypertrophy.
(b) Coexistence of two patterns. Stenotic and thickened loop with preserved stratification and an adjcent segment with loss of stratification.
(c) Stenotic intestinal tract characterized by marked dilatation of the bowel lumen, with thickened bowel wall. (d) Wall thickening with loss
of normal stratification. Discontinuous outer margin with hypoecoic indented irregularities due to extramural findings.

Ultrasonography has the further disadvantage of being suggesting the use of the other imaging technique. The use
difficult to perform on overweight patients affected by severe of US has also been proposed in the followup of patients
meteorism. Furthermore, an ultrasound exam does not allow with known Crohn’s disease in asymptomatic patients in
operators to detect superficial intramural lesions [15–17]. order to identify the occurrence of complications at an earlier
The significant heterogeneity of the estimates of diag- stage [22] and recurrences (diagnostic accuracy 72.7%)
nostic accuracy (sensitivity 75–94% and specificity 67–100% [23].
[18]; sensitivity and specificity 90% and 96% [19]; sensitivity All studies showed a high accuracy of US for the diagnosis
and specificity 85% and 98% [7]; sens. 92% and spec. 97% of postsurgical recurrence in CD, detecting almost all cases of
[8]) precluded the possibility of obtaining a cumulative value severe or complicated recurrence, as well as high sensitivity
of diagnostic accuracy. and specificity in differentiating mild from severe recurrence,
In general, the magnitude of US changes has a high cor- especially after giving oral contrast [7].
relation with endoscopic and histological magnitude of alte- US has demonstrated a high diagnostic accuracy for the
rations and a weak correlation with indexes of clinical activity detection of small bowel fistulae, abscesses, and stenosis [24].
and biomarkers [7], especially in fistulae (sens. 71.4%, spec. For the detection of internal fistulas, the combination
95.8%, acc. 85.2%) and abscesses (acc. 88.5%) evaluation [3]. of small bowel enteroclysis and US significantly improved
Moreover, the bowel hydrosonography (with oral nonab- diagnostic accuracy (small bowel enteroclysis 84%, US 85%,
sorbable solution) results in an increase in the sensitivity of combination 91%) [7].
US for the detection of segments with active disease [20]. In conclusion, in known Crohn’s disease for following
To date, sonography of intestinal loops is useful as the disease course and evaluating relapses and extramural man-
preliminary examination [21], can help in clinical diagnostic ifestations, US is an excellent tool (sens. 88.4%, 93.3%, acc.
confidence, and can provide important diagnostic findings, 90.4%) [25].
4 Gastroenterology Research and Practice

3. Color-Power Doppler (PD) 30–70 KPa) produces microbubble resonance with produc-
tion of regular harmonic frequencies and allows real-time
Color and power Doppler US permits the measurement of scanning, and it is the technique of insonation which is usu-
arterial and venous flows in the upper mesenteric vessels, the ally in the clinical practice.
evaluation of the increase of the relevant loop, determination Now are available also specialized contrast-specific US
of alterations in the vascular and microvascular nature of the techniques, such as pulse inversion, recognition imaging,
inflammatory process and association with neoangiogenesis power modulation, and contrast pulse sequence [31].
in the intestinal wall [26]. CEUS provides an adequate evaluation of the increased
Color and power Doppler imaging usually is performed parietal vascularization in the active phase of the Crohn dis-
with parameters optimized to detect low velocity and low- ease. It might help in characterizing bowel-wall thickening
flow states (pulse repetition frequencies 800–1500 Hz, wall by differentiating inflammatory vascularization, edema, and
filter 40–50 Hz, maximal color signal gain immediately below fibrosis and may help to grade disease activity by assessing
the noise threshold, high levels of color versus echo priority, the presence and distribution of vascular perfusion within
and color persistence) [13]. the layers of the bowel wall, although it is limited to the eva-
The intensity of the vascularity may be subjectively cat- luation of a specific loop (Figure 4).
egorized as mild (small focal area of color signal), moderate Four different perfusion patterns of bowel enhancement
(multiples areas of weak color signal), or marked (multiple related to Crohns activity have been recently proposed: (a)
areas of color signal) because some studies have found that a complete enhancement of the entire wall section, from the
increased vascularity of the diseased bowel wall correlates mucosal to the serosal layer; (b) the absence of enhancement
with the activity of the disease [26]. only in the outer border of the muscularis propria; (c) the
Dopple, sonographic parameters of superior mesenteric absence of enhancement both in the outer and in the inner
artery are significantly correlated with disease activity in border of the bowel wall and enhancement only in the inter-
nonoperated and noncomplicated Crohn’s disease [27]. mediate layer; (d) the complete absence of enhancement in
Combination of B-mode and power Doppler sonography the entire wall section [29].
has a high accuracy in the determination of disease activity in Contrast-enhanced US could classify severity signifi-
Crohn’s disease when compared to ileocolonoscopy [27]. cantly better than Doppler-US signal and measurement of
To date, the use of power Doppler US has been suggested mural thickening (P < 0.001) [32].
to improve the diagnostic accuracy of US, particularly in dis- Patients with Crohn’s disease require frequently multiple
criminating inflammatory from fibrotic strictures, in better imaging examinations. CEUS is a noninvasive technique,
defining the presence of internal fistulas, and to differentiate which is also more comfortable for the patient with signif-
these lesions from intra-abdominal abscesses [13, 15–19, 21, icant diagnostic accuracy. The high sensitivity and temporal
22, 28] (Figure 3). resolution of CEUS in the assessment of small bowel vascu-
larity is the real strength of this technique [30].
4. Contrast-Enhanced Ultrasonography (CEUS) CEUS can become the most useful imaging modality in
the differential diagnosis between fibrotic and inflammatory
The limit of US evaluation is the impossibility of assessing thickening, in the detection of possible disease complications
bowel wall vascularization and the differentiation between (abscess, phlegmons, and fistulas) and for assessing the effi-
thickening due to active inflammation or fibrosis cannot be cacy of medical therapy in reducing bowel-wall vascularity in
reliably made with ultrasound. However, the bowel wall neo- patients with chronic inflammatory disease.
vascularization is an early pathological change occurring in To date, one study evaluated the accuracy of contrast-
patients with active CD [29]. enhanced US for assessment of activity in CD, showing that
The availability of dedicated contrast-specific techniques the technique has a high sensitivity and specificity (93% and
overcomes the limitations of CD-US with microbubble con- 94%, resp.) [33], (sens. 81%, spec. 63% for semiquantitative
trast agents, including blooming artifacts and the limited vis- method; sens. 81%, spec. 55.6% for quantitative method)
ibility of vessels with a slowflow [13] and has enabled ultra- [29].
sonography to obtain information regarding the perfusion The comparison of the diagnostic accuracy of conven-
behavior of the organs and their diffuse or focal diseases tional US, Doppler US, and contrast-enhanced US for assess-
[30]. ment of disease activity showed that the sensitivity of three
Microbubble contrast agents are mainly blood-pool modalities of examination and specificity are virtually iden-
agents and present a pure intravascular distribution and tical (94, 94, 94% and 97, 97, 97%, resp.) [33].
allow to increase the backscatter signal from blood cells. In conclusion, CEUS has a high sensitivity and specificity
Microbubbles consist of small gas particles with a diameter of in detecting inflammatory activity and a strong correlation
2–6 µm with a stiff or flexible shell composed by biocompati- with the CDAI (sens. 93.5%, spec. 93.7%, acc. 93.6%, corre-
ble materials (proteins, lipids, or biopolymers) presenting an lation coefficient 0.74; P < 0.0001) [33].
overall thickness from 10 to 200 nm. CEUS allows real-time assessment of the bowel-wall per-
Insonation techniques are available for CEUS. The high- fusion with the highest temporal resolution of all imaging
transmit-power insonation produces extensive microbubble techniques and with a spatial and contrast resolution that
destruction with the production of a wide-band irregu- rivals that of CT and MRI. In consideration of the need for
lar harmonic signal. Low-transmit-power insonation (about patient comfort, especially in pediatric imaging, CEUS might
Gastroenterology Research and Practice 5

(a) (b)

(c) (d) (e)

Figure 3: PDs. Wall thickening in B mode (a), in PD (b), (c), (d), and arterial doppler spectrum (e).

(a) (b)

(c) (d)

Figure 4: CEUS. Last ileal loop wall thickening and submucosal contrast enhancement after contrast medium (SonoVue, Bracco). 0 (a), 15
(b), 30 (c), and 45 (d) sec.
6 Gastroenterology Research and Practice

become the most useful modality for assessing the efficacy of CT-dependent patient’s dose. CT images are analyzed on
medical therapy with chronic inflammatory disease. a soft-tissue window (30-HUcenter level, 400-HU-window
The routine use of the CEUS in the clinical assessment of width).
the patient with active Crohn’s disease for therapeutical and Multiplanar reconstructions are undertaken in all pa-
surgical management should be suggested [33]. tients to help interpret conflicting findings in axial scans, im-
prove the detection of lesions, and increase the capability for
5. Multidetector CT Enteroclysis (MDCT-E) assessing lesions’ extension.
Patients with the disease do not form a clinically homo-
Multidetector CT enteroclysis was introduced as an alterna- geneous group, and they may be very different from one ano-
tive imaging method to overcome the individual deficiencies ther, with different clinical situations influenced by individ-
of CT and conventional enteroclysis and to combine the ual expression of the disease and possible previous surgical
advantages of both in one technique. procedures; this does not always allow a uniform and rep-
MDCT-E has been described as highly accurate in reveal- roducible clinical and radiological standardization of the dis-
ing mural and extraluminal manifestations of disease, in- ease [38, 39].
cluding abscesses, while conventional enteroclysis was supe-
In patients suspected of having Crohns disease, MDCT-E
rior for luminal abnormalities and ulceration (Figure 5) [34,
is accurate in depicting mucosal abnormalities, bowel thick-
35].
ening, mucosa hyperemia, ulcers, stenosis, engorgement of
CT enteroclysis can be performed by using positive ent-
vasa recta, and lymph nodes and mesenteric involvement
eral contrast material without intravenous contrast material
[40–42].
or neutral enteral contrast material with intravenous contrast
material [36]. It is superior to CT enterography in that it provides a sui-
The advantages of neutral CM through the lumen out- table uniform distension of the lumen, thus allowing assess-
weigh those offered by positive CM for the following reasons: ment of wall thickness [43].
lower costs, low viscosity, faster injections, and better view of Evidence suggest a high sensitivity, specificity, and accu-
enhancement, wall thickening, and mesenteric involvement. racy in the evaluation of relapse of ileocolic anastomosis [7].
Positive CM through the lumen is useful in the case of con- It also has higher sensitivity and greater interobserver
traindications to CM intravenously injected. As far as our reliability if compared to MR enteroclysis and does not entail
study is concerned, we combined neutral and intra-venously any risk of capsule retention to the patient while performing
injected CM through the lumen in all patients [37]. video capsule endoscopy [44].
In our experience, before the exam, patients take laxatives Nonetheless, MDCT-E has its drawbacks. Take for ins-
for small-bowel and colon cleansing. Then a nasoenteric tance, ionizing radiation, time needed for placing the naso-
tube—150 cm long, 21 mm in diameter, 2.8 mm in external enteric tube, high costs, contrast medium intravenously in-
diameter, and a distal end closed by a plastic tip with 4 side jected, likely inhalation of contrast medium injected into the
holes [Guerbet, Paris]—is placed. The patient is moved to the lumen, necessity to attain a suitable distension of the lumen,
CT room where scout-view and volumetric scan are carried and lower sensitivity when it comes to identifying lesions of
out. the mucosa and jejunum.
A layer not wider than 3 mm and a reconstructing inter- Differences in specificity and sensitivity can be ascribed
val not larger than 5 mm are chosen. to a distinct lack of standard protocols [45–49] and to the
20 mg of hyoscine butylbromide are administered intra- different methods followed for data analysis (CD diagnosis
venously in order to reduce intestinal peristalsis and segmen- sens. 84%, spec. 95% [19]; location and extension sens. 88%,
tation of the intestinal loops and foster their distension. spec. 88% [7]; disease activity and severity sens. 81%, spec.
1800 mL of water at temperature 37◦ C is used as a neutral 88% [7] or sens 89%, spec 80% [50]; complication sens.
contrast agent and administered through a peristaltic pump 81%, spec. 98% [7]; extraintestinal complications sens. 100%
so as to obtain a suitable distension of the intestinal loops. [50]).
The initial 500 mL is flushed through the tube at a speed
Moreover, for the identification of abscesses, accuracy is
of 120 mL/min in order to avoid stress caused by sudden
higher for CT (92%) than for US (87%) because false positive
loosening. Then the inoculation of another 1000 mL at
results in US studies [7] and significant correlations are ob-
240 mL/min follows, with the aim of loosening the loops
served between the intensity of various CT changes and the
and pushing the contrast medium (CM) forward. The last
severity of endoscopic lesions [51].
300 mL is injected at 120 mL/s.
After introducing 1500 mL of intraluminal contrast med- For these reasons, by defining universal procedures (e.g.,
ium, iodinated contrast agent is injected intravenously, 1 mg patient’s preparation, performing techniques, diagnostic
iodine/kg body weight (BW) through a mechanic injector standards for IBD, etc.) we will be able to increase sensitivity
at a concentration of 400 mg iodine/mL (“Iomeprol” and and specificity values in addition to being able to establish
“‘Iomeron 400”’ Bracco, Italy) with a 80 s delay in scanning. a more accurate diagnosis in order to establish therapy pro-
In the first 40 s, the CM is injected at a speed of 1 mL/s, grams which suit the individual’s needs [37].
whereas in the remaining 30 s it is administered at a speed To date MDCT-E is indicated in case of patient with ini-
of 3 mL/s. The exam is carried out with one volumetric acq- tial diagnosis of Crohn’s disease, suspected complications or
uisition at 70 s during breathing-in apnea, thus reducing the recurrence [39].
Gastroenterology Research and Practice 7

(a) (b) (c) (d) (e)

(f) (g) (h) (i)

Figure 5: MDCT-E. Intraintestinal findings: intramural (a), (b) wall thickening (b) (“double halo sign”), (c) hyperemia of the mucosa,
(d) ulcer, (e) stenosis, extramural (f) engorgement of vasa recta (“comb sign”). Extraintestinal findings: (g), (h) lymph nodes involvement
and mesenteric fat stranding, (i) abscess.

6. MRI Enteroclysis (MR-E) and examination with the use of peroral contrast agent admi-
nistration may not be accurate for detection of early mucosal
MRI enteroclysis is a noninvasive, nonionizing radiation dia- lesions of CD [50].
gnostic technique able to obtain multiplanar diagnostic Moreover, this method is less accurate in the detection of
information about intra- and extraintestinal lesions and eva- a small-bowel stricture, especially a partially obstructing stri-
luate disease activity [43]. cture [50].
The high soft-tissue contrast, multiplanar capabilities In our experience, two days prior to the examination, all
and possibility of obtaining functional information make patients take a 2,000 cc solution of polyethylene glycol (PEG)
MR imaging the ideal technique for evaluating small-bowel in water (SELG 2000, Milan, Italy) to cleanse the bowel and
inflammatory disease (sens. 78%, spec. 85% [7]; sens. 93%, are invited to follow a semiliquid diet and on the day of the
spec. 93% [19]). examination to have nothing by mouth. Allergic patients
In addition, MR imaging has the advantage over tradi- undergo desensitisation therapy with cortisone and antihis-
tional techniques of visualizing the entire thickness of the tamines for 3 days prior to MR examination [60].
bowel wall and the perivisceral loose connective tissue [53– Distension of the small bowel is obtained with the
55]. administration of an 1,800 cc solution of PEG in water (SELG
Some technical aspects, in particular distension of the 2000). The solution is injected via the nasoenteric tube after
bowel and use of a luminal contrast, may affect the accuracy they have entered the scanner (MR enteroclysis).
of MRI for assessing changes associated with active disease Patients are premedicated with 20 mg i.v. of hyoscine N-
such as wall thickening and enhancement of bowel wall after butylbromide to reduce intestinal peristalsis and segmenta-
MRI contrast administration [56]. tion of the bowel loops during the examination and are ima-
However, the study protocol has not yet been standard- ged in the prone position with a 1.5-T MR scanner (Magne-
ized, and some controversy remains regarding the value of tom Symphony, Siemens, Germany) and phased-array body
nasoenteric intubation [57]. coils.
Some authors [58] suggest that although bowel disten- The study protocol includes unenhanced and enhanced
sion is greater in patients undergoing MR enteroclysis than in scans (Figures 7 and 8) and the postcontrast acquisitions are
patients undergoing MR enterography, this produces no sig- processed, and the time-intensity (T/I) curves are evaluated
nificant difference between the two groups. (Figure 9).
Nevertheless, MR enteroclysis (sens. 90%, spec. 100%) MR enteroclysis—thanks to the adequate distension it
proved to be more effective than MR enterography (sens provides all bowel loops, including the jejunum and the
89%, spec 67%) in evaluating stenosis and its significance proximal small-bowel loops—is the technique that best
and also in evaluating bowel-wall thickness (Figure 6) [59], enables accurate assessment of Crohn’s disease (sens. 74%,
8 Gastroenterology Research and Practice

(a) (b)

Figure 6: MR-E. (a), (b) Coronal true fast induction steady-state potential and single-shot hydrographic sequence showing a suitable degree
of jejunum distension.

(a) (b) (c) (d)

(e) (f) (g) (h)

Figure 7: MR-E. Last ileal loop wall thickening (a), (b) axial TRUFI T2. (c), (d) Coronal TRUFI T2. (e) Coronal FLASH 3D. (f), (g), (h)
Coronal FLASH 3D postcontrast medium.

spec. 91%) [7]. The technique, in fact, enables identification be achieved with MR enteroclysis, makes it a unique imaging
of lesions to the mucosa and complications. MR enteroclysis modality [61].
enables identification of a stenotic segment, evaluation of The correlation for the assessment of activity between
significance or insignificance, definition of characteristics— endoscopy and MR and differentiation between mild and
whether inflammatory or fibrous—and therefore guidance severe lesions is considered very high [7].
towards the most appropriate treatment. The possibility of The main drawbacks are represented by high operating
obtaining dynamic-functional information, which can only costs and the need for contrast injection. It also has relatively
Gastroenterology Research and Practice 9

(a) (b)

(c) (d)

Figure 8: MR-E. Crohn’s disease: colon involvement (a), (b) coronal TRUFI T2 showing (c) axial TRUFI T2; (d) coronal TRUFI T2.

220

129.5

39
−0.4 0.5 1.4 2.3 3.2 4.1 5
(min.sec) Normal time
(a) (b)

Figure 9: MR-E. (a) Coronal TRUFI T2 showing ileal loop wall thickening. (b) Intensity/time curve not showing inflammatory activity.

lower sensitivity than MDCT-E (60% versus 89% in the asse- enteroclysis (sens. diagnosis 95.2%, abscesses 77.8%, fistulae
ssment of bowel-wall thickening only) [59]. 70.6%) [62].
However, MRI can detect the most relevant findings To date, the elevated soft-tissue contrast and the func-
in patients with IBD with an accuracy superior to that of tional information it can provide make MR imaging an
10 Gastroenterology Research and Practice

Table 1: Imaging techniques features in Crohn’s disease.

Superficial Intra/
IV Nasoenteric Well Widely Operator Radiation Activity of
Invasiveness lesion extraintestinal
infusion tube accepted available dependent exposure disease
detection structures
CE + − + − + − + + − −
US − − − + + + − − − −
PD − − − + + + − − − −
CEUS − + − + − + − − − +
MDCT-E + + + − − − + − + +/−
MR-E + + + − − − − − + +/−
TLLS − + − − − − + − − +
CE: conventional enteroclysis; US: ultrasonography; PD: power Doppler; CEUS: contrast-enhanced ultrasonography; MDCT-E: multidetector CT enteroclysis;
MR-E: magnetic resonance enteroclysis; TLLS: 99mTc-HMPAO-labeled leukocyte scintigraphy; IV infusion: intravascular infusion.

ideal candidate for diagnosis at a young age and followup of obtainable from this type of examination is lower because
patients with Crohn’s disease [43, 50, 63]. image quality is distinctly inferior.
In vivo labeling can be performed by means of tech-
netium-99 m-labeled anti-granulocyte antibodies. The exam
7. 99mTc-HMPAO-Labeled Leukocyte neither requires patient’s preparation nor blood count, nor
Scintigraphy (TLLS) does it need subsequent separation of leukocyte components.
In vitro leukocyte labeling, on the other hand, has the
99mTc-HMPAO-labeled leukocyte scintigraphy can identify disadvantage of more complex procedures. It also demands
the location of the inflammation and consequently assess its trained staff, well-equipped laboratories for cell labeling in
activity level. aseptic conditions not to mention longer performing times.
Therefore, it provides rationale not only when clinical The undeniable advantage of in vitro labeling is, however,
data and CT data are unclear but also during the assessment given by its distinctly higher image quality due to a selective
of a previously known inflammatory process so as to devise labeling of granulocytes with lower residual [65].
a suitable therapy program [64]. In our experience, 99mTc-HMPAO-labeled leukocyte
TLLS, used as a tool to identify location, level of inflam- scintigraphy (TLLS) is performed upon in vitro labeling. As
mation, and level of infection in nuclear medicine can boast for the whole-body 99mTc-HMPAO-labeled autologous leu-
of a well-established tradition. The response to an inflamma- kocyte scintigraphy, a sample of venous blood of 50 mL is
tion or acute infection process is characterized by an increase taken through syringes containing 10 mL of acid citrate dex-
in the local amount of blood, increased vascular permeability trose formula A (ACD-A) upon adding 5 mL of hydroxyethyl
in addition to plasma protein exudation, and leukocyte starch (HES) at 10%. After sedimentation and centrifuga-
stream [65]. tion, a leukocyte button is obtained and then labeled with
During an acute inflammation/infection process, we wit- 740 MBq 99mTc-HMPAO (hexamethyl-propyleneamine ox-
ness a majority of polymorphic nuclear infiltrating cells while ime) (CERETEC GE, Healthcare) [38].
in chronic inflammation/infection cases cellular response After labeling and quality control, the level of neutro-
mostly concerns lymphocytes, monocytes, and macrophages. phils in suspension is higher than 95%, and cellular activity
Although Crohn’s disease represents a chronic condition reached 99%. Autologous leukocytes are injected intraven-
with a predominant mononuclear infiltrate, labeled leuko- ously. The actual dose, which is given according to the label-
cytes, in the case of leukocytes infiltrating at the level of the ing result, ranges from 370 to 555 MBq.
mucosa, give operators a clear view of intestinal inflamed Scintigraphy images are obtained by employing a rectan-
tracts during the acute phase of the disease [64]. gular dual-head large-field-of-view digital gamma camera
TLLS has been extensively employed in patients affected equipped with high-resolution and low-energy collimators.
by Crohns disease throughout the years producing not always Images are obtained 60 and 180 m after labeled leuko-
unanimous results due to the differences among labeled cells, cytes have been administered again.
labeling methods, and the type of imaging which is obtained. Compared to early scan, late scan (3 h) has a higher sen-
Through the years, many labeling methods have been put sitivity (85% versus 100%) and accuracy (85% versus 95%)
forward both in vitro and in vivo. In vivo labeling is easy to in identifying patients with active IBD and in defining IBD
perform and does not require special equipment. It reduces extension [66].
performing times as well as being well tolerated by patients Still front/rear images of the abdomen and pelvis are
because it calls for only one injection. Conversely, the acquired. In order to further assess perianal and rectal invol-
generally low quality of view obtained by labeling methods vement, a projection of the pelvis is carried out in five cases,
which present great residual decreases the tracer substance the aim being to separate such districts, which overlap during
amount needed for tracing diapedesis. As a result, sensitivity anterior projection, from the bladder. So as to have a clear
 Table 2: Diagnostic accuracy of CE, US, CEUS, CT, MR, and TLLS in the assessment of diagnosis, disease activity, complication and, relapses in Crohn’s disease.
CE US CEUS CT MR enteroclysis MR enterography TLLS
Sens. Spec. Acc. Sens. Spec. Acc. Sens. Spec. Sens. Spec. Acc. Sens. Spec. Sens. Spec. Sens. Spec. Acc.
Panes 85 98 78 85
Gastroenterology Research and Practice

Horsthius 90 96 84 95 93 93
Fraquelli 75 94
Diagnosis 83– 92–
Alberini
98 100
Rispo 98 97 92 97 90 93
Rieber 85 77 95 93
Lee 83 100
Migaleddu 2009 93 94
Serra 81 63
Disease activity
Lee 2009 89 90
Panes 81 88
Complication Panes 81 98
Maconi 70 95 71
Fistulae
Rieber 18
Maconi 80 77
Abscesses Rieber 0 78
Panes 87 92
Stenosis Cappabianca 90 100 89 67
Extraintestinal Lee 100
Tarjàn 88 93
Relapses
Paredes 78
CE: conventional enteroclysis; US: ultrasonography; PD: power Doppler; CEUS: contrast-enhancement ultrasonography; MDCT-E: multidetector CT enteroclysis; MR-E: magnetic resonance enteroclysis; TLLS:
99mTc-HMPAO-labeled leukocyte scintigraphy; IV infusion: intravascular infusion; sens.: sensitivity; spec.: specificity; acc.: accuracy.
11
12 Gastroenterology Research and Practice

(a) (b)

(c) (d)

Figure 10: TLLS. (a) No inflammatory activity; (b) mild inflammatory activity; (c) moderate inflammatory activity; (d) severe inflammatory
activity.

view of the liver and transverse colon, the anterior projec- pathologies with necrotic component). Crohn’s disease case
tions of the standing patient’s abdomen are acquired. studies in nontreated patients report sensitivity percentage
In the last few years, technetium-labeled hexamethyl- values of 83–98% and specificity percentage values of
propyleneamine oxime scintigraphy (99mTc-HMPAO) has 92–100% [64, 65]; particularly in Crohn’s disease diagnosis
proved itself to be extremely useful in the diagnosis and fol- sensitivity percentage amounts to 90%, specificity to 93 [8];
lowup to Crohn’s disease. There are a great number of advan- in postsurgical recurrences, diagnostic accuracy percentage
tages to it, for instance, high sensitivity and specificity, low amounts to 81.3–81.8% [23].
invasiveness, the possibility of performing the exam even in To date, the existence of (almost) standard criteria (asses-
the acute phase of the disease, the opportunity to perform the sment of light activity, be it moderate or serious depending
exam even without bowel cleansing, the further opportunity upon the level of the uptake of the bone marrow at the level
to evaluate the seriousness of the process and multifocality of the ileac crests) make it possible for the exam to be rep-
at the same time, lack of risks or contraindications, no side roduced and consequently be valid for identifying the degree
effects, and good tolerance on the part of the patient. of inflammation (Figure 10).
However, procedures are long and complex not to men-
tion the fact that they require blood manipulation and have 8. Conclusion
low anatomic resolution. Moreover, 99mTc-HMPAO man-
ages to visualize only acute inflammatory cases and may In recent years, several radiologic techniques have been deve-
show false positives (Yersinia enteritis, ischemic colitis, tuber- loped for the study of the small bowel. Each technique is
cular enteritis, rejection, pseudomembranous colitis, vasculi- characterized by its own profile of advantages and disadvan-
tis, appendicitis, hematomas, radiation enteritis, malignant tages (Table 1).
Gastroenterology Research and Practice 13

Table 3: Appropriateness of examination in Crohn’s disease.

CE US CPD/CEUS MDCT-E MDCT-e MR-E MR-e TLLS

First diagnosis 8 7 7 9 8 9 8 7
Followup∗ 2 9 6 2 2 4 5 2
Relapse 6 6 6 8 7 9 8 7
Complications 7 6 6 9 8 9 8 6
9: extremely appropriate; 7-8: usually appropriate; 4–6 doubt; 2-3: usually inappropriate; 1: extremely inappropriate [52].
CE: conventional enteroclysis; US: ultrasonography; PD: power Doppler; CEUS: contrast-enhancement ultrasonography; MDCT-E: multidetector CT
enteroclysis; MDCT-e: multidetector CT enterography; MR-E: magnetic resonance enteroclysis; MR-e: magnetic resonance enterography; TLLS: 99m Tc-
HMPAO-labeled leukocyte scintigraphy; IV infusion: intravascular infusion; ∗ negativity of clinic and laboratory exams.

Because of the relapsing nature of Crohn’s disease and the sonography and Tc-99m-HMPAO leukocyte scintigraphy,”
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