Evaluation of intestinal tuberculosis by multi-slice computed tomography enterography

Prior to CTE, using conventional CT for evaluations on the small intestine has been considered inadequate because pathology could easily be obscured amongst collapsed intestinal loops. With the rapid development of CT techniques, CTE has made it be possible. In CTE, the small intestine is expanded by oral ingestion of a neutral or negative contrast agent, such that mucosal and mural changes are clearly depicted [12]. One major challenge in performing good quality CTE is about the optimal volume and timing of oral contrast administration, balancing the quality of intestinal distension with patient tolerance and degree of side effects. Nowadays, CTE is considered as an effective imaging technique to detect and evaluate many gastrointestinal diseases [12, 13, 21]. Most CTE studies have concentrated on the diagnostic performance for the intestinal inflammation and intestinal complications of Crohn’s disease [22]. Reports on the utility of CTE in the diagnosis of ITB are still rare.

We retrospectively evaluated the clinical data and MSCTE images of 15 patients with ITB. We found that the ileocecum was the most common site affected by ITB. MSCTE showed that nine patients (60 %) mainly manifested with solid masses, and six patients (40 %) were shown as having multiple segments of symmetric intestinal mural thickening. Rim enhancement of LNs was found in 10 (67 %) patients, which also could be used to enhance the diagnostic confidence of ITB.

Prior studies also reported the ileocecum as the most commonly affected site of ITB [6, 11, 23, 24]. The abundance of lymphoid tissues, the relatively longer time for fecal stasis, the appropriate neutral pH environment and the absorptive transport mechanisms (increasing rate of fluid and electrolyte absorption) of the ileocecum work together to allow the swallowed mycobacterium to be absorbed and might contribute to the predilection of ITB [25]. The duodenum is the fourth most commonly affected site following the ileocecum, colon and jejunum, and greater than 90 % of duodenal TB was also found to have co-infections in other parts of the intestine [26]. However, in our study, one patient showed isolated duodenal TB.

Generally, there are three pathological types of ITB, as follows: ulcerative, hypertrophic and ulcerohypertrophic. The last two types display mass-like lesions and mimic malignancies. The bowel wall changes were variable, reflecting the different pathological types. Seven patients (47 %) in our study were found to have symmetrical, single or multi-segmental intestinal mural thickening due to ulcerations. Focal solid masses representing the hypertrophic or ulcerohypertrophic types were observed in nine patients (60 %).

ITB is also a chronic granulomatous disease with inflammatory and reparative phases. The individual lesions could be in different stages of inflammation and repair, such that the MSCTE findings vary between different lesions within the same patient. During the inflammatory phase, the length and size of lesions were larger with indistinct boundaries and were expected to enhance homogeneously. In our study, all of the lesions manifested with indistinct boundaries. Further, as inflammation could cause submucosal edema, the affected intestine wall or solid mass appeared as a ‘target sign’. On the contrary, during the reparative phase, the lesions tended to have more clearly defined boundaries with less contrast enhancement because of the fibrosis in the middle layer of the intestinal wall. In addition, fibrosis could further progress into stricture formation, resulting in abnormal peristalsis and mechanical obstruction. Proximal to the obstruction site, the bowel was often dilated with the edematous intestinal wall manifesting as submucosal edema and appearing as a double-ring sign on contrast-enhanced CT. In our study, seven patients with MSCTE showed these signs.

Lymphadenopathy was another common manifestation of ITB. The most common CT manifestation of diseased LN was rim enhancement with a low-density center, representing peripheral inflammatory reactions and central caseous necrosis. This imaging appearance was highly suggestive of ITB although other conditions such as metastasis, Whipple’s disease, lymphoma, and infection with mycobacterium avium-intracellulare can have a similar appearance [27]. In our research, LNs with rim enhancement were observed in 10 patients (67 %). In addition, the low-density necrotic components in affected LNs ranged from tiny dots to large areas involving the majority of an LN, which did not correlate with the size of the LN. The smallest necrotic node found in our study was only 6 mm in size. We also found that the artery phase of MSCTE was the best for detecting caseous necrosis. Moreover, we identified an interesting phenomenon in that two of our patients with the most severe TB symptoms and active PTB also showed signs of complete central caseous necrosis in their LNs. It is, therefore, surmised that activity of ITB may be reflected by the degree of necrosis in LNs, but this assumption requires further confirmation. On the other hand, only one patient in our study had calcified LNs, suggesting that calcified LNs might not be frequently observed.

Other changes associated with ITB found in our study included ascites (n = 3), mesenteric thickening and hypervascularity (comb sign; n = 2), suggesting that the comb sign is not a unique sign of Crohn’s disease as mentioned in previous literature [28]. Biochemically, the ascitic fluid showing high attenuation values (25–45 HU) indicated exudative fluid with high protein and cellular content. The scans showed that the peritoneal fluid was diffusely distributed throughout the peritoneal cavity, suggesting wet peritonitis as the possible cause [29].

ITB could accompany abdominal complications, including obstruction, perforation, and fistula formation. All of the complications in our study, with the exception of one with intestinal hemorrhage, were correctly diagnosed by MSCTE. Four of the patients (27 %) had imaging manifestation of PTB. Daucourt V et al. found that 69 % of extra-PTB presentations was associated with PTB [30]. In our study, the percentage was a little lower, and the reason may be that not all patients had thorax examination. Still, we recommend that a plain chest X-ray be obtained in clinically suspicious ITB patients because patients who have PTB are at a higher risk of secondary intestinal involvement.

Of the differential diagnoses of ITB, Crohn’s disease (CD) is at the top of the list. ITB and CD are both chronic granulomatous disorders with similarities in clinical presentation and pathology [31‐34]. As discussed before, ileocecal region is the most common site of involvement in ITB [11, 23]. Isolated involvement of the ileocecal region is not found in CD, which typically involves the ileum whilst sparing of the ileocecal valve. The cecum may rarely be involved in direct contiguity with the ileum or colonic disease in ITB. Whilst the ascending colon may be involved in direct contiguity with the ileocecal region in ITB, colorectal involvement with small bowel disease is more often observed in CD than in ITB. Isolated colorectal involvement in ITB is rare compared with CD. Presence of hypodense LNs with peripheral rim enhancement in the mesentery and retro-peritoneum is rarely observed in CD, which also helps differentiate between the two. Furthermore, it is difficult to differentiate a solitary ITB from malignancy on imaging, especially in older patients [35]. Malignant stricture often occurs in elderly patients and manifests as solitary lesion, usually ranging from 2 to 6 cm long with irregular contours, intraluminal filling defects, and rigid, tapering margins. ITB is more commonly found in younger patients and often presents as multiple lesions [35]. Other differential diagnsises include Yersinia enterocolitis and Yersinia pseudotuberculosis, which preferentially affect the gut-associated lymphoid tissue and related LNs, respectively. These conditions commonly masquerade as acute appendicitis and ileitis or mesenteric adenitis in children and young adults [36].

One major limitation of this study is the relatively small case number, which is to a large extent due to the fact that ITB is a rare disease. Therefore, the imaging manifestations of ITB in CTE as reported in our study might not necessarily reflect the full spectrum of related imaging findings.