Common and uncommon imaging features of abdominal tuberculosis
Despite the advances in the medical care, tuberculosis (TB) still remains an important health problem. This is particularly relevant to the developing countries as well as the immunocompromised population in the developed world. Multidrug resistance poses another challenge and may be responsible for increasing incidence of TB, to some extent. The respiratory system is the most commonly involved, although any organ system may be affected. Abdominal involvement occurs in 11-12% of the patients with extrapulmonary TB. The clinical features of abdominal TB are nonspecific. Imaging plays an important role in the diagnosis of abdominal TB. Although a few imaging features strongly favour the possibility of TB, abdominal TB is a greater masquerader. In this review, we highlight the entire spectrum of the manifestations of abdominal tuberculosis (excluding the genitourinary involvement) with an emphasis on imaging findings.abdomen; biliary and pancreas; gastrointestinal imaging; tuberculosis.
Tuberculosis most commonly involves the respiratory system. However, any organ system can be affected,particularly in immunocompromised individuals.The diagnosis of extrapulmonary TB is often difficult; though many patients may have positive tuberculin skin test and chest radiographic findings; however, negative results do not exclude the diagnosis.The diagnosis of extrapul-monary tuberculosis requires a high clinical suspicion,especially in predisposed population.Abdominal involvement occurs in about 11–12% of patients with extrapulmonary TB.Abdominal TB may practically affect any organ. It may involve the hepatobiliary system, pancreas, gastrointestinal (GI) tract, genitourinary tract, peritoneum and lymph nodes.The diagnosis of abdominal TB is often delayed as the presentation is nonspecific. Imaging plays an important role in diagnosis. In certain cases, the findings may be specific.However, in many cases, the imaging features are nonspecific and overlap with other conditions. In such cases,a high index of suspicion is required to timely diagnose this condition. In this article, we review common and uncommon imaging features of abdominal TB except for genitourinary TB (Table 1).
Isolated hepatic TB is a rare condition and is usually associated with concomitant involvement of other organs.On imaging, hepatic TB may be divided into two types, micronodular (miliary TB of the liver) and macronodular (tuberculoma or abscess of the liver) (Fig. 1). Fig. 1. Hepatic tuberculosis. (a) Axial CT image in a 40-year-old male with disseminated TB shows a small hypodense lesion in segment 8(arrow), a case of macronodular TB. (b) Ultrasound image shows subtle ill-defined hypoechoic lesions suggestive of micronodular TB. (c, d)Axial (c) and coronal (d) CT images in a middleaged female with past history of pulmonary tuberculosis and pain upper abdomen for few days show plaque-like hypodensity along the surface of right lobe of liver suggestive of serohepatic TB.The micronodular form is more common and is associated with hematogenous dissemination leading to diffuse enlargement of the liver. Most commonly micronodular form is related to the miliary pulmonary TB.On imaging, the miliary form presents with hepatosplenomegaly and sometimes small hypodense lesions are seen on computed tomography (CT). High-resolution ultrasound is more sensitive in detecting the small lesions which appear as ill-defined hypoechoic lesion usually less than 10 mm or more commonly a diffusely heterogeneous liver echotexture. Similar pattern may be seen in metastases, other granulomatous pathologies (fungal infection and sarcoid) and lymphoma.The macronodular form is less common and is not associated with the pulmonary TB. It is secondary to dissemination through the portal vein. On CT, hypodense lesions of 1–3 cm in diameter or a single mass is seen in a diffusely enlarged liver.Magnetic resonance imaging (MRI) shows minimally enhancing honeycomblike lesions on postcontrast T1-weighted images. These lesions are hyperintense on T2-weighted images and have a rim that is hypointense relative to the surrounding liver. Pyogenic/amoebic abscess and metastases are important differentials of macronodular form.Uncommon presentation of hepatic TB includes serohepatic TB.Serohepatic TB is the rarest variant reported in the literature. On imaging, peripherally positioned lesions in the subcapsular plane of the liver are seen.Thickened liver capsule and subcapsular tissue adjacent to these hypoattenuating lesions (on T2-weighted images) simulate a ‘sugar-coating’, an appearance popularly referred to as ‘frosted liver’. Another related imaging appearance could be scalloping of the liver (or other visceral organs) in patients with tubercular ascites(Fig. 1).Biliary tree (tubercular cholangitis) and gallbladderThe involvement of the biliary tree by TB is rare and its annual incidence is around 0.1% in southeast Asia. Both the small and large ducts can be involved directly leading to strictures. The strictures are multisegmental and cause parenchymal atrophy. The extrahepatic ducts are involved uncommonly. Imaging features include bile duct thickening and irregularity. The segments of biliary dilatation alternating with stenosis are not uncommon and mimic primary sclerosing cholangitis, IgG4-related cholangitis and cholangiocarcinoma (Fig. 2). Fig. 2. Tubercular cholangitis. Axial CT image in a young male with history of abdominal pain, fever and jaundice for few months shows left-sided mild biliary dilatation (arrow) with ill-defined hypodensity (short arrow).Biliary dilatation can also result from extrinsic ductal compression by lymph nodes. Features that favour biliary TB include associated hepatic granulomas, parenchymal or periductal miliary calcifications, calcified or necrotic periportal lymph nodes. The gallbladder is very rarely involved in abdominal TB. There is no typical clinical presentation or imaging finding. Xu et al. reviewed the CT features of gallbladder TB in seven patients and classified the pattern of involvement into three types: micronodular type (n = 1),mural thickening (n = 4) and mass (n = 2).Splenic TB is rare. Clinical and imaging characteristics are similar to those of hepatic TB and in fact, in the miliary form, both liver and spleen are commonly involved(Fig. 3). Fig. 3. Splenic tuberculosis. (a) High-resolution ultrasound image in a patient with disseminated TB shows multiple tiny nodules (arrows) in the enlarged spleen. (b) Axial CT image in a patient with fever and loss of appetite for 1 month shows a tiny hypodense nodule (arrow) with central hyperdensity in spleen. (c) Ultrasound image in a young female with pain left upper abdomen and fever for 2 months shows a single large nodule in the inferior pole of spleen (arrow). (d) Ultrasound image in a 26-year-old male on antitubercular treatment for pulmonary TB having pain left upper abdomen for few days shows a large well-defined nodule with central anechoic component (arrow) resembling an abscess. (e) Ultrasound image in a middle-aged female with past history of pancreatitis having nonspecific upper abdominal complaints shows a well-defined heterogeneous nodule (arrow) mimicking a neoplasm.Miliary form leads to splenomegaly and the multiple small nodules are better delineated on high-resolution ultrasound as ill-defined hypoechoic lesions.The macronodular form presents as single or multiple larger nodule/s or mass/es that are hypodense on CT and hypoechoic on ultrasound. These nodules commonly have an appearance similar to abscesses showing peripheral enhancement on CT and anechoic areas or debris on ultrasound.However, a single large nodule may mimic a neoplasm. Tuberculosis of the pancreas is uncommon and its true incidence is unknown. It usually occurs as a part of miliary TB. Pancreatic TB most commonly presents as a solitary lesion with multiple cystic components. It is typically located in the pancreatic head; peripancreatic lymphadenopathy can be found along with additional features of other abdominal organ involvement (Fig. 4).Fig. 4. Pancreatic tuberculosis. (a) Ultrasound image shows hypoechoic nodules in the pancreatic body (arrow). (b) Axial CT images in a different patient show a hypodense lesion in the head of pancreas.Gastrointestinal tuberculosisAny part of the GI tract from oesophagus to rectum may be involved by TB. The GI TB can be of different forms such as ulcerative, hypertrophic and ulcero-hypertrophic based on gross morphological appearance (Fig. 5).Fig. 5. Ileocaecal tuberculosis. (a) Ileo-colono-scopic image in a 44-year-old male with altered bowel habits for 1 month shows hypertrophy and ulceration of ileocaecal valve (arrow). (b)Barium meal follow through of the same patient.The caecum is contracted (arrow) and the terminal ileum is pulled up (short arrow). (c) Coronal CT image of the same patient shows mild mural thickening of the ileocaecal region (arrow). (d)Coronal CT image in another patient with history of diarrhoea and bleeding per rectum for 1 month shows a relatively greater degree of mural thickening with enhancement (arrow).Commonly, the ileocaecal region is involved, possibly because of the physiological stasis with an increased rate of fluid and electrolyte absorption, minimal digestive activity and abundance of lymphoid tissue at this site.Thickening of the valve lips or wide gaping of the valve with narrowing of the terminal ileum (the Fleischner sign) has been described on barium meal follow through (BMFT). Other signs seen on BMFT are (i) ‘conical caecum’, wherein caecum is shrunken and pulled out of the right iliac fossa due to contraction and fibrosis of the mesocolon; (ii) ‘gooseneck deformity’ due to loss of normal ileocaecal angle and dilated terminal ileum, appearing suspended from a retracted caecum; (iii) ‘Purse string sign/stenosis’– focal stenosis opposite the ileocaecal valve with a rounded off smooth caecum and a dilated terminal ileum (iv) ‘String sign’ – narrow stream of barium indicating stenosis of terminal ileum. String sign can also be seen in Crohn’s disease (CD). On CT scan, ileocaecal TB in early stages is seen as a mild circumferential mural thickening of the caecum and terminal ileum (Figs 5, 6). Fig. 6. Small bowel tuberculosis. (a)Axial CT image in a patient with subacute intestinal obstruction shows marked mural thickening of the terminal ileum (arrow) with mucosal enhancement and adjacent fat stranding. (b)Axial CT image in another patient with subacute intestinal obstruction shows marked mass like thickening of a distal ileal loop (arrow). (c, d)Axial and coronal CT images in a young male with acute intestinal obstruction show luminal narrowing with mucosal thickening and enhancement involving proximal ileum (arrows). There is marked dilatation of proximal bowel loops.Later, the ileocaecal valve and adjacent medial wall of the caecum is asymmetrically thickened. In advanced stages, gross mural thickening with adherent loops, large regional nodes, and mesenteric thickening can form a soft tissue mass centred on the ileocaecal junction (Fig. 4). Isolated jejunal involvement is rare (Fig. 7).
Fig. 7. Jejunal tuberculosis. (a) Barium meal follow through image in a patient with multiple episodes of intestinal obstruction shows a tight short segment stricture involving the proximal jejunal loop (arrow). (b, c) Axial (b) and coronal (c) CT images of the same patient show a long segment mural thickening of the proximal jejunal loop (arrows).There can be multisegmental involvement as well, though it is less common compared to CD (Fig. 8).Fig. 8. Multifocal small bowel tuberculosis. (a)Axial CT image in a patient with intermittent episodes of pain abdomen and fever for 1 month shows a short segment of mural thickening and luminal narrowing involving a distal ileal loop (arrow). (b) Coronal CT image in the same patient shows a skip lesion involving mid jejunum (arrow). Note that the entire small bowel is dilated.Gastroduodenal TB is rare and is reported to comprise 0.5–4% of the GI TB. A high index of suspicion is required to diagnose TB at this site. The diagnosis is usually made after surgical intervention (exploratory laparotomy). In the study by Nagi et al., the following findings were reported on US: lymphadenopathy (n = 15), mural thickening (n = 10), ascites (n = 11) and pleural effusion (n = 9). CT findings included necrotic lymphadenopathy (n = 7), non-necrotic lymphadenopathy with or without calcification (n = 3), circumferential mural thickening (n = 7), ascites with or without peritoneal thickening and enhancement (n = 5) and thickening of ileocaecal junction and/or terminal ileum (n = 4). Besides mural thickening, other patterns of involvements were polypoidal intraluminal growth mimicking duodenal malignancy (n = 3), duodenal ulcerations (n = 3), duodenal perforation with the localized leak (n = 4) (Fig. 9).Fig. 9. Gastroduodenal tuberculosis. (a) Upper GI endoscopy image in a patient with dyspepsia and vomiting for few weeks reveals an elevation in the greater curvature (arrow) with ulceration.(b) Barium meal image of the same patient shows a short segment stricture involving the second part of the duodenum (arrow).Isolated tubercular appendicitis is rare. In a study by Chong et al., an incidence of 0.08% in appendicectomy specimens was reported. It is reported to comprise 0.2% of TB cases and 8.6% of abdominal TB cases. The imaging appearance may be indistinguishable from acute appendicitis, however, in the setting of contiguous involvement of caecum and terminal ileum, the diagnosis of TB may be suspected. Mass mimicking malignancy may be seen.Colorectal TB has been reported to comprise ~10% of the GI TB. In the study by Nagi et al. comprising 74 patients with colorectal TB, the commonest site was a transverse colon, followed by rectum and ascending colon(Figs 10, 11). Fig. 10. Colonic tuberculosis. (a, b) Barium enema images in a middle-aged male with history of constipation for 2 months shows a tight stricture involving the ascending colon and hepatic flexure (arrow, a). In another patient with similar complaints of longer duration, there is multifocal; involvement of the sigmoid colon (arrow, b) and descending colon (short arrow, b).(c) Contrast-enhanced CT image in an elderly male with history of pain lower abdomen and alternating constipation and diarrhoea shows an annular lesion involving the ascending colon (arrow, c). Coronal CT image in another patient with fever and back pain shows mural thickening of the distal small bowel and right colon (arrows,c and d) with a left-sided psoas abscess (short arrow, d).Fig. 11. Magnetic resonance imaging in bowel TB. (a, b) Coronal non contrast (a) and contrast enhanced T1-weighted (b) MR images in an 18-year-old female with pain abdomen, fever and constipation for 3 months show segmental mural thickening (arrow, a) and enhancement (arrow,b) involving the ascending colon. (c, d) Axial T2-weighted and coronal post contrast T1-weighted images in a 44-year-old female with history of diarrhoea for 1 month show a long segment mural thickening (arrow, c) and enhancement (arrow, d) involving a distal ileal loop.Seventy-three percent patients had isolated colonic involvement without the involvement of the ileocaecal region. Noncontiguous involvement of the ileocaecal region was reported in rest of the patients. Multiple sites were involved in 10 patients and diffuse colonic involvement was reported in 15 patients (Fig. 10). The most common radiological finding was strictures (54%),followed by features of colitis (39%) and polypoid lesions(7%). Perforations and fistulae were reported in 18.9% of patients. Colonic TB may mimic malignancy. Complications such as bowel perforation, obstruction, and localized abscess formation can also be seen with GI TB. Less commonly, fistula and sinus formation are seen with the involvement of the GI tract. Anal canal involvement can also present with multiple fistulae (Fig. 12). Fig. 12. Anal disease in tuberculosis. (a, b) Axial ，CT images in a patient with fever, altered bowel habits and per-anal discharge for 2 weeks show ano-cutaneous fistula on the left side (arrow). (c,d) Contrast-enhanced MRI. Axial T2-weighted MRI in another patient with similar complaints shows a horse-shoe peri-anal fistula (arrow, c).Coronal contrast-enhanced MRI in the same patient shows a complex fistula with abscess in the right ischio-anal fossa (arrow, d).Peritoneal TB is the most common presentation of abdominal TB and includes the involvement of the peritoneal cavity, mesentery and omentum. Though it is believed that its origin is haematogenous, peritoneum may be involved secondary to lymph node rupture, GI dissemination or tubal involvement in females. Peritoneal involvement (peritonitis) is subdivided into three main types, that is, wet type, fibrotic and dry types. A considerable overlap may be seen in these presentation patterns (Fig. 13). Fig. 13. Peritoneal tuberculosis. (a) Axial contrast-enhanced CT image in a patient with fever and abdominal distension for 8 weeks shows ascites (arrow) with peritoneal enhancement (short arrow). (b–d) High-resolution ultrasound images in a patient with abdominal pain and fever show omental thickening (arrow, b). Also note an omental lymph node (arrow, c).There is small loculated collection with marked omental thickening (arrow, d). (e) Cocoon. High-reso-lution ultrasound image in another patient with subacute intestinal obstruction shows dilated clumped small bowel loops (short arrows) and a hypoechoic membrane (arrow).Abdominal ‘cocoon’ may be considered a fourth type of peritoneal TB in view of its distinctive clinical and imaging presentation and therapeutic implications. Abdominal cocoon or sclerosing encapsulating peritonitis has also been reported with abdominal TB which usually presents with intestinal obstruction. On CT, it is seen as the concentration of a part of or the entire small bowel with or without large bowel in the centre of the abdomen encased by a soft tissue density mantle (Fig. 14). (a, b) Axial and coronal CT images show clumping of the pelvic small bowel loops (arrows). Note the thick enhancing encapsulating membrane (short arrow).Fixed and adherent intestinal loops with bowel wall thickening, localized fluid collections, enhancing peritoneal thickening, calcification in peritoneum or bowel wall can also be seen on CT.Ascites may be free or with loculations with CT density of around 20–45 HU. Omental involvement can be seen as omental fat stranding/densification or thickening forming an omental cake.Peritoneal TB has to be differentiated from peritoneal carcinomatosis, both of which may have overlapping clinical symptoms. Useful CT sign to differentiate between two is peritoneal thickening which, in the former condition, is smooth and regular, and in the latter, is nodular and irregular. In doubtful cases, needle aspiration can be performed under image guidance. Other differentials for peritoneal TB include nontubercular peritonitis, pseudomyxoma peritonei, and mesothelioma.Abdominal lymph node involvement is usually seen in association with GI TB and less commonly with the peritoneal and solid organ involvement. Most commonly involved lymph node chains are related to drainage of the terminal ileum, IC junction and right colon.Common findings on imaging include an increase in size (adenopathy) or a number of lymph nodes with or without central caseation which is of low attenuation on CT (Fig. 15). Fig. 15. Abdominal lymph node tuberculosis. (a) High-resolution ultrasound image in a 22-year-old male with subacute intestinal obstruction shows marked mural thickening of a distal ileal loop (arrow) with an enlarged lymph node in right iliac fossa (short arrow). (b–d) Axial CT images in a patient on antitubercular treatment for abdominal tuberculosis for 3 months show necrotic lymph nodes (arrows, b–d). Few lymph nodes also show calcification (short arrows, d). CT image in a patient with history of abdominal tuberculosis several years back having pain abdomen shows few calcified lymph nodes (arrows). (f) Contrast-enhanced CT image in a patient with fever and lump abdomen shows a conglomerate necrotic lymph nodal mass is seen in peripancreatic location (arrow).Lymph nodes may be discrete or conglomerate. In the latter case, nodes can form large masses.Calcification and fibrosis are seen in healing stages.Imaging features of abdominal TB in immunocompetent versus immunocompromised patientsMost of the data regarding abdominal tuberculosis in immunocompromised patients come from HIV-infected patients. Clinical presentation of TB in early HIV infection resembles that observed in immunocompetent persons. It can be extrapolated that the imaging features of patients with early HIV infection (with normal CD+T cell counts) and TB will be no different from those without HIV infection. In patients with AIDS/immunosup-pression, there is a higher prevalence of extrapulmonary involvement. In a study, pulmonary involvement, extrapulmonary involvement and both pulmonary and extrapulmonary involvement occurred in 38%, 30% and 32% patients respectively. A few studies have evaluated the differences in the imaging mani-festations between patients with early HIV infection (or immunocompetent) and AIDS (immunocompromised) patients. The AIDS group had a significantly higher proportion of splenomegaly, hepatomegaly, lymphadenopathy, biliary tract abnormalities, gut wall thickening and ascites. There were no significant differences in pancreatic involvement between the AIDS and HIV-groups.In conclusion, abdominal TB is a great masquerader and clinical, as well as imaging features, mimic those of many other diseases. A definitive diagnosis although requires cytological or histopathological analysis, imaging features can aid in diagnosis, especially when there is a high degree of clinical suspicion. Additionally, imaging can also guide tissue sampling for culture and histopathology. Knowledge of various common and uncommon imaging features of abdominal TB is thus essential for early diagnosis.
原文：Gupta P, Kumar S, Sharma V, Mandavdhare H, Dhaka N, Sinha SK, Dutta U, Kochhar R. Common and uncommon imaging features of abdominal tuberculosis. J Med Imaging Radiat Oncol. 2019 Jun;63(3):329-339. doi: 10.1111/1754-9485.12874. Epub 2019 Apr 1. PMID: 30932343.