Tuberculosis Gastrointestinal PDF
Tuberculosis Gastrointestinal PDF
Tuberculosis Gastrointestinal PDF
MINIREVIEWS
Uma Debi, Vasudevan Ravisankar, Kaushal Kishor Prasad, Saroj Kant Sinha, Arun Kumar Sharma
Uma Debi, Division of GE Radiology, Department of Super- occur in the gastrointestinal tract, peritoneum, lym-
speciality of Gastroenterology, Postgraduate Institute of Medical phnodes or solid viscera. Various investigative methods
Education and Research, Chandigarh 160 012, India have been used to aid in the diagnosis of abdominal
Vasudevan Ravisankar, Department of Radiodiagnosis, Post- tuberculosis. Early diagnosis and initiation of antituber-
graduate Institute of Medical Education and Research, Chandi-
culous therapy and surgical treatment are essential to
garh 160 012, India
Kaushal Kishor Prasad, Division of GE Histopathology, Depart- prevent morbidity and mortality. Most of the patients
ment of Superspeciality of Gastroenterology, Postgraduate Insti- respond very well to standard antitubercular therapy
tute of Medical Education and Research, Chandigarh 160 012, and surgery is required only in a minority of cases. Im-
India aging plays an important role in diagnosis of abdominal
Saroj Kant Sinha, Department of Superspeciality of Gastroenter- tuberculosis because early recognition of this condition
ology, Postgraduate Institute of Medical Education and Research, is important. We reviewed our experience with the find-
Chandigarh 160 012, India ings on various imaging modalities for diagnosis of this
Arun Kumar Sharma, Division of GE Virology, Department of potentially treatable disease.
Superspeciality of Gastroenterology, Postgraduate Institute of
Medical Education and Research, Chandigarh 160 012, India
2014 Baishideng Publishing Group Inc. All rights reserved.
Author contributions: Debi U, Ravisankar V and Sinha SK
contributed equally in generating the figures and writing the ar-
ticle; Sharma AK contributed in writing the article; and Prasad Key words: Tuberculosis; Abdomen; Extrapulmonary;
KK substantially contributed in writing the article, generating the Gastrointestinal tract
figures, revising the article critically and gave final approval of
the version to be published. Core tip: Tuberculosis has become a resurgent global
Correspondence to: Kaushal Kishor Prasad, MD, PDC, CFN, problem with increasing numbers of immunocompro-
MAMS, FICPath, Additional Professor, Chief, Division of GE mised patients, largely related to the global acquired
Histopathology, Department of Superspeciality of Gastroenterol-
ogy, Postgraduate Institute of Medical Education and Research,
immunodeficiency syndrome pandemic. The spread of
Sector 12, Chandigarh 160 012, the disease is further aided by poverty, overcrowding,
India. kaushalkp10@hotmail.com and drug resistance. Abdominal tuberculosis rates are
Telephone: +91-172-2756604 Fax: +91-172-2744401 rising, consistent with the overall trend. Nonspecific
Received: January 30, 2014 Revised: March 16, 2014 features of the abdominal tuberculosis result in difficulty
Accepted: June 14, 2014 in establishing a diagnosis. After a diagnosis has been
Published online: October 28, 2014 established, prompt initiation of treatment helps prevent
morbidity and mortality as it is a treatable disease. This
article should alert the clinician to consider abdominal
tuberculosis in the correct clinical setting to ensure
Abstract timely diagnosis and enable appropriate treatment.
Abdominal tuberculosis is an increasingly common dis-
ease that poses diagnostic challenge, as the nonspecific
Debi U, Ravisankar V, Prasad KK, Sinha SK, Sharma AK.
features of the disease which may lead to diagnostic
Abdominal tuberculosis of the gastrointestinal tract: Revisited.
delays and development of complications. This condi-
World J Gastroenterol 2014; 20(40): 14831-14840 Avail-
tion is regarded as a great mimicker of other abdominal
able from: URL: http://www.wjgnet.com/1007-9327/full/v20/
pathology. A high index of suspicion is an important
i40/14831.htm DOI: http://dx.doi.org/10.3748/wjg.v20.i40.14831
factor in early diagnosis. Abdominal involvement may
Tubercular lymphadenopathy
Peritoneal tuberculosis
Acute
Chronic
Wet ascitic type
Fixed fibrotic type
Dry plastic type
Encysted/loculated type
Visceral tuberculosis
Liver, pancreas, spleen etc.
Gastrointestinal tuberculosis
Esophageal tuberculosis
Gastric tuberculosis
Figure 2 Plain X ray images. Plain abdominal radiographs in supine (A) and Duodenal tuberculosis
erect (B) position showing dilated small bowel loops with air fluid levels in a pa- Jejunal and ileocecal tuberculosis
tient who presented with subacute intestinal obstruction secondary to tubercular Colorectal tuberculosis
ileal stricture.
of organisms on smear and culture is low. Staining for tively in confirmed (AFB/culture/histopathology) cases
acid fast bacilli is positive in less than 3% of cases and a of gastrointestinal TB and positive results in 72.41% of
positive culture is seen in only 20% of cases. Ascitic fluid the suspected gastrointestinal TB cases[18].
adenosine deaminase (ADA) levels are elevated in tuber-
cular ascites. Serum ADA level above 54 U/L, ascitic flu-
id ADA level above 36 U/L and an ascitic fluid to serum CLINICAL PRESENTATION OF
ADA ratio more than 0.98 are suggestive of tuberculo- ABDOMINAL TB
sis[14]. However, in cases of co-infection with HIV, ascitic
The abdominal TB is of four types: tubercular lymphade-
ADA levels can be normal or low. Also, falsely high val-
nopathy, peritoneal TB, gastrointestinal TB and visceral
ues can be seen in malignant ascites. Interferon- levels
TB (Table 2).
are also elevated in tubercular ascites[15]. The sensitivity
and specificity increased by combining ascitic fluid ADA
and interferon- assay. The various radiological studies Tubercular lymphadenopathy
are used for the diagnosis of abdominal TB include ultra- Abdominal lymphadenopathy is the most common
sonography (USG), CT, barium studies and magnetic res- manifestation of the abdominal TB. It usually follows
onance imaging (MRI). Ultrasound is an initial modality the drainage of the affected organs, though it can af-
of choice which is useful in picking up lymphadenopathy, fect any lymphnode in abdomen. The most commonly
tubercular ascites, peritoneal thickening, omental thicken- involved lymphnodes are the mesenteric nodes, omental
ing and bowel wall thickening in some cases. Plain radio- nodes, those at porta hepatis, along the celiac axis and in
graphs may show enteroliths, perforation and features of peripancreatic location. The commonest route of trans-
intestinal obstruction (Figure 2A and B). Barium studies mission is usually secondary to ingestion of the infected
are still gold standard in diagnosing strictures, fistulae, material along with associated intestinal TB. Hematog-
erosions, etc. Contrast enhanced CT and CT enterography enous route of transmission and contiguous spread from
provide adequate cross sectional imaging in depicting adjacent affected abdominal organ can also occur. On
various forms of abdominal TB. imaging, the appearance of affected lymphnodes can vary
In the recent years various molecular and immunolog- from increase in the number of the normal sized nodes
ical techniques are used as a new approach for the rapid to increase in the size of the nodes to formation of large
diagnosis of abdominal TB[16,17]. The clinical samples conglomerate lymphnodal masses. However, the most
can be ascitic fluid, lymphnode, thickened omentum or common presentation is presence of multiple mildly
mesentery. The insertion sequence IS6110 is used as a enlarged nodes in clusters which are circular or ovoid.
target for polymerase chain reaction (PCR) amplification They usually have central areas of caseous necrosis with
in these samples[16]. Real time assay using fluorescence peripheral enhancement (Figure 3).
resonance energy transfer hybridization probes show a
positivity index of 36% in those patients with clinical and Peritoneal tuberculosis
radiological suspicion of TB, but with negative acid fast Traditionally the peritoneal TB is divided into three
bacilli (AFB) and culture[17]. In addition, immune charac- types: (1) The wet ascitic type is more common and is
terization show depleted CD4+ count and increased levels associated with large amounts of free or loculated fluid
of interferon- and tumor necrosis factor- cytokines. in abdomen; the ascites is usually of high density due to
Multiplex PCR using MPB64 and IS6110 are useful in increased protein content of the inflammatory exudate.
rapid diagnosis of gastrointestinal TB[18]. Multiplex PCR Associated peritoneal enhancement is usually present;
has sensitivity and specificity of 90% and 100%, respec- (2) The fixed fibrotic type is relatively less common and
B
Figure 3 Ultrasound image. Multiple enlarged conglomerate lymphnodes in
retroperitoneum with hypoechoic centers due to caseation.
A B
Figure 7 Barium swallow image. An old treated case of pulmonary tubercu- Figure 8 Computed tomography images. Contrast enhanced computed to-
losis showing traction diverticulum in right lateral wall of upper thoracic esopha- mography with oral contrast of another case of esophageal tuberculosis show-
gus (A). There is also a long segment smooth stricture in the distal thoracic ing circumferential mural thickening in the mid thoracic esophagus. Histopatho-
esophagus with pulsion diverticulum in the right lateral wall of distal thoracic logical examination of biopsies from the involved segments showed epithelioid
esophagus (A, B). granulomas.
tremely rare in immunocompetent patients and ac- pertrophic variety, presence of multiple miliary tubercles
count for only 0.2%-1% of gastrointestinal TB [20,21], and tubercular pyloric stenosis in late stages. Associated
but it is more commonly seen in AIDS patients [10,22]. tubercular lymphadenitis is usually present.
The symptoms are usually retrosternal pain, dysphagia On imaging these lesions can appear as benign ulcers
and odynophagia. In esophagus, TB usually occurs in or erosions. In late stages features of pyloric stenosis
the middle third and manifests as ulcerative lesion or a with distorted antropyloric region can be present (Figure
tumor like lesion. The esophageal involvement is usually 9). The differential diagnosis of gastric TB can be carci-
secondary to a contiguous tubercular mediastinal nodal noma, lymphoma and other infections like syphilis.
involvement (extrinsic TB). Hematogenous spread from
a small endobronchial lesion can occur as well. Primary Duodenal TB: Duodenal involvement is seen in
involvement of esophagus (intrinsic TB) is extremely 2%-2.5% of all gastrointestinal TB cases[26]. As in stom-
rare and can be attributed to ingestion of the infected ach, primary involvement is rare. The most common
sputum. site of primary involvement is the third part of duode-
On barium studies, extrinsic TB is seen as narrow- num[27]. It can be intrinsic, extrinsic or both[28]. Extrinsic
ing or displacement of esophagus especially at the level form, which is more common, is usually secondary to the
of carina[23]. In late stages, the patients may present with lymphadenopathy in the C-loop of the duodenum. The
formation of ulcers, strictures and fistulae. In fibrotic intrinsic form can be ulcerative, hypertrophic or ulcero-
mediastinal disease, traction diverticulae can occur in the hypertrophic. It is usually complicated by formation of
adjoining esophagus (Figure 7)[24]. The diagnosis of pri- strictures or fistulas. These patients usually present late
mary esophageal TB is usually made on histopathological with features of obstruction where strictures are identi-
examination as the radiological features are nonspecific fied on imaging or an extrinsic impression by lymphade-
(Figure 8) and are driven by high degree of suspicion. nopathy is noted. Barium studies demonstrate presence
Since the tuberculous granulomas are located deep in of narrowing either extrinsic or intrinisic (Figure 10)[29].
the submucosal layer of esophagus, multiple and deep Band like narrowing of third part of duodenum may
esophageal endoscopic biopsies should be obtained for mimic superior mesenteric artery syndrome. A persistent
optimum diagnosis[21]. narrow stream of barium in the bowel suggestive of the
string sign may be seen. Formation of fistulous com-
Gastric TB: The gastric involvement is usually associated munication is readily identified by real time barium stud-
with pulmonary tuberculosis or immunodeficient state[20]. ies. Cross sectional imaging like CT demonstrates luminal
Primary involvement of the stomach is rare (0.4%-2%) narrowing, mural thickening of duodenum (Figure 11)
because of the bactericidal property of the gastric acid, and also adjacent lymphnodal masses causing compres-
scarcity of lymphoid tissue in gastric wall and thick intact sion. The differential diagnosis of duodenal TB can be
gastric mucosa. The other routes of spread can be either lymphoma, malignancy, atypical peptic ulcer disease or
hematogenous or from adjacent lymphnodes. The pa- carcinoma of head of pancreas. Since the features of du-
tients may present with nonspecific symptoms of vague odenal TB can be nonspecific, a high index of suspicion
epigastric discomfort, weight loss and fever or may pres- is necessary for diagnosis.
ent with features of gastric outlet obstruction. Morpho-
logically many types of gastric involvement can be seen. Jejunal and ileocecal TB: The most common site of
The most common type is ulcerative lesion along the GI involvement is the ileocecal region which is involved
lesser curvature and pylorus[25]. The other types are hy- in 64% of cases of gastrointestinal TB[30]. The terminal
A B
Figure 9 Endoscopic images. Gastric tuberculosis with gastric outlet obstruction - before (A) and after (B) balloon dilatation.
Figure 10 Barium meal follow through image. Long segment circumferential Figure 11 Computed tomography images. Same patient showing smooth
narrowing in first and second part of duodenum. circumferential mural thickening involving the duodenum (D1 and D2). Biopsy
showed granulomatous inflammation consistent with tuberculosis. Few enlarged
subcentimetric lymphnodes are also seen in the mesentery.
ileum is more commonly involved because of the vari-
ous contributing factors like stasis, presence of abundant
lymphoid tissue, increased rate of absorption at this site and the cecum are concomitantly involved in the majority
and closer contact of the bacilli with the mucosa[7,31,32]. of cases (Figure 12C-F).
Concomitant jejunal involvement may be seen in the form Plain X-ray abdomen may show enteroliths, features
of single or multiple short or long segment strictures. Iso- of obstruction like dilated bowel loops with multiple air
lated jejunal involvement is rare, and if present, may mim- fluid levels (Figure 2A and B), or presence of air under
ic Crohns disease (CD)[33]. The clinical features of small diaphragm in case of perforation. In addition, there
intestinal TB are protean, and the patients usually present may be calcified lymphnodes, calcified granulomas and
with colicky abdominal pain, borborygmi and vomiting[30]. hepatosplenomegaly. The features which may be seen in
The most common complication is bowel obstruction barium studies are accelerated intestinal transit; hyperseg-
secondary to hyperplastic mural thickening, stricture for- mentation of the barium column (chicken intestine),
mation or due to adhesions[9]. Tuberculosis accounts for precipitation, flocculation and dilution of the barium;
5%-9% of all small intestinal perforations in India, and is stiffened and thickened folds; luminal stenosis with
the second commonest cause after typhoid fever[30]. smooth but stiff contours (hourglass stenosis), mul-
Morphologically, the lesions in intestinal tuberculosis tiple strictures with segmental dilatation of bowel loops;
are classified into ulcerative and ulcero-hypertrophic va- and fixity and matting of bowel loops (Figure 13A). Vari-
rieties. The distinction between these two lesions is not ous signs have been described in the ileocecal TB are the
sharp and the two types may co-exist (Figure 12A and B). Fleischner or inverted umbrella sign, in which there
The macroscopic features present a very wide range and is thickening of the lips of the ileocecal valve and/or
at times distinction from CD may be difficult. Confluent wide gaping of the valve with narrowing of the termi-
granulomas, presence of caseation necrosis, presence of nal ileum. The Goose neck deformity signifies loss
granulomas in lymphnode in the absence of granuloma- of normal ileocaecal angle and dilated terminal ileum,
tous lesions in the intestine, absence of transmural cracks appearing suspended from a retracted, fibrosed cecum.
and fissures (present in CD) serve to distinguish intestinal The Purse string stenosis signifies localized stenosis
tuberculosis from CD[30]. Caseation necrosis remains a opposite the ileocecal valve with a rounded off smooth
very important criterion for the histological diagnosis of cecum and a dilated terminal ileum. The two other signs
intestinal TB. The terminal ileum, ileocecal (IC) junction are Stierlin sign and string sign. The Stierlin sign
A B C
D E F
Figure 12 Endoscopic images. A: Ulcerative form of ileocaecal (IC) tuberculosis - multiple ulceration on IC valve, caecum and ascending colon with nodularity in
intervening area and some mucosal bridges; B: Hypertrophic form of ileocaecal tuberculosis - mass like lesion on IC valve with ulceration on surface; C: Ileocaecal
tuberculosis - contracted caecum, narrowed and deformed IC valve and multiple ulceration on IC valve, caecum and ascending colon; D: Superficial ulcers in terminal
ileum; E: Gaping IC valve with multiple ulcers on IC valve, caecum and ascending colon; F: Terminal ileal stricture with multiple ulcers on ileocaecal valve and con-
tracted caecum.
A B
Figure 13 Barium meal follow through images. A: A young patient who was a known case of peritoneal tuberculosis (TB) showing matting of small bowel loops; B:
Luminal narrowing with ulcerations involving the terminal ileum and ileocaecal junction with contracted cecum- characteristic of ileocecal TB.
is a manifestation of acute inflammation superimposed thickening of the IC valve and medial wall of the cecum,
on a chronically involved segment and is characterized by exophytic and engulfing the terminal ileum is seen. The
lack of barium retention in the inflamed segments of the associated lymphadenopathy is usually massive and cen-
ileum, cecum and variable length of the ascending colon, tral areas of low attenuation are indicative of caseous
with a normal configured column of barium on either necrosis. Multiple small segment concentric strictures
side. It appears as a narrowing of the terminal ileum with involving the jejunum and ileum can also be seen (Figure
rapid emptying into a shortened, rigid or obliterated ce- 15). Enteroclysis followed by a barium enema may still be
cum. The String sign shows persistent narrow stream the best protocol for evaluation of intestinal TB[23].
of barium indicating stenosis (Figure 13B). Both Stierlin
and String signs can also be seen in CD and hence are Colorectal TB: Isolated involvement of colon is 10.8%.
not specific for TB[34]. Computed tomography may show The incidence is increased in the immunocompromised
circumferential wall thickening up to 3 cm in the cecum patients and patients with AIDS. The cecum is the most
and terminal ileum with associated mesenteric lymphade- common site of involvement of colon but it is usually in-
nopathy (Figure 14A and B)[22,35]. Typically, asymmetric volved in contiguous involvement with the terminal ileum
A A B
B
Figure 16 Barium enema images. A: Tuberculous colitis presenting with
concentric stricture in the distal transverse colon and splenic flexure. A fistulous
tract is seen arising from hepatic flexure of colon with ulcerations in adjacent
colon; B: Another patient with tuberculous colitis presenting with mucosal ir-
regularity, ulcers in the sigmoid colon complicated by fistula formation in the
distal sigmoid colon.
USG of abdomen
Figure 17 Management algorithm for abdominal tuberculosis. Reproduced from Sood et al[41]. USG: Ultrasonography; CECT: Contrast enhanced computed tomography.
cases where it is absolutely indicated as in cases of non- strictureplasty in those strictures which cause more than
resolving intestinal obstruction, perforation and abscess 50% luminal compromise[42]. These kinds of conservative
or fistula formation. Even in cases of tuberculous stric- surgeries are usually preferred nowadays. The tuberculous
tures medical management with antituberculous drugs bowel perforations are usually treated with resection of
will result in significant resolution of symptoms in most involved segments with primary anastomosis.
of patients[39]. Endoscopic balloon dilation offers an
alternative to the surgical management of GI strictures
(Figure 9)[40]. Management algorithm for the abdominal CONCLUSION
TB is presented in (Figure 17)[41]. Abdominal TB can be of various forms like peritoneal
All the diagnosed cases of gastrointestinal TB should TB, tuberculous lymphadenopathy, gastrointestinal TB
receive at least 6 mo of antituberculous therapy which and visceral TB. Though gastrointestinal TB usually in-
includes initial two months of therapy with isoniazid, volves the ileocecal region, it can virtually affect any part
rifampicin, pyrazinamide and ethambutol thrice weekly[12]. of GI tract. The symptoms of abdominal TB can be
Although 6 mo treatment regimen is recommended as nonspecific. Various imaging features and radiological
per the revised national tuberculosis program guidelines, signs are useful in making a diagnosis of abdominal TB.
many clinicians extend the treatment regimen to 9 or A high degree of clinical suspicion is required to make
12 mo. However, no difference seen in effectiveness a diagnosis of TB in those areas which are not com-
between the 6 mo short course therapy regimen with monly involved. Various molecular and immunological
rifampicin, isoniazid and pyrazinamide for 2 mo followed techniques are increasingly used for rapid diagnosis in
by rifampicin with isoniazid for another 4 mo (6R series) suspected cases of abdominal TB. Gastrointestinal TB is
and 12 mo standard regimen of ethambutol and isoniazid generally managed with medical therapy with antituber-
with streptomycin supplemented for 2 wk[33]. culous drugs and surgeries are usually conservative and
The surgeries performed in the gastrointestinal TB are done only if absolutely indicated.
are of three types[12]. The first type is the surgery which is
done to bypass the involved segments of bowel as in case
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