diagnosis of abdominal tuberculosis : role of imaging

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* Additional Professor, Department of Medicine, All India Institute of Medical Sciences, Ansari Nagar, New Delhi-110 029. Diagnosis of Abdominal Tuberculosis : Role of Imaging Rita Sood* Tuberculosis has been declared a global emergency by the World Health Organization and is the most important communicable disease worldwide. The prevalence of extra-pulmonary tuberculosis seems to be rising, particularly due to increasing prevalence of acquired immunodeficiency syndrome (AIDS) 1,2 . In patients with extrapulmonary tuberculosis, abdomen is involved in 11% of patients 3 . Though potentially curable, abdominal tuberculosis continues to be a major cause of morbidity and mortality in India. In the abdomen, tuberculosis may affect the gastrointestinal tract, peritoneum, lymph nodes, and solid viscera. The disease can mimic various other gastrointestinal disorders, particularly inflammatory bowel disease, colonic malignancy, or other gastrointestinal infections. Because of the non-specific symptoms and signs, its diagnosis is often delayed. A high index of suspicion therefore needs to be maintained for an early diagnosis and timely treatment. Pathological spectrum of abdominal tuberculosis Abdominal tuberculosis denotes involvement of gastrointestinal tract (GIT), peritoneum, lymph nodes, and solid organs i.e., liver, spleen, and pancreas. The involvement of the gastrointestinal tract is seen in 65%-78% of patients of abdominal tuberculosis 4,5 . The common sites of involvement in GIT are the terminal ileum and the ileocaecal region, followed by colon and jejunum. Rarely, tuberculosis may involve stomach, duodenum, and oesophagus. The intestinal lesions produced by tuberculosis are of three types – ulcerative, hypertrophic, and stricturous. Strictures are usually produced by the cicatricial healing of the ulcerative lesions. A combination of the three morphological forms of lesions i.e., ulcero-constrictive or ulcero- hypertrophic may occur. Many of these patients of gastrointestinal tuberculosis have associated nodal and peritoneal involvement. Peritoneal involvement may be adhesive or ascitic. The nodal involvement due to tuberculosis is commonly mesenteric or retroperitoneal. The lymph nodes may show evidence of caseation or calcification. Intestinal, peritoneal, and nodal tuberculosis may occur together in varying permutations and combinations. Hepatosplenic tuberculosis is common as a part of disseminated and miliary tuberculosis. Macronodular form of hepatosplenic tuberculosis is an uncommon form of tuberculosis. Clinical spectrum The disease can present at any age but is seen most commonly in young adults. In children, the peritoneal and nodal form of tuberculosis is much more common than intestinal tuberculosis 6 . The modes of presentation can vary from acute, acute- on-chronic or chronic, occasionally as an incidental finding on laparotomy for unrelated causes. The clinical presentation depends upon the site of disease and the type of pathological involvement. Ulcerative type of intestinal tuberculosis can present with chronic diarrhoea and features suggestive of malabsorption. Rectal bleeding is rare but has been reported particularly with colonic tuberculosis. Stricturous type of intestinal tuberculosis presents with features of recurrent subacute intestinal obstruction in the form of obstipation, vomiting, abdominal distension, and colicky abdominal pain. This may be associated with gurgling, feeling of ball of wind moving in the abdomen, and visible intestinal loops. These symptoms may get relieved spontaneously after passage of flatus or sometimes CLINICAL MEDICINE

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Page 1: Diagnosis of Abdominal Tuberculosis : Role of Imaging

* Additional Professor,Department of Medicine,All India Institute of Medical Sciences,Ansari Nagar, New Delhi-110 029.

Diagnosis of Abdominal Tuberculosis : Role of Imaging

Rita Sood*

Tuberculosis has been declared a globalemergency by the World Health Organization andis the most important communicable diseaseworldwide. The prevalence of extra-pulmonarytuberculosis seems to be rising, particularly dueto increasing prevalence of acquiredimmunodeficiency syndrome (AIDS)1,2. In patientswith extrapulmonary tuberculosis, abdomen isinvolved in 11% of patients3. Though potentiallycurable, abdominal tuberculosis continues to bea major cause of morbidity and mortality in India.In the abdomen, tuberculosis may affect thegastrointestinal tract, peritoneum, lymph nodes,and solid viscera. The disease can mimic variousother gastrointestinal disorders, particularlyinflammatory bowel disease, colonic malignancy,or other gastrointestinal infections. Because of thenon-specific symptoms and signs, its diagnosis isoften delayed. A high index of suspicion thereforeneeds to be maintained for an early diagnosis andtimely treatment.

Pathological spectrum of abdominaltuberculosisAbdominal tuberculosis denotes involvement ofgastrointestinal tract (GIT), peritoneum, lymphnodes, and solid organs i.e., liver, spleen, andpancreas. The involvement of the gastrointestinaltract is seen in 65%-78% of patients of abdominaltuberculosis4,5. The common sites of involvementin GIT are the terminal ileum and the ileocaecalregion, followed by colon and jejunum. Rarely,tuberculosis may involve stomach, duodenum, andoesophagus. The intestinal lesions produced bytuberculosis are of three types – ulcerative,hypertrophic, and stricturous. Strictures are usually

produced by the cicatricial healing of the ulcerativelesions. A combination of the three morphologicalforms of lesions i.e., ulcero-constrictive or ulcero-hypertrophic may occur. Many of these patientsof gastrointestinal tuberculosis have associatednodal and peritoneal involvement. Peritonealinvolvement may be adhesive or ascitic. The nodalinvolvement due to tuberculosis is commonlymesenteric or retroperitoneal. The lymph nodesmay show evidence of caseation or calcification.Intestinal, peritoneal, and nodal tuberculosis mayoccur together in varying permutations andcombinations. Hepatosplenic tuberculosis iscommon as a part of disseminated and miliarytuberculosis. Macronodular form of hepatosplenictuberculosis is an uncommon form of tuberculosis.

Clinical spectrumThe disease can present at any age but is seenmost commonly in young adults. In children, theperitoneal and nodal form of tuberculosis is muchmore common than intestinal tuberculosis6. Themodes of presentation can vary from acute, acute-on-chronic or chronic, occasionally as anincidental finding on laparotomy for unrelatedcauses. The clinical presentation depends uponthe site of disease and the type of pathologicalinvolvement. Ulcerative type of intestinaltuberculosis can present with chronic diarrhoeaand features suggestive of malabsorption. Rectalbleeding is rare but has been reported particularlywith colonic tuberculosis. Stricturous type ofintestinal tuberculosis presents with features ofrecurrent subacute intestinal obstruction in the formof obstipation, vomiting, abdominal distension,and colicky abdominal pain. This may beassociated with gurgling, feeling of ball of windmoving in the abdomen, and visible intestinalloops. These symptoms may get relievedspontaneously after passage of flatus or sometimes

C L I N I C A L M E D I C I N E

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patients can present with acute intestinalobstruction. Ano-rectal tuberculosis can presentas strictures and fistula-in-ano. Tuberculous fistulaeare usually multiple. In the caecum and largeintestine, lesions are usually hypertrophic andpresent as either obstruction or as abdominallump. Gastroduodenal tuberculosis may presentas peptic ulcer with or without gastric outletobstruction or perforation and may mimicmalignancy. Microscopic involvement of the liveris common in patients with abdominal tuberculosisbut focal lesions in the liver and spleen aregenerally seen as a part of disseminatedtuberculosis. Tuberculosis at unusual sites likepancreas, and oesophagus, more commonlymimics the commoner diseases in those organs,e.g., malignancy. Peritoneal tuberculosis oftenpresents as abdominal distension and ascites orsometimes as a soft cystic lump due to loculatedascites. Lymph node involvement due totuberculosis can present as a lump in centralabdomen, or as vague abdominal pain.

These focal symptoms depend upon the site ofinvolvement and are often associated with systemicmanifestations of tuberculosis in the form of low-grade fever, malaise, night sweats, anaemia, andweight loss. These constitutional symptoms arepresent in about one-third of patients withabdominal tuberculosis7. About one-third ofpatients may have tuberculous involvement ofother organs or systems5. The more commonextra-abdominal sites are lungs, pleura, lymphnodes, and genito-urinary system.

A physical examination may show features ofascites, lump abdomen, or visible peristalsis withdilated bowel loops. However, abdominalexamination may not reveal any findings in a largenumber of patients.

Differential diagnosisBecause of a wide spectrum of clinicalpresentation, abdominal tuberculosis can mimica large number of medical and surgical conditions.Abdominal tuberculosis should be considered in

any patient with unexplained and chronicabdominal symptoms. In the hypertrophic formof intestinal tuberculosis, the clinical picture maymimic malignant neoplasms such as lymphomaor carcinoma. In the ulcero-hypertrophic form, itmay mimic inflammatory bowel disease. The nodalform of abdominal tuberculosis may closely mimiclymphomas. Ascitic form can be difficult todistinguish from malignant peritoneal disease andsometimes ascites due to chronic liver disease.However, a high index of suspicion needs to bemaintained for an early diagnosis and timelytreatment.

InvestigationsHaematological examination may show presenceof anaemia and an elevated ESR. However, theseare nonspecific findings and may not aid much indiagnosis. Tuberculin test may be positive but isof not much value as it does not differentiatebetween an active and inactive disease.Serological tests like soluble antigen fluorescentantibody (SAFA) and enzyme-linkedimmunosorbent assay (ELISA) are not sensitive andare non-specific and can only suggest a probablediagnosis8. In patient with ascites, peritoneal fluidis straw coloured with proteins more than 30g/l,cells more than 1,000/cu.mm (mostlylymphocytes), ascitic/blood glucose ratio of lessthan 0.96, and adenosine deaminase (ADA) levelsof more than 33 U/l9,10. Acid fast bacilli (AFB) arerarely seen on smear but may be cultured fromthe ascitic fluid. The yield may be increased byculturing a litre of fluid concentrated bycentrifugation.

Confirmation of the diagnosis of tuberculosis atany site is ideally established by demonstratingAFB on smear or mycobacterial culture from thetissue or by demonstrating caseating granulomasat histopathology. Since abdominal tuberculosisis paucibacillary, the yield of organisms is low andcharacteristic histological changes are taken asdiagnostic. However, getting a tissue for histologymay not always be possible.

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Radiological investigationsPlay a very important role in the diagnosis ofabdominal tuberculosis. Plain X ray of theabdomen, both erect and supine may show thepresence of multiple air-fluid levels and dilatedbowel loops which signifies presence ofobstruction. The pattern of dilated bowel loopsalongwith clinical symptom profile may give cluesto the site of obstruction. Enteroliths may formproximal to the site of obstruction. Calcification inthe lymph nodes may also be evident. Aradiograph of chest may show evidence of activeor healed pulmonary tuberculosis in some patients.While finding of tuberculous lesions on chest x-ray support the diagnosis of abdominaltuberculosis, a normal chest x-ray does not rule itout.

Barium contrast studies are often rewarding inpatients suspected to have intestinal tuberculosis.Sharp and Goldman reported barium meal follow-through examination as the best diagnostic test,demonstrating bowel lesions highly suggestive oftuberculosis such as multiple strictures anddistended caecum or terminal ileum in 84% ofcases11. The other radiologic findings that may beseen on small bowel study are mucosal irregularityand rapid emptying (ulcerative), flocculation andfragmentation of barium (malabsorption), dilatedloops and strictures, displaced loops (enlargedlymph nodes), and adherent fixed loops (adhesiveperitoneal disease). The thickening of theileocaecal valve lips and/or wide gaping of thevalve with narrowing of the terminal ileum(Fleischner sign) has been described ascharacteristic of tuberculosis12. The mucosal detailspossible with double contrast barium examinationallows visualisation of the ulceration in the earlystages of the disease. These ulcers are shallowwith characteristic elevated margins. Withprogression, the ulcers may become confluent.

In ileocaecal tuberculosis, double-contrast bariumenema may show a deformed (irregular,shortened, narrowed) caecum, deformed andincompetent ileocaecal valve, dilated ileum and

a distorted ileo-caecal junction with increased(obtuse) ileocaecal angle, a shortened ascendingcolon and an upwardly displaced caecum13.

In a study conducted by us, barium studies werehelpful in 18 out of 24 (75%) patients suspectedto have intestinal tuberculosis14. Findings includeddilated bowel loops, strictures, deformed andpulled-up caecum, ulceration of ileum, bowel wallthickening, and extrinsic compression by lymphnodes. Thus, contrast barium studies seem to havea good diagnostic yield, when performed inpatients with suspected intestinal involvement.

Imaging plays a very important role in thediagnosis of abdominal tuberculosis particularlyextra-intestinal disease.

UltrasonographyUltrasonography being a widely availableinvestigation, is now a ‘low threshold’ diagnosticprocedure for all patients suspected to haveabdominal tuberculosis. It can accuratelydemonstrate small quantities of ascitic fluid andis an effective method for detection of peritonealdisease.

The reported findings include multiple, thin,complete and incomplete septae, visible echogenicdebris seen as fine strands or particulate matterwithin the fluid15,16 (Fig. 1). These strands of septaemay be due to high fibrin content of the exudativeascitic fluid. Septae have also been reported in afew cases of malignant ascites17. Peritonealthickening and nodularity are the othersonographic features of abdominal tuberculosis.The other conditions that may give rise to thesefindings are peritoneal mesothelioma, peritonealcarcinomatosis, and sometimes pyogenicperitonitis and haemoperitoneum. Omental cakesand adhesions which, in addition to peritonealthickening, are the sonographic features ofperitoneal mesothelioma can also be detected inpatients with tuberculous peritonitis. However, inmesothelioma the ascites is disproportionatelysmall in relation to the degree of tumourdissemination18. In peritoneal mesothelioma, there

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may be adhesive bands between parietalperitoneum and bowel loops, but these bands arethick and immobile unlike fine mobile septae intuberculous peritonitis. Peritoneal tubercles areusually very small and rarely detected byultrasound.

Lymphadenopathy in abdominal tuberculosisusually occurs in mesenteric, peri-pancreatic, peri-portal, and para-aortic groups of lymph nodes.The distribution reflects the lymphatic drainage ofsites in the small bowel and liver that have beenseeded haematogenously. The nodes may be seenas conglomerate masses and/or as scatteredenlarged nodes with hypoechoic or anechoiccentres because of necrosis. The involvement ofretroperitoneal nodes and lesions not confined toone anatomic area of drainage are moresuggestive of lymphoma.

A thickening of the small bowel mesentery of 15mm or more and an increase in mesenteric

echogenicity combined with mesentericlymphadenopathy has been reported as thecharacteristic sonographic feature of earlyabdominal tuberculosis19 (Fig. 2). Pathologically,this mesenteric thickening results fromlymphadenopathy, fat deposition, and oedemadue to lymphatic obstruction which makes it moreechogenic20. Omental thickening with alteredechogenicity was also reported. Ultrasonographyis also sensitive to detect abnormalities in intestinaltuberculosis21. The findings reported includeddilated small bowel loops and bowel wallthickening. Diseased intestine is recognised asnon- specific bowel wall thickening showing as ahypoechoic halo measuring more than 5 mm.Occasionally, ulceration may be visible.Ultrasonography may also be useful for guidingprocedures like ascitic tap and fine needleaspiration cytology or biopsy from the lymph nodesor hypertrophic lesions.

Computed tomographyThough findings are nonspecific, computedtomography (CT) has an advantage overultrasound in that it examines a range ofabdominal structures . Till a few years ago, theonly feature of abdominal tuberculosis reportedon CT was the nonspecific appearance of highdensity ascites22. Over the years, a number ofreports have been published highlighting thewide spectrum of abnormalities demonstratedon CT. The most common findings on CT that

Fig. 1 : Sonogram showing loculated ascites with thinechogenic incomplete septations within.

Fig. 2 : Echogenic mesenteric thickening (within calipers) andsmall round lymph nodes interspersed within the mesentery.

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are highly suggestive of abdominal tuberculosisare high density ascites, lymphadenopathy,bowel wall thickening, and irregular soft tissuedensities in the omental area23-26. Abdominallymphadenopathy is the commonestmanifestation of tuberculosis on CT. Asmentioned earlier, the lymph nodes involvedmost commonly include mesenteric, peri-portal,peri-pancreatic, and upper para-aortic groupsof nodes (Fig. 3).

The contrast enhancement of tuberculous lymphnodes on contrast-enhanced CT (CECT) have beendescribed as (four patterns) - peripheral rimenhancement, non-homogenous enhancement,homogenous enhancement and homogenousnon-enhancement, in that order of frequency27.Different patterns of contrast enhancement couldbe seen within the same nodal group, possiblyrelated to the different stages of the pathologicalprocess. Though not pathognomonic, the patternof peripheral rim enhancement, could be highlysuggestive of tuberculosis in an appropriate clinicalsetting (Fig. 4). A similar pattern can however beseen in malignant adenopathy, especially inmetastasis from testicular tumours, Whipple’sdisease, and rarely in lymphoma followingradiotherapy28. The presence of nodal calcificationin the absence of a known primary tumour in

patients from endemic areas suggests a tubercularaetiology (Fig. 5). A study to evaluate CECTimaging criteria differentiating abdominal lymphnode enlargement due to tuberculosis orlymphoma suggested some differences in theanatomic distribution and the CT enhancementpatterns29. Tuberculosis predominantly involvedlesser omental, mesenteric, and upper para-aorticlymph nodes whereas lower para-aortic lymphnodes were involved more often in Hodgkin’s andnon-Hodgkin’s lymphoma. Tuberculouslymphadenopathy commonly showed peripheralrim enhancement, frequently with a multilocularappearance, whereas lymphomatous adenopathycharacteristically showed homogenousattenuation.

Fig. 3 : CT scan at the level of porta showing multiplehypodense nodes showing peripheral rim enhancement intuberculous lymphadenitis.

Fig. 4 : CECT abdomen showing multiple hypodensemesenteric nodes having enhancing peripheral rim.

Fig. 5 : Tuberculous lymphadenitis showing multiple lymphnodes at porta with amorphous calcification.

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Ascites in abdominal tuberculosis can either befree or loculated. Characteristically, it is a highdensity ascites which could be because of highprotein and cellular contents of the fluid. A similarperitoneal appearance may occur incarcinomatosis and mesothelioma. Recently, theCT features that can help in differentiatingtuberculous peritonitis from peritonealcarcinomatosis have been described. A smoothperitoneum with minimal thickening and markedenhancement after contrast suggests tuberculousperitonitis whereas nodular and irregularperitoneal thickening suggests the presence ofperitoneal carcinomatosis30 (Fig. 6). Mesentericinvolvement and presence of macronodules (>5mm in diameter), a thin omental line (fibrouswall covering the infiltrated omentum), peritonealor extraperitoneal masses with low density centresand calcification, and splenomegaly or spleniccalcification have been more commonly seen withtuberculous peritonitis31. Pelvic tuberculousperitonitis can sometimes mimic pelvicinflammatory disease.

The diagnosis of tuberculosis is suggestive whenloculated fluid collections are detected in thepresence of omental infiltration, peritonealenhancement, transperitoneal reaction, andmesenteric or bowel involvement. Bowel wallthickening is a non-specific manifestation ofabdominal tuberculosis. The most common CT

finding is a mural thickening affecting the ileo-caecal region, either limited to terminal ileum,caecum, or both the regions (Fig. 7). Though non-specific, when associated with other suggestivefeatures, it can be helpful in diagnosis ofabdominal tuberculosis. Diffuse bowel wallthickening can also occur due to intestinalinvolvement by lymphomas.

The other CT features reported to be highlysuggestive of abdominal tuberculosis are irregularsoft tissue densities in the omental area, low densitymasses surrounded by thick solid rims, and adisorganized appearance of soft tissue densities,fluid and bowel loops forming a poorly definedmass23. Involvement of the liver and spleen inmiliary tuberculosis may appear on CT as tiny lowdensity foci widely scattered throughout the organ.The macronodular form of hepatosplenictuberculosis may be seen as multiple lowattenuation (15-50 HU), 1-3 cm round lesions orsimple tumour like masses. The lesions may showperipheral enhancement after i-v contrastadministration32. The tuberculous involvement ofthe pancreas may show as well defined hypoechoicareas on ultrasonography and as hypodensenecrotic regions within the enlarged pancreas13.

Our study on the role of ultrasonography and CTabdomen in abdominal tuberculosis suggestedthat CT was more accurate than ultrasound in

Fig. 6 : An axial scan through pelvis showing presence offree ascites surrounded by smoothly thickened and enhancingperitoneum.

Fig. 7 : CECT abdomen showing diffuse circumferential muralthickening of caecum.

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detecting abnormalities like peri-portal and peri-pancreatic lymph nodes, and bowel wallthickening11. This may be due to the disturbanceof the sonographic window by bowel gas.However, bowel wall dilatation was betterappreciated on ultrasound than CT scan.Therefore, while CT appears to be more sensitiveand specific, ultrasound has the advantage ofbeing less expensive, widely available, and easyto perform.

Knowledge about the utility of magnetic resonanceimaging (MRI) in abdominal tuberculosis is verylimited. MRI when compared to CT added noadditional information33.

Endoscopy may be useful in cases of GItuberculosis where lesions are accessible.Endoscopic appearances in tuberculosis includehyperaemic nodular friable mucosa, irregularulcers with sharply defined margins andundermined edges, and pseudopolyps. These maymimic inflammatory bowel disease andmalignancy. Endoscopic biopsy may not revealgranulomas in all cases, as the lesions aresubmucosal34. Biopsies from the edges and thebase of the ulcer or multiple biopsies from thesame site may increase the yield. Endoscopicbiopsy specimens may be subjected to polymerasechain reaction for detection of AFB35.

In peritoneal tuberculosis, laparoscopicappearances of thickened peritoneum alongwithwhitish to yellowish miliary tubercles studded overthe peritoneum and other viscera have been foundto be more helpful in diagnosis of tuberculosisthan either histological or bacteriologicalexamination36.

Reports have described a number of patients inwhom tuberculosis could not be diagnosedduring l i fe but was revealed only atnecropsy37,38. This occurs mostly when there aresmall intestinal strictures which are notamenable to endoscopic biopsies or adhesiveperi toneal lesions where ascit ic tap orlaparoscopic biopsy cannot be performed.Therapeutic trial of antitubercular treatment

(ATT) is recommended by some authors insuspected cases of abdominal tuberculosis,when diagnosis cannot be proven. However,sometimes it may lead to a delay in diagnosisand treatment of conditions like malignancy,lymphoma, and Crohn’s disease which canmimic tuberculosis clinically and radiologically.Recurrence of obstructive symptoms requiringsurgery has been observed in some patients whowere put on ATT for obstructive symptoms20. Incircumstances where clinical suspicion is strong,but results of investigations are equivocal, adiagnostic laparatomy may be a safer option.This may allow concurrent treatment of intestinallesions. The imaging has proven to be a veryuseful modality for diagnosis of extra-intestinaldisease. Where clinical suspicion is strong andimaging features are suggestive, a therapeutictrial of ATT may be justified.

However, laparotomy is definitely indicatedwhere malignancy cannot be ruled out withcertainty. In many patients, it may not bepossible to rule out malignancy even atlaparotomy. A frozen section examination mayhelp in such cases. A mesenteric lymph nodeshould always be removed in such cases ascaseation and granulomas are much more likelyto be present in lymph nodes than intestinallesions4,20.

Management All patients with abdominaltuberculosis should be given standard full courseof ATT. Conventional regimens suggest ATT for12 to 18 months39. However, the use of shortcourse regimens for 6-9 months have been foundto be equally effective40. Patients with peritoneal,nodal, or ulcerative intestinal disease are usuallytreated with drugs (ATT). Some authors haverecommended the addition of corticosteroids inpatients with peritoneal disease in order to reducesubsequent complications of adhesions41. Nocontrolled studies have been performed to showtheir benefit. Patients with intestinal obstruction dueto strictures and hypertrophic lesions requiresurgical treatment42. However, some reports haveshown successful treatment of obstructing intestinal

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lesions with ATT alone40,43.

Though patients usually report improvement insystemic symptoms in few weeks, relief of intestinalsymptoms may require a much longer duration.A number of patients with abdominal tuberculosiswho present with acute abdomen requireemergency surgical intervention44. Subacuteintestinal obstruction or acute-on-chronicobstruction responds usually to conservativemanagement and patients can be investigatedlater and managed electively.

The surgical procedures recommended presentlyfor the management of intestinal tuberculosis arelargely conservative, as it is a systemic disease. Anumber of surgical procedures are recommendeddepending upon the type and extent of intestinallesions45. A description of these is beyond the scopeof this article. Despite being a treatable disease,abdominal tuberculosis carries a mortality of 4-12% which is largely due to associated problemsof malnutrition, anaemia, and hypoalbuminaemiaand due to acute complications. A high clinicalindex of suspicion and judicious use of diagnosticprocedures can certainly help in timely diagnosisand treatment and thus reduce the mortality ofthis curable but potentially lethal disease46.

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