sonographic appearances in abdominal tuberculosis

Pictorial Essay

Sonographic Appearances inAbdominal Tuberculosis

Arun Batra, MD, DNB, Manpreet Singh Gulati, MD, DNB, Dipanka Sarma, MD,Shashi Bala Paul, MBBS

Department of Radiodiagnosis, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110 029, India

Received 19 October 1999; accepted 8 February 2000

A bdominal tuberculosis can be a diagnosticchallenge even for experienced physicians

because patients with the disease usually presentwith nonspecific signs and symptoms. The diseaseis endemic in most developing countries, and itsincidence in western countries has risen becauseof the increased incidence of the Acquired immu-nodeficiency syndrome (AIDS).1 Sonography candetect findings in individuals with early-stagedisease; can delineate lesions of the bowel, peri-toneum, lymph nodes, and solid organs; and canhelp to identify targets for biopsies. Sonography isalso inexpensive and readily available in areas ofthe world where abdominal tuberculosis is mostprevalent.

Abdominal tuberculosis can mimic conditionsas varied as lymphoma, Crohn’s disease, amebia-sis, and adenocarcinoma. Imaging features arenot pathognomonic but can readily suggest thediagnosis when considered along with the clinicalpresentation, immune status, and demographicbackground of the patient.

The purpose of this pictorial essay is to discussthe sonographic findings in tuberculosis of thegastrointestinal tract, peritoneum, lymphatic sys-tem, hepatobiliary system, and spleen. A spec-trum of sonographic appearances selected from aretrospective review of the records of 100 immu-nocompetent patients with tuberculosis (Table 1)is shown. This review does not include patientswith AIDS or genitourinary tuberculosis.

TECHNIQUE

Sonography can usually demonstrate all of thefeatures of abdominal tuberculosis because thepatients tend to be emaciated, which provides agood acoustic window for a thorough examination.The use of a 5–7.5-MHz linear-array transducer isparticularly effective for evaluating the perito-neum, omentum, and mesentery. Graded com-pression sonography is the most effective tech-

Correspondence to: M. S. Gulati, B-3/185 Janak Puri, NewDelhi 110 058, India

© 2000 John Wiley & Sons, Inc.

TABLE 1

Sonographic Findings in 100 Patients with

Abdominal Tuberculosis

Site of Disease/Finding % of Patients

Peritoneum 65Mesenteric disease 60Ascites 20Peritoneal thickening 12Omental involvement 18

Lymph nodes 62Mesenteric node involvement 52Retroperitoneal node involvement 4Periportal node involvement 6

Gastrointestinal tract 32Ileocecal disease* 18Small bowel disease† 12Colonic disease 1Gastric disease 0Duodenal disease 2

Viscera 16Splenic disease 8Liver disease 1Gallbladder disease 1Pancreatic disease 1Adrenal gland disease 2

Psoas muscle involvement 3

*Includes involvement of the terminal ileum, the cecum, and theadjoining portion of the ascending colon.

†Isolated transverse-colon involvement.

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nique for evaluating the mesentery. With gradualand varying degrees of compression by the trans-ducer, the bowel loops—particularly when dilatedand filled with air because of a distal obstruc-tion—can be displaced from the region of interest.The limited field of view provided by the high-

frequency transducers can be compensated for tosome extent by juxtaposing 2 images of adjacentareas in the dual-screen mode and printing a hardcopy of the combined images. The recently intro-duced extended field-of-view technology is an ef-fective alternative.

FIGURE 1. Ileocecal tuberculosis in a 17-year-old girl. Oblique sagittal sonogram obtained using a 3.5-MHzcurvilinear-array transducer (A) and high-resolution, oblique sagittal sonograms obtained using a 7.5-MHzlinear-array transducer (B) of the right iliac fossa show circumferential wall thickening of the contracted cecumand ascending colon (open arrows). The adjacent terminal ileum (arrows) shows mild thickening of its wall.(A) The ileocecal junction and medial wall demonstrate greater thickening (arrowheads). (B) The high-resolution images show small, round mesenteric lymph nodes (long arrow) around the thickened bowel andadjacent echogenic omental thickening. The terminal ileum, which is air-filled on the low-frequency sonogram(A), appears collapsed on the high-resolution sonograms (B) because of graded compression sonography.

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234 JOURNAL OF CLINICAL ULTRASOUND

PATHOGENESIS AND PATHOLOGY

The causative organism for abdominal tuberculo-sis is usually Mycobacterium tuberculosis or My-cobacterium avium-intracellulare, the latter ofwhich is more common in immunocompromisedhosts. Abdominal tuberculosis is usually causedby ingestion of bacilli in infected sputum or con-taminated food. The bacilli incite formation of epi-thelioid granulomas and caseous necrosis in thebowel wall. The most common form of the diseaseis the ulcerative type, which results from ulcer-ation of overlying mucosa. A second form is thehyperplastic type, which features florid bowel-wall thickening. A combination of these 2 typesresults in the ulceroproliferative type. Localspread of abdominal tuberculous to the mesenter-ic nodes may lead to rupture of the nodes into theperitoneum, causing tuberculosis peritonitis. Vis-ceral involvement usually occurs by hematoge-nous spread of infection.

GASTROINTESTINAL TUBERCULOSIS

Gastrointestinal tuberculosis may be the ulcer-ative type, hyperplastic type, or a combination ofthe 2. The features of the combination type arewell demonstrated on sonography. Gastrointesti-nal tuberculosis most frequently occurs in the il-eocecal junction; other sites in which the diseaseoccurs are, in descending order of frequency, theileum, cecum, ascending colon, jejunum, otherparts of the colon, rectum, duodenum, and stom-ach.2 Sonography shows extramucosal changesdirectly and can occasionally detect mucosalchanges.

Ileocecal tuberculosis is often hyperplastic, andthe gross morphology is well evaluated with so-nography.3 In early-stage disease, a few regionalnodes and circumferential thickening of the wallof the cecum and terminal ileum (normal thick-ness of wall of small and large bowel is 3 mm4)may be sonographically visualized. In later stagesof disease, the ileocecal valve and adjacent medialwall of the cecum are predominantly and asym-metrically thickened (Figure 1). These changesare, however, nonspecific and may also be seen incecal adenocarcinoma, Crohn’s disease, lym-phoma, and amebiasis. In advanced ileocecal tu-berculosis, gross wall thickening, adherent loops,large regional nodes, and mesenteric thickeningmay together form a complex mass of varied echo-genicity centered on the ileocecal junction (Figure2). These features are highly suggestive of tuber-culosis in the appropriate clinical setting.5

Mucosal changes that occur in early stages of

tuberculous enteritis are not usually sonographi-cally visible. However, deep ulcerations occasion-ally can be detected and appear as radial exten-sions of the echogenic luminal contents into thesurrounding thickened wall (Figure 3A). As thedisease progresses, wall thickening and short-segment strictures develop in the intestine, re-sulting in partial intestinal obstruction and occa-sionally in intestinal perforation and abscessformation. On transverse sonograms, areas ofnarrowing representing strictures appear as seg-ments of circumferential mural thickening andreduced luminal content (Figure 3B). Real-timesonography helps to assess hyperperistalsisproximal to an obstructing lesion. Long-standingobstruction leads to the formation of enteroliths,which may occasionally be sonographically de-tected (Figure 4). Enteroliths are rare in the pre-sent era, probably because of early management.Intussusception induced by mural lesions canalso be sonographically detected, especially inchildren (Figure 5).

Colonic tuberculosis may also be sonographi-cally evaluated. Although it can occur indepen-dently, colonic tuberculosis is usually contiguouswith ileocecal tuberculosis. The extent of involve-ment (ie, whether the disease involves a long orshort colonic segment) is better evaluated on real-time sonography and may be difficult to docu-ment. Short-segment involvement is seen moreoften around the hepatic flexure than in other ar-eas of the colon.

FIGURE 2. Abdominal tuberculosis in a 19-year-old woman withsymptoms of recurrent partial intestinal obstruction. Transversesonogram of the right iliac fossa reveals a complex heterogeneousmass consisting of matted bowel (short black arrow), thickened echo-genic mesentery (curved white arrow) with enlarged lymph nodes(long arrow), and surrounding loculated ascites with septa (curvedblack arrow).

ABDOMINAL TUBERCULOSIS

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Duodenal tuberculosis is uncommon.2 Tuber-culous duodenal obstruction usually results fromextrinsic compression of the third part of the du-odenum by lymph nodes in the superior mesen-teric region. Sonograms of the third part of theduodenum may show hypoechoic centers and helpestablish a diagnosis. Intrinsic involvement of theduodenum (Figure 6) is less common than is duo-denal obstruction by extrinsic nodes and may beulcerative or hyperplastic.

Gastric tuberculosis is very rare and usuallydifficult to diagnose. Antral narrowing occursusually secondary to ulceration and fibrosis but issometimes due to surrounding caseous lymphade-

nopathy. Sonography shows concentric muralthickening [normal thickness of stomach is 5 ± 1mm (standard deviation)6] with surroundinglymph nodes, both of which are visualized bestwhen the patient has a fluid-filled stomach. Mu-cosal involvement may also be sonographicallydetected when the patient’s stomach is fluid-filled.

PERITONEAL TUBERCULOSIS

Peritoneal tuberculosis is the most common formof abdominal tuberculosis and involves—alone orin combination—the peritoneal cavity, mesen-

FIGURE 3. Subacute intestinal obstruction due to tuberculous small-bowel stricture in a 25-year-old woman.(A) Oblique sonograms of the left lower quadrant obtained using a 7.5-MHz linear-array transducer reveal along, circumferential thickening of the jejunum with adjacent involved nodes (arrowhead). Radial extension ofthe echogenic luminal contents into the thickened wall (arrow) represent ulcerations, confirmed on a bariumx-ray study. (B) Transverse sonogram through the stricture shows the thickened wall with a narrow lumen andan adjacent mesenteric lymph node (arrowhead).

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FIGURE 4. Long-standing recurrent partial intestinal obstruction dueto tuberculosis in a 48-year-old woman. Oblique sagittal sonogram ofthe lower abdomen reveals a markedly dilated ileal loop (arrowheads)containing a large intraluminal structure (curved arrows) with distalshadowing. At surgery, a 3-cm, oval enterolith was found proximal toa tight ileal stricture.

FIGURE 5. Intussusception in a 9-year-old child with intestinal tuber-culosis. Transverse sonogram through the right lower abdomenshows the intussusception with the echogenic mesenteric fat inter-posed between the concentric bowel loops.

FIGURE 6. Duodenal tuberculosis in a 22-year-old woman presentingwith recurrent episodes of abdominal pain, vomiting, and weight lossfor 5 months. Transverse sonogram of the epigastric region revealsgross thickening of the duodenal wall (arrows), seen anterolateral tothe head of the pancreas (arrowheads).

FIGURE 7. Tuberculous ascites in a 45-year-old man with weight loss,fever, and abdominal distention. High-resolution sagittal sonogramof the pelvic region using a 7.5-MHz linear-array transducer demon-strates multiple thin, incomplete septa and low-level internal echoes.The debris and fine septa appeared on real-time sonography to befloating. These features are best seen on sonograms and are not seenon CT scans.

tery, and omentum. Classically, 3 types of perito-neal tuberculosis are described: wet, dry, and fi-brotic-fixed.7 The wet type manifests as free orloculated ascites; the dry type with mesentericthickening, lymphadenopathy, and fibrous adhe-sions creating a “plastic abdomen”; and the fi-brotic-fixed type with omental thickening andmatted bowel loops, which may be clinically in-terpreted as a mass.

Sonography may demonstrate free, loculated,

or focal ascites.5 Free ascitic fluid is commonlyseen; on sonograms, it may be anechoic or containdebris. Lacy strands or fine septa and low-levelinternal echoes within the ascitic fluid are char-acteristic of exudative ascites (Figure 7). Locu-lated ascites appears on sonograms as an en-cysted collection of fluid with thin, interlacingseptations. Focal ascites is an interloop fluid col-lection that appears on sonograms as the “club-sandwich” sign.8 This results from alternating

FIGURE 8. Peritoneal tuberculosis in an 18-year-old woman. (A) Sagittal sonogram of the pelvis revealsexudative ascites in the pouch of Douglas seen as a fluid collection (COLL) with internal echoes and associatedperitoneal thickening (arrow) best appreciated along the outer surface of the urinary bladder (UB). (B) Trans-verse sonograms obtained with a 7.5-MHz linear-array transducer reveal diffuse thickening of the peritoneum(arrowheads) with focal areas of nodularity (thick arrow) beneath the anterior abdominal wall. The underlyinggreater omentum is thickened and is predominantly echogenic with a hypoechoic nodule (long thin arrow)within it.

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hyperechoic and hypoechoic layers of the serosaand bowel wall of 2 adjacent loops with the inter-vening layer of anechoic fluid. Peritoneal thicken-ing appears as an irregular, sheet-like, hy-poechoic layer (Figure 8A). Thickening of theperitoneum just beneath the abdominal wall canbest be appreciated with a high-frequency linear-array transducer (Figure 8B).

Mesenteric disease is an important and com-mon manifestation of early-stage abdominal tu-berculosis.9 The mesentery is initially thickenedand echogenic9 with a few discrete lymph nodesinterspersed within it. In later-stage mesenterictuberculosis, irregular hypoechoic areas repre-senting a conglomerate of caseating lymph nodesmay be sonographically visualized (Figure 9A).Focal, irregular echogenic areas of calcificationwith distal shadowing may be identified (Figure9B). Matted and fixed bowel loops arrangedaround the thickened mesentery stand out asspokes radiating from a center and form the sono-graphic “stellate” sign.5

Omental thickening associated with peritonealtuberculosis is well demonstrated on sonography.In cases of peritoneal tuberculosis, the greateromentum is thickened, has a heterogeneous echo-texture, and sometimes contains hypoechoic nod-ules (Figure 8B).

TUBERCULOSIS OF THE LYMPH NODES

Lymphadenopathy is commonly visualized sono-graphically in abdominal tuberculosis. A diagno-sis of tuberculosis can be suspected based on dis-tribution and morphology of the lymph nodes. Themesenteric (Figures 1, 2, 3, and 9), celiac, portahepatis, and peripancreatic lymph nodes arecharacteristically involved, reflecting the lym-phatic drainage of the small bowel. The retroper-itoneal lymph nodes are relatively spared,9

and, unlike in cases of lymphoma, their involve-ment rarely occurs in isolation. In disseminated

FIGURE 9. Peritoneal tuberculosis in a 25-year-old woman who presented with abdominal pain and swelling, vomiting, and a palpable, ill-definedmass in the central abdomen. (A) Transverse sonograms of the umbilical region reveal extensive hypoechoic mesenteric thickening (curved whitearrow) with multiple conglomerate lymph nodes (straight white arrow). A few discrete lymph nodes (black arrow) are also seen. (B) A transversesonogram through an adjacent region reveals an irregular focus of central calcification (arrow) with distal shadowing within the conglomeratelymph nodal mass. The mesentery is best evaluated with graded compression sonography and a high-frequency linear-array transducer.


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FIGURE 10. Disseminated tuberculosis in an 18-year-old woman presenting with prolonged fever and weightloss. (A) Transverse sonogram of the central abdomen shows multiple conglomerate, hypoechoic mesentericlymph nodes adjacent to the bowel. (B) Transverse sonogram of the suprarenal regions reveals bilateralhypoechoic adrenal masses (curved arrow, calipers indicate mass on right side) and multiple retroperitoneal(paracaval) nodes on the right side. A lymph node at the porta hepatis region shows calcification (long arrow).A sonographically guided biopsy of the right adrenal mass confirmed tuberculosis.


tuberculosis, however, diffuse lymphadenopathywithout a predilection for any site may be seen(Figure 10). The involved lymph nodes are usu-ally matted together with hypoechoic centers andoccasionally contain calcification.

HEPATOBILIARY ANDSPLENIC TUBERCULOSIS

Tuberculosis of the liver or spleen is rarely seen inisolation and is more frequently part of multifocalor disseminated disease. Involvement of the liveror spleen can occur in the form of microabscessesin a miliary tuberculosis pattern representedsonographically by a coarsened echotexture (Fig-ure 11) or in the form of larger abscesses10 orgranulomas (Figure 12). The hypoechoic rimsometimes seen surrounding the abscesses (Fig-ure 12B) may represent compressed splenic pa-renchyma. Often the only feature of visceral in-volvement is organomegaly, with calcifiedgranulomas (Figure 13) occasionally visible inlate-stage disease or after healing.

Tuberculosis of the gallbladder is very rare. So-nography may show thickening of the gallbladderwall; irregular, shaggy septa within the gallblad-der; and regional lymphadenopathy. Sonographicfeatures in tuberculosis of the gallbladder usuallycannot be differentiated from those in carcinoma(Figure 14). However, sonographic features of

mesenteric thickening and lymphadenopathyalong with the clinical presentation may preop-eratively suggest the diagnosis of tuberculosis ofthe gallbladder.

Pancreatic tuberculosis is rare but should beconsidered in cases in which the patient presentswith fever, abdominal pain, and sonographicallydetected focal pancreatic lesions. Pancreatic in-volvement may result from either hematogenousdissemination or direct spread of the disease fromadjacent nodes. Imaging features are largely non-specific. Sonography may demonstrate focal pan-creatic enlargement mimicking pancreatic carci-noma or the formation of 1 or more pancreaticabscesses (Figure 15) suggestive of an infectedpseudocyst.

CONCLUSIONS

Manifestations of abdominal tuberculosis are pro-tean, and sonography can reliably demonstrate arange of findings. Conventional barium-contraststudies detect mucosal changes better than donon–barium-contrast studies but cannot providea direct image of extramucosal disease. Therefore,sonography is ideal in defining the true extent ofdisease, assessing complications, and performingfollow-up examinations. The technique of gradedcompression and the use of high-frequency trans-ducers can help detect early and subtle features ofabdominal tuberculosis. Sonography is an inex-

FIGURE 11. Splenic involvement in a 33-year-old man who had disseminated tuberculosis and presented withunexplained fever and weight loss of recent onset. High-resolution oblique coronal sonogram of the spleenusing a 7.5-MHz linear-array transducer reveals a coarse echotexture representing miliary involvement of theparenchyma. There was no corresponding correlative finding on CT (not shown).


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FIGURE 12. Multifocal abdominal tuberculosis in a 24-year-old man who for 6 weeks had fever, anorexia, and weight loss. Physical examinationrevealed pallor, hepatosplenomegaly, and an epigastric mass. (A) Oblique coronal sonogram of the spleen reveals multiple irregular, hypoechoicfocal lesions (arrowheads) representing abscesses scattered in the parenchyma. (B) High-resolution oblique coronal sonograms of the spleen showa thin, hypoechoic halo (arrowheads) surrounding an abscess and occasional specks of marginal calcification (arrow). (C) Oblique sagittalsonogram of the liver reveals a hypoechoic focal lesion with irregular echogenic margins in the left lobe (arrows). (D) Oblique coronal sonogramof the epigastric region shows multiple hypoechoic and necrotic celiac and lesser-omental lymph nodes. Echogenic debris is seen in the dependentpart of the individual nodes (arrows).

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FIGURE 12. Continued.


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pensive and readily available imaging modality.Sonography is especially useful in developing na-tions, where it may be the only radiologic studyavailable and may help to ensure an early diag-nosis of abdominal tuberculosis. Because tubercu-losis may involve the genitourinary organs, theadrenal glands (Figure 10B), the psoas muscles(Figure 16), and the spine, these sites should alsobe carefully evaluated in cases in which abdomi-nal tuberculosis is suspected.

REFERENCES

1. MacGregor RR. Tuberculosis: from history to cur-rent management. Semin Roentgenol 1993;28:101.

2. Paustian FF, Marshal JB. Intestinal tuberculosis.In: Berk JE, editor. Gastroenterology. Philadel-phia: WB Saunders Co, 1985. p 2018.

3. Lim JH, Ko YT, Lee DH, et al. Sonography of in-flammatory bowel disease: findings and value indifferential diagnosis. AJR Am J Roentgenol 1994;163:343.

4. Pradel JA, David XR, Taourel P, et al. Sonographicassessment of the normal and abnormal bowel wallin nondiverticular ileitis and colitis. Abdom Imag-ing 1997;22:167.

FIGURE 13. Longitudinal sonogram of the spleen of a 56-year-oldwoman shows a superficially located, calcified focal lesion (arrow)suggestive of an old granuloma. These lesions are sometimes inci-dentally detected in patients who previously had tuberculosis, as inthis case.

FIGURE 14. Tuberculosis of the gallbladder in a 29-year-old man whopresented with mild pain and a palpable mass in the right upperquadrant. Oblique sagittal sonogram shows a contracted gallbladder(arrowheads) with gallstones and ill-defined, associated wall thicken-ing of the fundus of the gallbladder (open arrow). Results of a sono-graphically guided fine-needle aspiration biopsy of the fundus wereconsistent with tuberculosis.

FIGURE 15. Pancreatic tuberculous abscess in an 8-year-old child.Transverse sonogram of the pancreas reveals within the pancreas ananechoic collection of fluid (arrow) with irregular, shaggy walls. Asonographically guided fine-needle aspiration biopsy of the lesionyielded yellowish pus, which was positive for acid-fast bacilli. Follow-up sonogram obtained after 6 months of antitubercular treatmentshowed complete resolution of the abscess (not shown).

FIGURE 16. Abscess in the psoas muscle of a 32-year-old man whopresented with fever and a deformity at the left hip. Oblique sagittalsonogram of the left lower quadrant reveals a multiloculated fluidcollection (arrows) with low-level internal echoes within the psoasmuscle. Extensive mesenteric adenopathy was also seen (not shown)as evidence of abdominal tuberculosis. Sonographically guided per-cutaneous drainage, a safe and established method in the manage-ment of such lesions, was performed.

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5. Kedar RP, Shah PP, Shivde RS, et al. Sonographicfindings in gastrointestinal and peritoneal tuber-culosis. Clin Radiol 1994;49:24.

6. Rapaccini GL, Aliotta A, Pompili M, et al. Gastricwall thickness in normal and neoplastic subjects: aprospective study performed by abdominal ultra-sound. Gastrointestinal Radiology 1988;13:197.

7. Thoeni RF, Margulis AR. Gastrointestinal tuber-culosis. Semin Roentgenol 1979;14:283.

8. Ozkan K, Gurses N, Gurses N. Ultrasonic appear-

ance of tuberculous peritonitis. J Clin Ultrasound1987;15:350.

9. Jain R, Sawhney S, Bhargava DK, et al. Diagnosisof abdominal tuberculosis: sonographic findings inpatients with early disease. AJR Am J Roentgenol1995;165:1391.

10. Jain R, Sawhney G, Gupta RG, et al. Sonographicappearances and percutaneous management of pri-mary tuberculous liver abscess. J Clin Ultrasound1999;27:159.


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sonographic appearances in abdominal tuberculosis

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