Spectrum of High-Resolution Sonographic Features of Urinary Tuberculosis
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1 Article Spectrum of High-Resolution Sonographic Features of Urinary Tuberculosis S. Boopathy Vijayaraghavan, MD, DMRD, Sangampalayam V. Kandasamy, MS, MCh, Mylsamy Arul, MS, DNB, Muniappan Prabhakar, MS, Chokkalingu L. Dhinakaran, MS, MCh, Ramasamy Palanisamy, MS, MCh Objective. To evaluate the high-resolution sonographic features of urinary tuberculosis. Methods. During a period of about 3 years 6 months, there were 45 patients with sonographic features of urinary tuberculosis that was subsequently proved by urine culture or biopsy. The clinical symptoms, urinalysis findings, sonographic features, urine smear findings, and biopsy findings were recorded. Results. The most common symptoms were dysuria and frequency of micturition. Sonographic features included parenchymal masses, cavities, mucosal thickening of the collecting system and urinary bladder, stenosis of the collecting system, a contracted urinary bladder, vesicoureteric reflux, and calcifications. The proof of tuberculosis was by urinalysis, culture, and biopsy. Conclusions. High-resolution sonography in appropriate clinical situations is useful in diagnosis of urinary tuberculosis. The various high-resolution sonographic findings in urinary tuberculosis are illustrated. The distinguishing features are visualization of involvement of multiple sites and multiple stages of disease in the same patient. Key words: calcification; cavity; mass; mucosal thickening; sonography; stenosis; urinary tuberculosis. Abbreviations IVU, intravenous urography Received November 19, 2003, from Sonoscan Ultrasonic Scan Centre (S.B.V.), Vedhanayagam Hospital Private Ltd (S.V.K., M.A., M.P.), Kumaran Hospital (C.L.D.), and Sri Ramakrishna Hospital (R.P.), Coimbatore, India. Revision requested December 17, Revised manuscript accepted for publication December 31, We thank Srambical Sreedharan, EDP, for technical assistance and Padma Ramesh for secretarial assistance in the preparation of this manuscript. Address correspondence and reprint requests to S. Boopathy Vijayaraghavan, MD, DMRD, 16 B Venkatachalam Rd, R. S. Puram, Coimbatore , India. sonoscan@vsnl.com and sboopathy@eth.net. Urinary tuberculosis is an insidious disease in which the diagnosis can be difficult and delayed. Despite the frequency with which tuberculosis involves the urinary tract, the sonographic features of the condition have been described infrequently. In this article, we illustrate the high-resolution sonographic features of various abnormalities of the urinary system caused by tuberculosis. Materials and Methods Between May 2000 and October 2003, there were 45 patients with sonographic features suggestive of urinary tuberculosis that was proved subsequently. The patients symptoms were recorded. Routine urinalysis was available for all the patients. Sonography was performed initially with an HDI 3500 scanner and later with an HDI 5000 Scanner (Philips Medical Systems, Bothell, WA) using convex 2- to 5-MHz, convex 4- to 7-MHz, and linear 5- to 12-MHz probes. Intravenous urography (IVU) 2004 by the American Institute of Ultrasound in Medicine J Ultrasound Med 23: , /04/$3.50
2 High-Resolution Sonographic Features of Urinary Tuberculosis followed sonography in 34 patients. Urine smears and cultures for tuberculosis were done in 30 patients. Twenty patients underwent cystoscopy and cystoscopic biopsy. Results Of the 45 patients, 29 (64%) were male and 16 (36%) were female. The ages of the patients ranged from 24 to 61 years. Dysuria and frequency of micturition were the most common symptoms (Table 1). Urinalysis showed abnormal numbers of pus cells in 40 patients (89%) and microscopic hematuria in 13 patients (29%). Abnormalities of the kidney and its collecting system were bilateral in 15 patients (33%), in the right kidney alone in 11 (24%), and in the left kidney alone in 15 (33%). The urinary bladder alone was abnormal in 4 patients (9%). Table 2 summarizes the sonographic findings. Renal parenchymal granulomas were seen as masses of mixed echogenicity in 5 patients (11%), cavitating masses in 3 (7%), and masses with calcifications in 2 (4%). Renal parenchymal cavities were seen in 16 patients (35%). Renal parenchymal scars were seen in 3 patients (7%), and scars with calcifications were seen in 2 (4%). Mucosal thickening of the collecting system was seen in 16 patients (36%), involving the calyces, pelvis, or both in 7 (15%) and the ureter in 9 (20%). Calyceal stenosis was seen in 13 patients (29%), stricture of the pelviureteric junction in 2 (4%), and ureteric stricture in 8 (18%). Irregular mucosal thickening of the urinary bladder was seen in 28 patients (62%). The capacity of the urinary bladder was reduced in 20 patients (44%). There were hypoechoic areas in the liver in 1 patient (2%), and enlarged lymph nodes Table 1. Symptoms of Patients With Urinary Tuberculosis (n = 45) Symptom No. of Patients % Dysuria Frequency of micturition Hematuria Loin pain 5 11 Fever 3 7 Lower abdominal pain 2 4 Urinary incontinence 2 4 Loss of appetite 2 4 Abdominal distension 1 2 Secondary amenorrhea 1 2 were seen in 2 (4%). One patient each had features of peritoneal tuberculosis and pleural fluid. Intravenous urography was done after sonography in 34 patients. It confirmed the sonographic features in 22. In 12 patients, there was poor or no visualization of the kidney and its collecting system on the side of the sonographic findings. Intravenous urography could not be done in 7 patients because they were in renal failure. The diagnosis of urinary tuberculosis was confirmed by urine culture, cystoscopic biopsy, or both in 40 patients. In the remaining 5 patients, the diagnosis was confirmed in the following ways. The right kidney of 1 patient showed parenchymal cavities, calyceal stenosis, and mucosal thickening of the ureter with hydronephrosis. The urinary bladder was normal on sonography and cystoscopy. Retrograde pyelography confirmed the sonographic findings. The analysis of a urine sample taken from the renal pelvis was positive for Mycobacterium tuberculosis. The earlier urine sample and the urine from the renal pelvis both grew M tuberculosis on culture. Cystoscopy showed cystitis in 1 patient with sonographic features of mucosal thickening and a reduced capacity of the urinary bladder and negative urinalysis and culture results, but the biopsy results were reported as follicular cystitis on 2 occasions. The patient was treated with antituberculous drugs and was Table 2. Sonographic Findings in Urinary Tuberculosis (n = 45) Sonographic Findings No. of Patients % Parenchymal mass Parenchymal cavity Parenchymal scar 5 11 Parenchymal calcification 4 9 Decrease in size of the kidney 2 4 Renal and perinephric abscess 1 2 Mucosal thickening of calyx, 7 15 pelvis, or both Mucosal thickening of ureter 9 20 Calyceal stenosis Pelviureteric junction stenosis 2 4 Ureteric stricture 8 18 Hydronephrosis Calcification of collecting system 5 11 Urinary bladder mucosal thickening Urinary bladder capacity reduced Enlarged lymph nodes 2 4 Hypoechoic areas in liver 1 2 Ascites 1 2 Pleural fluid J Ultrasound Med 23: , 2004
3 Vijayaraghavan et al relieved of the symptoms. On sonography, the mucosal thickening of the urinary bladder was found to have resolved, and the bladder capacity had come back to normal. In 1 patient, confirmation was by fine-needle aspiration cytologic analysis of an enlarged lymph node. Sonography revealed a renal and perinephric abscess in a patient with fever and flank pain. Percutaneous drainage of the abscess was done. The wound did not heal, and sonography showed a fistulous tract with small perinephric exudate. The discharge was negative for M tuberculosis. The patient was treated with antituberculous drugs. The wound healed, and sonography revealed a normal kidney. One patient in this series had undergone surgery 2 weeks before for a nonhealing discharging sinus of the scrotum, and the epididymal biopsy showed tuberculosis. He subsequently had dysuria and loin pain, and sonography revealed features of urinary tuberculosis. Only 2 patients had features of pulmonary tuberculosis on radiography of the chest. Discussion The role of imaging studies in urinary tuberculosis has been to assess the extent of involvement, to monitor the effect of treatment, and to discover complications. Early findings are best detected on IVU or retrograde pyelography. Late or chronic changes are optimally evaluated with computed tomography and sonography. They are also extremely valuable in evaluation of areas of mass effect and the nonvisualized kidney at IVU. 1 Recently, however, sonography has been performed more often because it is more easily available and is economical. Another reason is that it is performed as the first investigation to look for lower urinary tract calculi, which produce symptoms similar to those of urinary tuberculosis. This is more so in developing countries such as India. To our knowledge, however, the sonographic features of urinary tuberculosis have been described infrequently. 2 5 Urogenital tuberculosis accounts for approximately 30% of cases of extrapulmonary tuberculosis. 1 Renal tuberculosis progresses in 2 steps: (1) initial seeding and (2) reactivation. Diffuse hematogenous dissemination occurs at the time of initial pulmonary infection in approximately 25% of cases. 1,6 The bacilli are trapped in the periglomerular capillaries and cause formation of numerous small abscesses in both kidneys. These cortical lesions are too small to be imaged. 7,8 If the cellular immunity of the host is intact, or if antituberculous chemotherapy has been administered for clinically active primary tuberculosis, the organisms stay confined to the cortex with the subsequent formation of multiple small healed granulomas. If host immunity is impaired, reactivation may occur between 5 and 25 years after the initial pulmonary infection. 1 Initial cortical foci reactivate and spill organisms into the renal tubules, and these propagate to the papillae through the loop of Henle. 9 In the renal medulla, bacillary proliferation leads to formation of granulomas, caseation, and cavitation. Massive destruction may produce coalescent granulomas, which produce a mass lesion if they fail to rupture into a calyx. This is seen on sonography as masses of variable size and echogenicity. 2 5 These lesions are better visualized by the high-resolution sonography available now. They are seen as masses of mixed echogenicity in the renal parenchyma, with or without necrotic areas of caseation (Figures 1 and 2). A new appearance seen in this series was a mass of mixed echogenicity with multiple punctate calcifications (Figure 3). Caseation and cavitation occurs in the mass, resulting in parenchymal cavities seen on sonography (Figures 4 6). None of these parenchymal lesions are seen on IVU. When papillary lesions affect the calyx, the resulting mucosal edema is seen as a slight loss of sharpness of the calyceal margin on IVU, described as a fuzzy or feathery calyx. On high-resolution sonography, this is seen as a medullary cavity close to the calyx, distorting it (Figure 4). More commonly, this papillary lesion ruptures into the calyceal system and is seen as a cavity communicating by an anechoic tract with the calyx (Figure 5A). 5 When there is marked destruction of the papilla, the resulting cavity is seen in continuity with the calyx with a broad communication (Figure 5B). Sometimes the sloughed necrosed papilla is seen (Figure 7). The parenchymal cavity can extend outward and can rupture, producing a perinephric abscess (Figure 8) and later a fistula to skin. 1 The disease then spreads distally by seeding through the urothelial submucosa and lymphatic vessels to the infundibula, renal pelvis, ureter, and urinary bladder. The urothelium J Ultrasound Med 23: ,
4 High-Resolution Sonographic Features of Urinary Tuberculosis A B Figure 1. High-resolution sonograms of the kidney showing a parenchymal mass (arrows) of mixed echogenicity (A) and a mass (arrows) with an area of caseation and cavitation (B). becomes inflamed, edematous, and ulcerated with multiple tiny granulomas in the mucosa and submucosa. The areas most severely affected are sites of anatomic narrowing, such as the infundibula of the calyces, the pelviureteric junction, and the ureterovesical junction. 1,6,10 To our knowledge, sonography at this stage of disease of the collecting system has not been reported so far. With high-resolution sonography, these changes are visible. They are seen as varying degrees of irregular mucosal thickening in calyces, the pelvis (Figures 6, 9, and 10), and the ureter. On IVU, a ragged irregular appearance of the ureter with proximal dilatation is the first sign of ureteric tuberculosis. 1 This early and potentially reversible dilatation has been attributed to spasms or mucosal edema. 11 If multiple sites of the ureter are involved, the ureter has a beaded appearance on IVU. The same changes are seen on high-resolution sonography as mucosal thickening of the ureter with proximal dilatation (Figure 11) and a beaded appearance (Figure 12). In the urinary bladder, initial changes are seen as cystitis with ulceration, inflammation, and edema of the mucosa. With generalized involvement, the bladder capacity is reduced. Figure 2. High-resolution sonogram of the kidney showing a large irregular parenchymal cavity (C) within a hypoechoic mass (arrows). 588 J Ultrasound Med 23: , 2004
5 Vijayaraghavan et al A B Figure 3. Sagittal scan (A) and high-resolution sonogram (B) of the kidney showing parenchymal masses with calcifications in them. Renal tuberculosis is characterized pathologically by 2 basic processes: (1) destruction and (2) healing by fibrosis, granuloma formation, and calcification. 1,10 In the kidney, this results in scars of parenchyma with or without calcification. The fibrous scarring of the collecting system usually involves the sites of anatomic narrowing. Narrowing of the infundibulum of the calyx produces focal caliectasis. If multiple calyces are involved, the characteristic feature seen is uneven or asymmetric caliectasis, which means that some calyces are grossly dilated, some are slightly dilated, and some are not dilated. If all the calyces are involved, there is asymmetric or symmetric dilatation of all the calyces without renal pelvis dilatation (Figure 13). The fibrosis of the infundibulum and pelvis results in retraction of some part of the kidney and dilatation of the other part, resulting in kinking and distortion of the renal pelvis (Figure 14). 11,12 Fibrotic healing of the pelviureteric junction results in hydronephrosis (Figure 10) or pyonephrosis (Figure 15). In the ureter, fibrosis leads to single or multiple strictures with hydronephrosis. In the lower ureter, it can result in a straight, rigid tube with a patulous ureteric orifice and vesicoureteric reflux (Figure 16). 9,11 When there is dilatation of the collecting system, either a part or the whole of the collecting system may not be visualized on IVU, rendering it impossible to be studied. Nevertheless, it can be studied well on sonography. In the urinary bladder, mucosal tubercles coalesce and produce ulceration and edema, seen on sonography as irregular areas of mucosal thickening (Figure 17). Edema of the trigonal mucosa can cause ureteral obstruction (Figure 18). Extensive involvement of bladder mucosa results in a potentially reversible decrease in the capacity of the urinary bladder, most probably due to spasms. The inflammation progresses to involve the muscular layer, and mural fibrosis causes the bladder to become markedly thick- Figure 4. High-resolution sonogram of the kidney showing the lower pole calyx (CX) and a large medullary cavity (C) distorting the calyx. J Ultrasound Med 23: ,
6 High-Resolution Sonographic Features of Urinary Tuberculosis A B Figure 5. High-resolution sonograms of the kidney showing an irregular medullary cavity (C) communicating by an anechoic tract (arrow) with the calyx (A) and multiple large parenchymal cavities (C), 1 having a broad communication with the calyx (CX; B). ened and contracted. Fibrosis in the region of the trigone may produce gaping of a ureteric orifice and vesicoureteric reflux (Figure 16). 9,11 Calcification of the lesions occurs as part of healing. In the renal parenchyma, this is seen as clumps of punctate calcification (Figure 3) or a lobar type of calcification deep to a scar. In the collecting system, when focal, it is seen as speckled or curvilinear calcifications in the wall of the calyx (Figure 6), pelvis (Figure 19), and ureter. When large, they produce a cast of most of or the entire kidney. 1,6,13 Figure 7. High-resolution sonogram of the kidney showing a sloughed necrosed papilla (P) in the calyx. Figure 6. High-resolution transverse sonogram of the kidney showing mucosal thickening (arrows) of calyces and the pelvis (P). There are calcifications of the wall of the calyx and pelvis (arrowheads). A parenchymal cavity (C) is also shown. 590 J Ultrasound Med 23: , 2004
7 Vijayaraghavan et al Thus, sonography can visualize a myriad of conditions caused by urinary tuberculosis, and each of these can be caused by other disease processes, such as other forms of papillary necrosis, malignant lesions of the kidney and collecting system, and bacterial cystitis. The major distinguishing feature of urinary tuberculosis on sonography is involvement of multiple areas of the urinary tract and visualization of different stages of the disease in the same patient. Even though IVU has been the chosen imaging modality in urinary tuberculosis, it fails to show the parenchymal masses of granulomas, and it is not helpful when the kidney and the collecting system are not visualized or are poorly visualized. This may be the result of extensive cavities of ulcerocavernous tuberculosis 1 or obstruction due to stenosis of various areas of the collecting system. Intravenous urography is also not useful in patients with renal failure. In this series, IVU failed to reveal lesions for the above reasons in 12 of 34 patients in whom it was done. It could not be done in 7 because of renal failure. In conclusion, the spectrum of sonographic features of urinary tuberculosis is described here, with emphasis on the mucosal changes seen on high-resolution sonography. Figure 9. A and B, Coronal (A) and transverse (B) scans of the kidney showing mucosal thickening in the calyces and pelvis. C, High-resolution sonogram from the same patient. A B C Figure 8. Coronal scan of the kidney showing a renal and perinephric abscess. J Ultrasound Med 23: ,
8 High-Resolution Sonographic Features of Urinary Tuberculosis Figure 10. Coronal scan showing hydronephrosis due to stenosis of the pelviureteric junction. Mucosal thickening of calyces and the pelvis is also shown. Figure 13. Coronal scan of the kidney showing dilatation of all the calyces without renal pelvic dilatation. Figure 11. High-resolution sonogram of the mid ureter showing marked mucosal thickening (arrow) of the ureter obliterating the lumen with a dilated proximal ureter (UR). Figure 14. Coronal scan of the kidney showing distortion and kinking of the renal pelvis due to fibrosis. Figure 12. High-resolution sonogram of the mid ureter showing a beaded appearance due to multiple segments of marked mucosal thickening. Figure 15. Transverse scan of the kidney showing pyonephrosis with debris in dilated calyces. 592 J Ultrasound Med 23: , 2004
9 Vijayaraghavan et al Figure 16. Color Doppler sonogram of the ureter showing vesicoureteric reflux. Figure 18. Oblique scan of the urinary bladder and ureter showing mucosal thickening of the trigone area (arrow) and distal ureter (UR) with a dilated proximal ureter. A Figure 19. Transverse scan of a grossly hydronephrotic kidney showing extensive calcification (CX) of the wall of the renal pelvis (P). B Figure 17. Transverse scans of the urinary bladder showing focal irregular mucosal thickening in the region of the trigone (A) and anterior wall (B). J Ultrasound Med 23: ,
10 High-Resolution Sonographic Features of Urinary Tuberculosis References 1. Kim SH. Urogenital tuberculosis. In: Pollack HM, McClennan BL (eds). Clinical Urography. 2nd ed. Philadelphia, PA: WB Saunders Co; 2000: Premkumar A, Lettimer J, Newhouse JH. CT and sonography of advanced urinary tract tuberculosis. AJR Am J Roentgenol 1987; 148: Das KM, Vaidyanathan S, Rajwanshi A, et al. Renal tuberculosis: diagnosis with sonographically guided aspiration cytology. AJR Am J Roentgenol 1992; 158: Schaffer R, Becker JA, Goodman J. Sonography of tuberculous kidney. Urology 1983; 22: Das KM, Indudhara R, Vaidyanathan S. Sonographic features of genitourinary tuberculosis. AJR Am J Roentgenol 1992; 158: Cohen MS. Granulomatous nephritis. Urol Clin North Am 1986; 13: Kim SH, Kim SH, Kim WH. Imaging makes progress in urinary tract tuberculosis. Diagn Imaging Asia Pac 1995; 2: Goldman SM, Fishman EK, Hartman DS, Kim YC, Siegelman SS. Computed tomography of renal tuberculosis and its pathological correlates. J Comput Assist Tomogr 1985; 9: Tonkin AK, Witten DM. Genitourinary tuberculosis. Semin Roentgenol 1979; 14: Eastwood JB, Dilly SA, Grange JM. Renal mycobacterial diseases. In: Massry SG, Glassock RJ (eds). Massry and Glassock s Textbook of Nephrology. 4th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2001: Elkin M. Urogenital tuberculosis. In: Pollack HM (ed). Clinical Urography. Philadelphia, PA: WB Saunders Co; 1990: Barrie HJ, Kerr WK, Gale GL. The incidence of tuberculous strictures of the renal pelvis. J Urol 1967; 98: Gow JG. Renal calcification in genitourinary tuberculosis. Br J Surg 1965; 52: J Ultrasound Med 23: , 2004
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