Ultrasonographic diagnosis and typing of renal tuberculosis

International Journal of Urology (2008) 15, 135 139 doi: 10.1111/j.1442-2042.2007.01962.x, Original Article: Clinical Investigation Ultrasonographic diagnosis and typing of renal tuberculosis Xuefang Rui, 1 Xin-De Li, 1 SongLiang Cai, 2 Geming Chen 2 and Baisen Cai 3 1 Department of Urology, Sir Run Run Shaw Hospital, Zhejiang University Medical School, 2 Department of Urology, the First Affiliated Hospital of the Medical School of Zhejiang University, and 3 Department of B-mode Ultrasonography, the First Affiliated Hospital of the Medical School of Zhejiang University, Hangzhou, Zhejiang, China Aim: To evaluate the clinical value of sonography in the diagnosis and typing of renal tuberculosis. Methods: A total of 258 cases of renal tuberculosis with complete sonographic data were reviewed. The distinguishing features of the ultrasound images of these cases were retrospectively analyzed. Results: The coincidence rate of ultrasonography in the diagnosis of renal tuberculosis was 58.9% (152/258). According to the distinguishing features of the ultrasound images, renal tuberculosis could be classified under six types. Type I: nephrectasia type, 23 cases; type II: hydrops type, 21 cases; type III: empyema type, 13 cases; type IV: inflammatory and atrophy type, 15 cases; type V: calcification type, 34 cases; type VI: mixed type, 46 cases. Conclusion: Ultrasonographic examination has convenient, low-priced and non-invasive advantages. The typing of renal tuberculosis based on the distinguishing features of the ultrasound images provides important and reliable information for the clinical diagnosis, differential diagnosis and treatment of renal tuberculosis. Key words: diagnosis, renal tuberculosis, ultrasonography Introduction In recent decades, because of the movement of the population, the prevalence of HIV/AIDS and the transmission of the drug-resistant tuberculous strain, the incidence rate of tuberculosis is on an upward trend, especially in developing countries. The cases of renal tuberculosis have increased correspondingly. B-mode ultrasonography as an examination for the diagnosis of renal tuberculosis has been widely used for its convenience, low price and non-invasive quality. The value of B-mode ultrasonography in the diagnosis of renal tuberculosis has been reported by different authors, 1 5 with various results. Some of the authors even thought that B-mode ultrasonography failed to have practical value in the diagnosis of renal tuberculosis. We collected the clinical data of 258 inpatients with renal tuberculosis in the period from October 1993 to October 2005 and analyzed the specific features of the ultrasound images of these patients, in an effort to explore the clinical value and the accuracy of ultrasonography in the diagnosis and typing of renal tuberculosis. Methods In a total 258 cases of renal tuberculosis, there were 136 (52.7%) males and 122 females (47.3%).The ages ranged from 17 to 73 years old. The mean age was 45.3 years old. Left kidney tuberculosis occurred in 120 cases, accounting for 46.5%; right kidney tuberculosis occured in 118 cases (45.7%); both-sided kidney tuberculosis occured in 20 cases (7.8%). Some patients underwent intravenous urography (IVU) examination, retrograde pyeloureterography (RGP) examination, computed tomography (CT) scanning and cystoscopy. Other examinations included routine urinalysis; urine and needle aspirated material or drain fluid from percutaneous nephrostomy smears and cultures for acid-fast tubercle Correspondence: Xuefang Rui MD, Sir Run Run Shaw Hospital, 3 Qing Chun Road East, Hangzhou, Zhejiang 310016, China. Email: fanger01@sina. com.cn Received 24 December 2006; accepted 18 October 2007. Online publication 19 December 2007 bacilli; and determinations of tuberculosis antibody (TB-Ab) in blood and TB-DNA in urine with the Polymerase Chain Reaction (PCR) method. The treatment included surgery (nephrectomy, clearance of focal lesions, nephrectomy and later allograft kidney transplantation) and antituberculosis chemotherapy with the regular and full course. Aloka SSD-mode 630 and LOGIQ-700 ultrasonic diagnostic apparatuses were employed. The probe frequencies used with both apparatuses were the same 3.5 MHz. The patients were observed via multiple cross sections in routine supine, prone and lateral positions. The size of the kidney was measured. The shape of the kidney, the intensity and homogeneous degree of the echoes reflected from the renal cortex and medulla were observed. Any abnormal echo, separation or distension of the renal sinus, calyx, pelvis, ureter, and so on, were also made note of. Grounds for clinical diagnosis of renal tuberculosis were: (1) Typical clinical presentation and typical imageological manifestations of renal tuberculosis, 152 cases; (2) Positive results of smears and/or cultures of urine, needle aspirated material or drain fluid from percutaneous nephrostomy for tubercle bacilli, 149 cases; (3) In association with bladder and/or epididymis tuberculosis confirmed by cystoscopy and biopsy, 32 cases; (4) Positive results of urine PCR-TB-DNA or blood TB-Ab determination with favorable response to anti-tuberculosis chemotherapy in clinical symptoms and general condition, 157 cases. Results In this series of 258 cases, 152 cases were correctly diagnosed as renal tuberculosis by B-mode ultrasonography. The coincidence rate was 58.9%. The remaining 106 cases at first were separately misdiagnosed by B-mode ultrasonography as hydronephrosis, 27 cases; hydronephrosis with calculi, 18 cases; renal cysts, 19 cases; ureterostenosis at the upper segment, 7 cases; kidney tumor, 3 cases; ureter tumor at the lower segment, 5 cases; non-tuberculous inflammatory change of the kidney, 26 cases; and duplicated kidney, 1 case. Their final diagnosis was obtained by multi-modality methods. Among the 245 cases who had an intravenous urography (IVU) examination and the 85 cases that underwent retrograde 2007 The Japanese Urological Association 135

R XUEFANG ET AL. Fig. 1 Nephrectasia type of renal tuberculosis. Fig. 2 Hydrops type of renal tuberculosis. pyeloureterography (RGP) examination for non-diagnostic IVU, 113 cases were correctly diagnosed as renal tuberculosis. The coincidence rate was 46.1% (113/245). Among the 138 cases who underwent a CT scan examination, 87 cases were correctly diagnosed as renal tuberculosis, the coincidence rate was 63.0% (87/138). For making a more accurate clinical diagnosis of renal tuberculosis, and thereby facilitating the appropriate and proper treatment, in accordance with the specific features of ultrasound images, combined with macropathological changes, we classified the 152 cases that were correctly diagnosed as renal tuberculosis by ultrasonography into six types. Type I Fig. 3 Empyema type of renal tuberculosis. Nephrectasia type, 23 cases, accounting for 15.1% (23/152). In this type of renal tuberculosis, the renal capsule manifesting in the ultrasound image was very irregular. At the renal parenchyma and the area of the renal sinus, there were one or several anechoic zones, in different sizes with irregular margins. Within these zones, there were some nebulous light spot echoes. Some times the thickness of the cystic wall was uneven or even appeared serrate. On the inner wall of the cyst, there were inhomogeneous, macula patch-like strong echoes (Fig. 1). Type II Hydrops type, 21 cases, accounting for 14.4% (21/152). In the ultrasound image, the renal capsule was irregular. The renal pelvis and calyces were distended, within which there was an anechoic zone, similar to hydronephrosis. However, for renal tuberculosis of hydrops type, the inner wall was rough and uneven, echoes from the margins were enhanced. With the scan to trace the ureter, in most cases, it showed that the ureter was involved and appeared thickened, with a stiff running course. The lumen of the ureter was stenotic, the wall of the ureter thickened and rough with enhanced echoes (Fig. 2). Type III Empyema type, 13 cases, accounting for 8.5% (13/152). The outline of the kidney was obviously enlarged. The renal capsule was rough or locally protuberant and uneven. The renal cortex was swollen and hypoechoic. The renal pelvis and calyces were obviously distended, the boundaries of which were obscure. Within the boundaries, there was an anechoic zone with poor ultrasound penetration, nebulous small light spots or bold macula patch-like echoes, which were diffusely distributed (Fig. 3). Type IV Inflammatory and atrophy type, 15 cases, accounting for 9.8% (15/ 152). The kidney was obviously micrified in size. In most cases, the long diameter of the kidney was less than 8 cm, and the short diameter less than 4 cm. The renal capsule was irregular. The demarcation between the renal cortex and parenchyma was unclear. The internal echoes were chaotic, similar to the ultrasound image of chronic renal failure. This type of renal tuberculosis had its own special features: usually it was unilateral renal disease, the surface of the kidney was ruggedly uneven, and an inhomogeneous strong echoic zone could be seen, showing autonephrectomy manifestations (Fig. 4). Type V Calcification type, 34 cases, accounting for 22.3% (34/152). The renal capsule was irregular. In the renal cortical area, several mass lump-like or macula patch-like, strong echoes with irregular shapes in different sizes were seen, accompanied by an obvious ultrasound shadow behind them (Fig. 5). Type VI Mixed type, 46 cases, accounting for 30.2% (46/152). The kidneys were different sizes. The renal surface was not smooth. In the renal 136 2007 The Japanese Urological Association

Classification of renal tuberculosis Fig. 4 Fig. 5 Fig. 6 Inflammation and atrophy type of renal tuberculosis. Calcification type of renal tuberculosis. Mixed type of renal tuberculosis. parenchyma, the echoes were disorderly with irregular shapes; several anechoic zones and macula patch-like or mass lump-like, strong echoes could be seen, behind part of them accompanied by an ultrasound shadow. The renal pelvis and calyces were separate and within that area there was an anechoic dark zone. The ureter could be distended (Fig. 6). Discussion 1. The complex and varied manifestations of the ultrasound images of renal tuberculosis result from its different pathologically developing processes. Therefore the understanding of the pathological changes of renal tuberculosis at different stages is the basis for the correct typing of the ultrasound images of renal tuberculosis. Caseous cavity, fibrosis, pyonephrosis, calcification, inflammatory and atrophy are the common pathological changes of renal tuberculosis. Sometimes caseous cavity and calyx empyema or hydrops as well as macula spot-like or mass lump-like calcific focuses exist simultaneously in the same kidney. Based on its different pathologically developing stages, the great majority of mid-stage and advanced renal tuberculosis could be correctly diagnosed with ultrasound image typing. For this series of cases, the diagnostic coincidence rate is 58.9%. This ultrasonographic typing of renal tuberculosis is similar to that created by Wang Zheng-Bing et al. 3 in 1997. They divided the sonographic pictures of renal tuberculosis into five types, devoid of the inflammatory and atrophy type. In this series of cases, 15 patients were in the inflammatory and atrophy type, accounting for 9.8% (15/152). Because several different pathological stages of renal tuberculosis may exist in the same kidney at the same time, the manifestation of the ultrasound images may be very atypical, and may cause misdiagnosis or difficulty in diagnosing. In this series of cases, there were 106 cases whose ultrasonographic diagnoses were not coincident with the real disease, accounting for 41.1%. These results indicate that at present, the diagnosis of renal tuberculosis requires multi-modality methods and cannot be made by a single examination. The results also suggest that the varied appearances of renal tuberculosis in the ultrasonographic images are the reflection of the different pathological changes of renal tuberculosis at different developing stages. Bearing this in mind, ultrasonography is a convenient method for providing reliable information on renal tuberculosis. 2. The diagnostic accuracy of ultrasonography in the diagnosis of renal tuberculosis is correlated with the experience of the examiner, the resolution of the ultrasonographic apparatus and factors such as whether the patient is obese, different stages of the disease, and so on. To make a definite diagnosis, a careful inquiry of the patient s history and an understanding of the pathologically developing process of renal tuberculosis are necessary and indispensable. When an ultrasonographic image of the kidney does not indicate any other renal disease, then the possibility of renal tuberculosis should be considered. 6 Ultrasonographically guided transcutaneous needle aspiration can provide effective approaches to bacteriological and pathological diagnosis of renal diseases. In this series of cases, 10 patients obtained their final diagnosis through this procedure. 3. Ultrasonographic examination has a special value in visually monitoring kidney lesions for the follow-up patients who are undergoing antituberculosis chemotherapy, thus precluding repeated radiographic examinations. The proper therapeutic method could be chosen according to the sonographic typing of renal tuberculosis. In general, most of the type I (nephrectasia type) and type II (hydrops type) renal tuberculosis patients only need antituberculosis chemotherapy; most of the type III (empyema type) and type VI (mixed type) renal tuberculosis patients have to undergo surgical intervention; and nearly all of the type IV (inflammatory and atrophy type) and type V (calcification type) renal tuberculosis patients have to accept nephrectomy. 4. At present, the manifestations of renal tuberculosis in ultrasound images are not quite specific to renal tuberculosis; at the early stage, when the pathological changes of renal tuberculosis are confined to the renal cortex, the ultrasonographic examination has difficulty detecting such a subtle and minimal lesion; regarding the problems with identifying renal calyceal, pelvic and ureteric 2007 The Japanese Urological Association 137

R XUEFANG ET AL. abnormalities, ultrasonography is not as sensitive as CT scanning; hence, while diagnosing renal tuberculosis with an ultrasonographic examination, special care should be taken to differentiate between renal tuberculosis and the following renal diseases. between them was usually based on the clinical manifestations, laboratory examinations, IVU, RGP and CT scans. Even the diagnostic anti-tuberculosis chemotherapy was given to establish the diagnosis. (1) Renal tuberculosis and the renal cyst Simple renal cyst is a benign degenerative manifestation of the senescent kidney. In the ultrasound image, it shows a single or several round anechoic zones with a clear boundary. Its wall is thin and smooth with enhanced echoes at the rear wall. Behind both lateral walls, there is an inward ultrasound shadow. If the cyst develops inwards, the compression sign of the collecting system group can be seen; if the cyst develops outwards, local protrusion and malformation of the kidney will occur. Nephrectasia type renal tuberculosis results from tuberculous cavity. In the renal parenchyma, several anechoic zones in different sizes can be seen. Within the cysts there are nebulous light spot echoes. When the cold abscess is combined with calcification, within the dark zone there are some strong light masses with ultrasound shadow. In most cases, the shape of the cyst is irregular, the wall of the cyst is thickened and rough, sometimes with different thicknesses or even appearing serrate. The inner wall of the cyst reflects inhomogeneous, macula patch-like strong echoes. In this series, 19 patients were misdiagnosed as having renal cysts. The primary cause leading to this misdiagnosis was the neglect of the different manifestations of both lesions in the ultrasound images. At first sight, both lesions appear to have similar anechoic zones in the ultrasound images, but careful observation reveals that the anechoic zones of both lesions have several differences in shape, boundary, wall thickness and echoic density and homogeneity, thereby differentiating both lesions. (2) Renal tuberculosis and hydronephrosis Hydrops type renal tuberculosis and hydronephrosis are easily confused with each other. In this series, 27 patients at first were misdiagnosed as hydronephrosis. The differences between both lesions in ultrasound images are often subtle or minimal, and make the differentiation of both lesions difficult or impossible through ultrasound images. Sometimes ultrasonographically guided needle aspiration of the kidney is required for differentiation. (3) Renal tuberculosis and ureterostenosis When the ureter is involved by the pathological developing process of renal tuberculosis, the wall of the ureter will become swollen, thickened and rough, its lumen becomes stenotic. If the patients have only mild or even no evident clinical symptoms, the examiner will often rest content with the diagnosis of ureterostenosis rather than further consider what the cause of the problem is. In this series, seven patients were at first diagnosed as having ureterostenosis for this reason. With the patients symptoms getting worse and multimodality methods for diagnosis employed, the final diagnosis of renal tuberculosis was established. (4) Renal tuberculosis and non-tuberculous inflammatory changes of the kidney Renal tuberculosis and non-tuberculous inflammatory changes of the kidney have similar manifestations in ultrasound images in some patients. Twenty-six patients were misdiagnosed as inflammatory change of the kidney in this series. The differentiated diagnosis (5) Empyema type renal tuberculosis and hydronephrosis with infection Both of these cases show the distended renal pelvis and calyces, within which there are anechoic zones due to poor acoustic penetration. The differentiation of both lies in that: (a) for renal tuberculosis, the boundary between the renal pelvis and calyces is unclear. The wall of the renal pelvis is thickened and rough with enhanced echoes; within it there is a nebulous spotted hypoechoic zone. In the local area of the kidney, some irregular macula spot-like strong echoes with a weak sound shadow could be seen. For the latter, there are only a few and scattered spotted echoes in the hydrops anechoic zone; (b) for pyonephrosis, the laminated planes of hypoechoic light spot sediments could be seen within the anechoic zone; and for the latter, there is no such manifestation; and (c) in the former, the lesion often involves the ureter, and causes the ureter wall to thicken and become rough, with enhanced echoes; the ureter lumen develops stenosis and distension above the stenosed segment of the ureter. There are no such lesions in the latter. (6) Renal tuberculosis and kidney stones In renal tuberculosis, calcification may occur in the renal cortex, the manifestation of which is strong echoic light masses in the ultrasound image. In some cases this may be accompanied with sound shadow, similar to that of calculus. But in most cases, the density of the strong echoes is inhomogeneous in renal tuberculosis. Part of the calcified focuses present macula patch-like appearances, irregularly distributed, with an unclear boundary. The intensity of the echoes is lower than that of calculus. In renal tuberculosis, most calcified focuses are located in the renal cortex; but the kidney stone is located in the renal pelvis and calyx. Calcification is an important denotation of advanced renal tuberculosis. When associated with hydronephrosis and without renal atrophy, it is easily confused with kidney stones. In this series, 18 patients were misdiagnosed as hydronephrosis with calculi. Careful attention to the differences between both lesions in the stone location in the kidney and in shapes, intensity and homogeneity of the echoes, would help to differentiate both lesions. (7) Renal tuberculosis and the renal tumor In mixed type renal tuberculosis, the kidney may present an enlarged contour with mass lump-like echoes, and can potentially be misdiagnosed as renal tumor. But the contour in most cases is irregular, and its rear echoes are lightly enhanced. For a renal tumor, it arouses a sense of spheroid; and for a bigger tumor, its rear echoes present an attenuated appearance. Both lesions may sometimes have similar appearances in ultrasound images. In this series, three patients were misdiagnosed as having a renal tumor. Different clinical presentation and different laboratory examination results may help to differentiate both diseases. Final diagnosis requires bacteriological or pathological examination of the aspirated material through ultrasonographically guided needle aspiration of the kidney. 138 2007 The Japanese Urological Association

Classification of renal tuberculosis (8) Renal tuberculosis and the polycystic kidney The ultrasound image of a polycystic kidney shows an enlarged renal contour. The surface is rugged. In the cortical area there are innumerable round or elliptic anechoic zones in the different sizes, with a thin wall and enhanced echoes from the rear wall. The renal pelvis and calyces are compressed. The bilateral kidneys are involved simultaneously, often accompanied by the polycystic liver. The distended shape of the renal multi-calyces caused by renal tuberculosis is irregular. The wall of the renal calyces is thickened and rough, with enhanced echoes. Conclusion Ultrasonographic examination has convenient, low-priced and noninvasive advantages. The ultrasonographic typing of renal tuberculosis based on the distinguishing features of ultrasound images provides important and reliable information for the clinical diagnosis, differential diagnosis and treatment of renal tuberculosis. It also has a special value in visually monitoring kidney lesions for the follow-up patients who are undergoing antituberculosis chemotherapy and in guiding needle aspiration of the kidney for bacteriological or pathological examinations. 7 References 1 Prekurmar A, Lattimer JK. CT and sonography of advanced urinary tract tuberculosis. AJR. Am. J. Roentgenol. 1987; 148: 65 9. 2 Li Y-F, Fang Y-H, Jin F-S et al. The symptoms and diagnostic analyses of 96 cases of atypical renal tuberculosis. J. Clin. Urol. 1999; 14: 104 6. 3 Wang Z-B, Yuan M, Fan Y-Y et al. Further investigation of sonographic diagnosis and typing of renal tuberculosis. Chin. J. Ultrasonogr. 1997; 6: 220 2. 4 Quan C-B, Tao C-Y, Li X-L et al. Imaging comparison of renal tuberculosis. Chin. J. Med. Imaging Technol. 2000; 16: 195 7. 5 Bai M, Han Y, Zhao Y. Diagnosis Evaluation of Different Radiological Examinations in Renal Tuberculosis. Tianjian Med. J. 2006; 34: 390 2. 6 Cheng R.-P, Wang H-L, Zhao X-X et al. B-mode ultrasonic diagnosis of renal tuberculosis. Chin. J. Ultrasonogr. 1995; 4: 83 4. 7 Nicholas Papanicolaou: Urinary tract imaging and intervention: Basic principles. In: Walsh PC, Retic AB, Vaughan ED, Wein AJ (eds). Campbell s Urology, 7th edn, Vol. 1. W.B. Saunders Company, Philadelphia, PA, 1998; 204 205. 2007 The Japanese Urological Association 139