Renal involvement in lymphoma: prevalence and various patterns of involvement on abdominal CT

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1 Int Urol Nephrol (2007) 39: DOI /s ORIGINAL ARTICLE Renal involvement in lymphoma: prevalence and various patterns of involvement on abdominal CT Mohammed Sherif El-Sharkawy Æ Neelam Siddiqui Æ Aamer Aleem Æ Abdulrahman Al Diab Received: 2 April 2007 / Accepted: 6 April 2007 / Published online: 5 June 2007 Ó Springer Science+Business Media B.V Abstract Objective The kidney is a frequent site of involvement in lymphoproliferative disorders. The aim of this study was to demonstrate the prevalence and spectrum of morphologic appearances of renal involvement in patients with lymphoma on helical computed tomographic (CT) scan. Methods Three phases of post-contrast helical CT of the abdomen in 74 patients with lymphoma were reviewed for possible renal involvement: the corticomedullary, nephrographic and delayed excretory phases. Tumor characteristics, patterns of distribution and enhancement features were evaluated. Results Of the 74 patients with lymphoma, 11 had CT evidence of renal involvement ten with non- Hodgkin s lymphoma and one with Hodgkin s lymphoma representing 15% of all patients scanned for routine staging of histologically diagnosed lymphoma. Five types of renal involvement were observed: enlarged lobular non-enhancing kidneys M. S. El-Sharkawy (&) Department of Radiology and Medical Imaging, King Khalid University Hospital, King Saud University, P.O. Box 7805, Riyadh 11472, Kingdom of Saudi Arabia sherif_elsharkawy@hotmail.com N. Siddiqui A. Aleem A. A. Diab Division of Oncology/Hematology, Department of Medicine, King Khalid University Hospital, King Saud University, P.O. Box 7805, Riyadh 11472, Kingdom of Saudi Arabia (four patients); bilateral multiple renal masses (two patients); focal single non-enhancing mass (two patients); perirenal infiltrations from retroperitoneal extension (two patients); bilateral diffuse areas of non-enhancing hypo-densities (one patient). Conclusion Five distinct patterns of renal involvement with lymphoma were detected with helical CT. The most common appearance was enlarged lobular kidneys. CT with intravenous contrast enhancement is currently the approach of choice for both the evaluation of renal involvement as well as for accurate staging of lymphoma. Awareness of different patterns of renal involvement in lymphoma allows proper differentiation from other similar diseases. Keywords Helical CT Hodgkin s lymphoma Non-Hodgkin s lymphoma Lymphoma Renal Abbreviations CT Computed tomography HL Hodgkin lymphoma MRI Magnetic resonance imaging NHL Non-Hodgkin Lymphoma Introduction All lymphoproliferative diseases (including lymphoma, leukemia and plasma cell dyscrasias) have the potential to infiltrate the kidney, but lymphoma is

2 930 Int Urol Nephrol (2007) 39: the most frequently observed of these. [1]. Malignant lymphomas comprise a heterogeneous group of neoplasms involving lymphoid cells that are broadly divided into Non-Hodgkin s lymphoma (NHL) and Hodgkin s lymphoma (HL). Extra nodal disease, including renal involvement, occurs more frequently with NHL than with HL even though their radiological patterns are similar [2]. Once the diagnosis of lymphoma has been established, the first step is pre-treatment evaluation and staging to identify prognostic factors and the assessment of impending problems, such as ureteral obstruction, spinal cord compression and biliary or vena caval obstruction [3]. Due to the availability of sophisticated imaging techniques, such as helical computed tomography (HCT), magnetic resonance imaging (MRI) and ultrasonography (US), it has been possible to improve clinical staging so that an invasive pathological staging is seldom necessary. In this respect, CT is the preferred modality, although US and MRI may also be diagnostically valuable [3, 4]. The presence of infiltrative renal lesions on crosssectional imaging when seen with concomitant bulky perinephric disease, widespread lymphadenopathy or contra-lateral renal involvement is very suggestive of lymphoma [1]. However, the radiological spectrum of renal infiltration by lymphoma is diverse and must be differentiated from other diseases involving the kidneys. The objective of this study is to describe the morphologic appearances, distribution and enhancement patterns of renal lymphoma on CT images. Materials and methods This study consisted of 74 patients with lymphoma who were referred the Radiology Department of King Khalid University Hospital in Riyadh as part of the staging procedures for histologically diagnosed lymphoma. The patients were subjected to clinical assessment, laboratory investigations and different imaging modalities, particularly chest x-ray, CT of the abdomen and bone marrow biopsy. The patients were examined by CT of the abdomen and pelvis in pre-and post-contrast studies. A nonionic contrast substance (Omnipaque 350; cc) was injected at a rate of 2 3 ml/s. Scanning was carried out on a GE Helical Multidetector machine (Model Light Speed 16; General Electric, USA) with 5-mm collimation; the slice thickness of the post-contrast studies was 3 5 mm. The scan delay was 30 s (cortico-medullary phase), 90 s (nephrographic phase) and 4 min (excretory phase); the reconstruction interval was 3 5 mm. Prior to CT examination a diluted oral contrast substance (3% gastrografin; 750 cc) was administered to allow proper bowel opacification. The CT abdominal studies of 74 consecutive patients diagnosed with lymphoma (with different subtypes) were reviewed. Results Following the review of the abdominal CT studies of the 74 known lymphoma patients included in this study, we observed radiological evidence of renal infiltration in 11 patients; of these, ten had NHL and one had HL. The different patterns of renal involvement observed in our patients are described below and in Table 1. Enlarged non-enhancing kidneys Four cases of enlarged kidneys with lobulated outline were seen: one patient showed unilateral involvement, and the other three had bilateral kidney involvement. The renal parenchyma was hypo-dense in the early postcontrast CT study (cortico-medullary phase). This Table 1 Renal involvement in lymphoma as revealed by the CT patterns of disease Involvement pattern Enlarged, non-enhancing lobular kidneys Bilateral, multiple, focal intraparenchymal lesions Focal single nonenhancing lesion Number of patients Percentage Distribution 4/ Bilateral 2/ Bilateral 2/ Unilateral; n = 2/2 Perirenal infiltration 2/ Bilateral; n =½ Unilateral; n =½ Diffuse, bilateral areas of non-enhancing hypodensities 1/11 9 All are bilateral

Int Urol Nephrol (2007) 39:929 933 931 was not a sign of renal failure as those patients did not show compromise on the routine pre-study renal function tests; fair parenchymal enhancement was also

Multiple renal masses Two cases of multiple masses in the renal parenchyma were seen.

Bilateral diffuse hypodensities Interestingly, the only HL case showed bilateral diffuse areas of nonenhancing hypo-density in enlarged kidneys.

3 Int Urol Nephrol (2007) 39: was not a sign of renal failure as those patients did not show compromise on the routine pre-study renal function tests; fair parenchymal enhancement was also exhibited on the nephrographic phase and good excretion was found on the excretory phase, which showed pelvicalyceal opacification. Multiple renal masses Two cases of multiple masses in the renal parenchyma were seen. In both these cases, the masses were multiple, bilateral, focal intraparenchymal, hypo-dense and non-enhancing foci that were visible that were less dense than the surrounding parenchyma. Bilateral diffuse hypodensities Interestingly, the only HL case showed bilateral diffuse areas of nonenhancing hypo-density in enlarged kidneys. This was also the only case that showed no evidence of retroperitoneal masses, whereas all other patients had retroperitoneal lymphadenopathy. Fig. 1. Fig. 2 Post-contrast CT of the kidneys in a NHL patient with renal involvement. A focal, hypo-dense single-mass lesion of the right kidney is visible Solitary masses Single, focal, intraparenchymal, non-enhancing hypo-dense lesions were observed in two patients. Fig. 2. Fig. 3 NHL patient with peri-aortic diffuse lymphomatous mass with right intrarrenal (hilar) and peri-renal infiltrations Perirenal infiltrates Two patients showed evidence of perirenal infiltration which took the form of an extension from retroperitoneal lymphomatous masses. The involvement was unilateral in one patient and bilateral perirenal in the other patient (Fig. 3). The atypical rare types of renal involvement that include spontaneous hemorrhage, necrosis, heterogeneous attenuation, cystic transformation and calcification were not identified in any of our cases [5]. None of the 11 patients, including those with periureteral lymphomatous extension, showed significant hydronephrotic changes, marked ureteric dilatation or non-functioning kidneys. Discussion Fig. 1 Post-contrast CT study. Diffuse non-enhancing parenchymal areas of lymphomatous infiltrations involving the entire left kidney and part of the right kidney Renal lymphoma is most often seen in conjunction with advanced, disseminated NHL, either at the time of initial staging in a newly diagnosed patient or with relapse of the disease [2]. Although less common than NHL, extra-nodal lesions in HL may develop and spread to virtually any organ system, simulating

4 932 Int Urol Nephrol (2007) 39: other neoplastic or infectious diseases [6]. In some autopsy studies renal involvement has been reported in 34 60% of patients with lymphoma [7]. However, renal lymphoma has been described in only % of lymphoma patients undergoing routine abdominal CT scans during staging investigations [2, 8]. In our study, renal involvement was detected in 15% of the 74 lymphoma patients reviewed. This incidence is higher than previously reported figures and could partly be explained by the continuously improving techniques of CT in more recent years, leading to the increased sensitivity of radiological detection of lymphomatous tissue. Another important aspect to consider is the fact that many of our patients presented late in the course of their disease, possibly leading to further dissemination of lymphoma. The combination of its non-invasive nature and extremely high diagnostic yield ultimately makes CT an integral component of uro-radiological diagnosis. Computed tomography is the most sensitive, efficient and comprehensive examination modality for evaluation of the kidneys in patients with suspected renal lymphoma [5, 9]. Intravenous contrast administration is essential for the diagnosis of renal lymphoma in the majority of patients. Subtle parenchymal involvement, especially infiltrative forms of the disease can be missed entirely without contrast enhancement [1, 10]. Contrast enhancement on CT studies enables the proper definition of retroperitoneal vasculature, which in turn helps the clinician to differentiate between normal retroperitoneal structures, enlarged lymph nodes, lymph node masses and their extensions. An additional advantage of contrast administration is the better definition of lymphomatous renal infiltrates, which are mostly hypo-or non-enhancing as they usually contain few blood vessels [11]. In our study, the post-contrast administration was carried out in the cortico-medullary and nephrographic phases in order to differentiate hypo- or non-enhancing lymphomatous masses from other mimicking neoplastic masses. In addition, the post-contrast administration in the excretory phase allowed proper exclusion of advanced obstructive pelvi-ureteric changes and renal excretory compromise. We have demonstrated five different patterns of renal lymphoma on CT examination. Although various patterns of renal involvement by lymphoma have been described by other authors, the frequency of these patterns differed somewhat in our patients [2, 12, 13]. In the literature, the most commonly encountered pattern of renal involvement in patients with lymphoma is the infiltration of kidney by multiple masses [1, 7, 8]. These are seen as hypoechoic masses on US sonograms and as hypo-dense masses on CT scans [13, 14]. Lymphoma presenting as a solitary renal mass is the most rare form and has a non-specific growth pattern mimicking renal adenocarcinoma [15]. In our patients, the commonest pattern was enlarged lobular kidneys (36.4%). The incidence of multiple renal masses, a solitary mass and peri-renal infiltration was similar in six patients (18% each). Diffuse non-enhancing hypo-dense patches in intraparenchymal zones of mildly enlarged kidneys was found in only one patient. Bilateral renal disease has been reported in 75% of cases of renal involvement with lymphoma [5]. Similarly, in this study, the incidence of bilateral disease was as high as 82% (n = 8/11). One of the surprising findings in peri-renal and hilar renal lymphomatous infiltration is the absence of hydronephrosis and renal function compromise until the late stages. This has been explained by the absence of mucosal infiltration in these cases [16, 17]. Lymphoma tends to infiltrate around, and not impinge on the ureter, a feature more easily demonstrated by CT than retrograde ureterography. This seems to be the reason why hematuria is not a feature in the cases of peri-ureteral lymphoma. None of our cases showed non-functioning kidneys or significant hydronephrotic changes. Even the four cases that showed enlarged lobular non-enhancing kidneys on the CT scans of the cortico-medullary and nephrographic phases did not show pelvicalyceal opacification or delayed scans. The lack of obstruction in cases of peri-ureteral lymphoma extension is striking in view of thebulk of the disease and may help in differentiating peri-ureteric lymphomatous infiltration from retroperitoneal fibrosis or nodal diseases of other etiologies [18]. Infiltration of perinephric fat and thickening of the perinephric fascia may occur in inflammatory disease and lymphoma [19]. Supportive clues for the lymphomatous nature of these lesions are hypo-dense or non-enhancing lesions on post-contrast CT scans along with the presence of bulky retroperitoneal lymph nodes [1, 8, 15]. Needless to say all, these findings are well demonstrated on helical CT scans following the administration of contrast bolus.

5 Int Urol Nephrol (2007) 39: The established radiological technique for diagnosis of lymphoma is currently CT, generally supplemented by initial sonography of the abdomen [19, 20]. In general, CT-based diagnosis of renal lymphoma is not difficult because most patients already have a known diagnosis of lymphoma; nevertheless, it is important to be familiar with both typical and atypical appearances of renal lymphoma because numerous disease processes, normal variants and artifacts may potentially mimic renal lymphoma [11]. In conclusion, lymphoma remains one of the diseases that requires accurate staging for proper treatment modality selection. One of the important sites of lymphomatous dissemination is the kidney. Although renal involvement does not cause renal function impairment except at very late stages in the course of the disease detection of renal involvement will have an impact on patient management. Recent advances in CT equipment and the widespread availability of multi-detector helical CT apparatus have made CT a valuable modality in the staging of lymphoma cases and the detection of renal involvement. Awareness of the different patterns of renal involvement and, consequently, differentiating them from other diseases will add much more to its diagnostic accuracy. References 1. Pickhardt PJ, Lonergan GJ, Davis CJ, Kashitani N et al. (2000) Infiltrative renal lesions: radiologic-pathologic correlation. Radiographics 20: Hartman DS, David CJ Jr, Goldman SM, Friedman AC et al. (1982) Renal lymphoma: radiologic-pathologic correlation of 21 cases. Radiology 144: Mavromatis BH, Cheson BD (2002) Pre and post treatment evaluation of non-hodgkin s lymphoma. Best Practice Res Clinic Hematol 15: Jung G, Heindel W, von Bergwelt-Baildon M, Bredenfeld H, Gossman A, Zahringer M, Tesch H (2000) Abdominal lymphoma staging: is MR imaging with T2-weighted turbo-spin-echo sequence a diagnostic alternative to contrast enhanced spiral CT. J Comput Assit Tomogr 24: Urban BA, Fishman EK (2000) Renal lymphoma: CT patterns with emphasis on Helical CT. Radiographics 20: Guermazi A, Brice P, de Kerviler EE, Ferme C, Hennequin C, Meignin V, Frija J (2001) Extra nodal Hodgkin disease: spectrum of disease. Radiographics 21: Richmond J, Sherman RS, Diamond HD et al (1962) Renal lesions associated with malignant lymphomas. Am J Med 32: Reznek RH, Mootoosamy I, Webb JA, Richards MA (1990) CT in renal and perirenal lymphoma: a further look. Clin Radiol 42: Sagel SS, Stanlely RJ, Levitt RG et al. (2002) Computed tomography of the kidney. J Urol 167: Jung G, Heindel W, VonBergwel-Baildon M, Bedenfeld H, Gossman A, Zahringer M, Tesch H (2000) Abdominal lymphoma staging: is MR Imaging with T2-weighted turbo-spin-echo sequence a diagnostic alternative to contrast enhanced spiral CT? J Comput Assit Tomogr 24: Eisenberg PJ, Papanicolaou N, Lee MJ, Yoder IC (1994) Diagnostic imaging in the evaluation of renal lymphoma. Leuk Lymphoma 16: Burgener FA, Hamlin DJ (1981) Histiocystic lymphoma of the abdomen: radiographic spectrum. Am J Roentgenol Horii SC, Bosniak MA, Megibow AJ, Raghavendra BN, Subramanyam BR, Rothberg M (1983) Correlation of CT and ultrasound in the evaluation of renal lymphoma. Urol Radiol 5: Heiken JP, Gold PR, Schnur MJ et al. (1983) Computed tomography of renal lymphoma with ultrasound correlation. J Comp Assist Tomogr 7: Sheeran SR, Sussman SK (1988) Renal lymphoma: spectrum of CT findings and potential mimics. Am J Roentgenol 171: Buck DS, Peterson MAS, Borochoviks D et al. (1992) Non-Hodgkin lymphoma of the ureter: CT Demonstration with pathological correlation. Urol Radiol 14: Chen HH, Panella JS, Rochester D et al (1988) Non- Hodgkin lymphoma of the ureteral wall: CT findings. J Comput Assist Tomogr 12: Connor SE, Umaria N, Guest PJ (2001) Extranodal peripelvic and periureteric lymphoma-demonstration with computed tomography. Clinic Radiol 56: Hauser M, Kresin GP, Hagspiel KD (1995) Bilateral solid multifocal and perirenal lesions: differentiation with ultrasonography, computed tomography and magnetic resonance imaging. Clin Radiol 50: Munker R, Stengel A, Stabler A et al. (1995) Diagnostic accuracy of ultrasound and computed tomography in the staging of Hodgkin s disease: verification by laparotomy in 100 cases. Cancer 76:

Educational Exhibit Authors:

Educational Exhibit Authors: Renal lymphoma: Patterns of disease with ultrasound (US), colourdoppler ultrasound (CDUS), contrast-enhanced ultrasound (CEUS) and Computed tomography (CT) Poster No.: C-1545 Congress: ECR 2011 Type: Educational