MR Renographic Measurement of Renal Function in Patients Undergoing Partial Nephrectomy

Genitourinary Imaging Review Kang et al. MR Renography and Partial Nephrectomy Genitourinary Imaging Review FOCUS ON: Stella K. Kang 1,2 William C. Huang 3 Vivian S. Lee 4 Hersh Chandarana 1 Kang SK, Huang WC, Lee VS, Chandarana H Keywords: MR renography, partial nephrectomy, renal function DOI:10.2214/AJR.12.10276 Received November 7, 2012; accepted without revision November 11, 2012. Partially supported by an RSNA seed grant (RSD0911) awarded to H. Chandarana. 1 Department of Radiology, New York University Langone Medical Center, New York, NY. 2 Present address: Department of Radiology, Massachusetts General Hospital, Division of Abdominal Imaging and Interventional Radiology, White Bldg, Rm 270, 55 Fruit St, Boston, MA 02114. Address correspondence to S. K. Kang (skang4@partners.org). 3 Department of Urology, New York University Langone Medical Center, New York, NY. 4 Department of Radiology, University of Utah Health Sciences, Salt Lake City, UT. CME/SAM This article is available for CME/SAM credit. AJR 2013; 200:1204 1209 0361 803X/13/2006 1204 American Roentgen Ray Society MR Renographic Measurement of Renal Function in Patients Undergoing Partial Nephrectomy OBJECTIVE. The purpose of this review is to describe the role of functional renal MRI, or MR renography, in the care of patients with renal masses undergoing partial nephrectomy. CONCLUSION. MR renography can be used to monitor renal functional outcome for patients undergoing partial nephrectomy and may help guide patient selection in this population with elevated risk of chronic kidney disease. T he management of renal masses has evolved with the downward stage migration of renal cell carcinoma (RCC) at presentation. From 1983 to 2002, there was a 52% increase in the diagnosis of RCC, of which T1a tumors (small renal masses up to 4 cm) had a threefold increased incidence, the highest of all stages [1]. T1a tumors now represent 70% of all renal cancers diagnosed [2, 3]. This trend is at least partially attributable to the rapid rise in utilization of abdominal imaging and the incidental detection of RCC [3, 4]. Surgical treatment of small renal masses has evolved from nephrectomy to nephron-sparing surgery, or partial nephrectomy. Radical nephrectomy was historically favored by urologists for treatment of all tumors, even category T1a, out of concern for oncologic control. However, adverse renal functional consequences of nephrectomy eventually drove the adoption of partial nephrectomy. The current standard of management of T1a tumors, partial nephrectomy has been found to have oncologic outcomes equivalent to and greater potential preservation of renal parenchyma than radical nephrectomy [5]. Even after partial nephrectomy, as many as 50% of patients have chronic kidney disease [6]. Functional renal MRI may play an important role by providing accurate estimates of individual kidney glomerular filtration rate (GFR) and help guide the development of improved surgical approaches to renal preservation. The purpose of this review is to describe the current status of partial nephrectomy techniques and the potential role of MR renography in eval- uating functional outcome in RCC patients undergoing partial nephrectomy. Current Status of Partial Nephrectomy Rationale for Use of Partial Nephrectomy As late as the 1990s, nephron-sparing surgery was reserved for patients with solitary kidneys, genetic syndromes predisposing to increased risk of RCC, or severe chronic kidney disease (CKD) [7]. Radical nephrectomy was long believed to have superior oncologic outcome. Since the mid-2000s, several studies have shown equivalent oncologic control of tumors smaller than 4 cm and of select tumors as large as 7 cm with partial nephrectomy [8 10]. Furthermore, for T1a lesions, studies have shown worse overall mortality with radical nephrectomy than with partial nephrectomy [11]. In addition, when stratified by estimated GFR, studies have shown a graded increase in cardiovascular and overall mortality [6, 11 13]. The results of these seminal studies highlight the importance of preserving renal function in patients with RCC who are elderly and who may have underlying renal disease at baseline [14, 15]. To improve patient outcome through preservation of renal function, partial nephrectomy has become the standard of care of patients with T1a renal masses. According to Surveillance, Epidemiology, and End Results registry data, use of partial nephrectomy increased from 20% to 45% for T1a RCC between 2000 and 2010 [16]. Despite the increase in diagnosis of early-stage renal tumors, there has been a paradoxic increase in cancer-specific and overall mortality rates among patients with RCC 1204 AJR:200, June 2013

MR Renography and Partial Nephrectomy irrespective of tumor size [1]. From 1983 to 2002, mortality associated with T1a lesions increased more than mortality associated with lesions larger than 7 cm. Causes of this increase in mortality may be multifactorial, including lead-time and selection biases and medical comorbidities such as cardiac and renal disease. This increase in mortality also correlated with the increase in surgical therapy for T1a tumors during the same period [1]. The effect of surgical intervention on long-term morbidity and overall mortality requires further investigation. Partial Nephrectomy: Techniques and Limitations Partial nephrectomy can be performed with either an open or a laparoscopic approach. A D Since the mid-2000s, laparoscopic and robotic techniques have been increasingly incorporated into urologic surgery and adopted for partial nephrectomy. Minimally invasive techniques have oncologic outcomes equivalent to those of open approaches. Benefits include decreased pain, shorter convalescence, and improved appearance [8, 17, 18]. One potential problem of a laparoscopic approach is the inability to protect the kidney from ischemic injury during surgery through the use of renal hypothermia. Clamping of the renal artery is essential in most cases to reduce bleeding during resection. With open partial nephrectomy, renal hypothermia can help prevent ischemic injury, but laparoscopic cold ischemia is not available clinically. Although it is unclear how much warm ischemia time is Gadolinium Retention 60 50 40 30 20 10 0 10 0 50 100 150 200 Time (s) 250 300 B E tolerable before induction of irreversible renal injury, data suggest shorter warm ischemia periods are safer [19, 20]. Although laparoscopic resection despite long warm ischemia times is preferable to radical nephrectomy for nephron preservation, the adverse effects of warm ischemia compared with cold ischemia remain controversial and poorly studied. Partial Nephrectomy and Chronic Kidney Disease Even though more renal parenchyma is preserved with partial nephrectomy, CKD develops in as many as 50% of patients undergoing this operation [6]. Increasing numbers of kidney tumors are being removed with laparoscopic and robotic techniques under conditions of warm ischemia. As larger and more complex and multiple tumors are resected lap- Fig. 1 Postprocessing of MR renographic images. A, After image registration, kidney is segmented from perinephric fat. B, Renal cortex (red) is segmented from the renal medulla and collecting system (blue). C, Renal medulla (blue) is segmented from the collecting system (red). D, Completed segmentation shows each compartment: renal cortex, medulla, and collecting system. E, Gadolinium retention (μmol) versus time plots for cortex (circles) and medulla (squares) generated before application of three-compartment tracer kinetic model to produce individual kidney glomerular filtration rates. Dashed line indicates fit for cortex; dotted and dashed line, fit for medulla. C AJR:200, June 2013 1205

Kang et al. blood sampling and is a time-consuming technique. Technetium 99m diethylenetriamine pentaacetic acid plasma clearance combined with scintigraphy may also serve as a reference standard for measuring single-kidney GFR. However, scintigraphy is a cumbersome method and clinically impractical for routine use [22, 23]. CT techniques for deriving GFR have the advantage of superior spatial resolution and accurate contrast quantification. However, disadvantages of ionizing radiation and the potential nephrotoxic effects of iodinated contrast preclude its routine use. Quantitative dynamic contrast-enhanced MRI of the kidneys, or MRR, has a number of important advantages for the noninvasive measurement of renal function. Without exposing the patient to ionizing radiation, the technique has been found to provide accurate information about single-kidney funcaroscopically, prolonged ischemia times expose patients to increased risk of permanent renal injury. Sensitive and accurate biomarkers for predicting susceptibility to CKD are needed to guide surgical interventions. One of the challenges in predicting renal injury and in studying functional outcomes after partial nephrectomy has been the lack of tools available for measuring individual kidney function. Most investigators have used serum creatinine concentration based estimates of GFR. These population-based estimators are limited in accuracy and sensitivity and do not show individual kidney GFR. As a functional imaging technique, MR renography (MRR) may complement standard preoperative and postoperative imaging of patients with renal masses and help overcome some of the existing limitations in evaluation of these patients. Fig. 2 54-year-old woman with renal cell carcinoma. A, Preoperative MR renographic image shows heterogeneously enhancing left upper pole renal mass measuring 6 cm (arrow). B, Patient had normal baseline renal function and underwent laparoscopic partial nephrectomy with warm ischemia time of 25 minutes with no complications. MR renographic image shows approximately 33% of parenchymal volume has been resected with corresponding 34% loss of glomerular filtration rate (GFR) in affected kidney in immediately postoperative period. With compensatory increase in contralateral GFR, however, total MRI-GFR decreases only 14% from baseline. C, MR renographic image 6 months after surgery shows resected kidney has qualitative enhancement similar to that of other kidney with GFR loss stable at 35%. MR Renography in Patients Undergoing Partial Nephrectomy Noninvasive Measurements of Kidney Function Several invasive and noninvasive tests are available for measuring renal function. Estimates of GFR are made with regression equations derived from specific populations so that serum creatinine concentration, weight, sex, and other parameters can be used to estimate a total GFR value for an individual. The accuracy of these approaches is limited, particularly when applied to patient cohorts that do not match those used to define the estimators [21]. Estimates of GFR are estimates of total kidney function and not of single-kidney function. After partial nephrectomy, knowledge of the response of each kidney to the procedure is critical. Inulin clearance is considered the reference standard for individual renal function measurement but requires A B C 1206 AJR:200, June 2013

MR Renography and Partial Nephrectomy tion across normal and abnormal values [24 28]. The method requires very low doses of gadolinium contrast material, less than 20% of a standard dose, and is safe in most patients. MRR may be performed as an adjunct to clinical MRI protocols, complementing the anatomic delineation and tissue characterization available with MRI. Parameters other than single-kidney GFR can be determined with MRR. Tumor volume and renal parenchymal volume are easily determined. With these advantages, MRR may be a suitable tool for assessing differences in functional outcomes based on patient selection and surgical technique. A C Fig. 3 53-year-old woman with renal cell carcinoma and baseline stage III chronic kidney disease who underwent open partial nephrectomy with ischemia time of 40 minutes because of collecting system injury requiring repair. Acute tubular necrosis developed postoperatively. A and B, Preoperative coronal HASTE (A) and MR renographic (B) images show 5-cm renal cell carcinoma in left upper pole (arrow) closely associated with upper pole calyx. C, MR renographic image shows resected kidney has approximately 50% loss of glomerular filtration rate (GFR) in immediately postoperative period with appreciable qualitative decrease in upper pole enhancement. No contralateral kidney GFR increase occurred in this patient with moderate chronic kidney disease. D, MR renographic image 6 months after surgery shows resected kidney GFR partially recovered and some qualitative improvement in enhancement. Technique MRR may be performed as an adjunct to standard preoperative MRI for renal mass evaluation. Conventional renal mass MRI protocols include coronal and axial T2-weighted HASTE, axial T1-weighted gradient-echo inand opposed-phase, and axial 3D T1-weighted fat-suppressed gradient-echo volume interpolated breath-hold examination (VIBE) unenhanced and contrast-enhanced acquisition in the corticomedullary, nephrographic, and excretory phases of enhancement with a standard (0.1 mmol/kg) dose of gadolinium contrast material. MRR acquisitions are performed before contrast administration for the VIBE sequence. MRR can be performed with 3D or 2D methods. For imaging of patients with renal masses, a coronal 3D spoiled T1-weighted gradient-echo sequence with a view-sharing under sampling technique called time-resolved angiog raphy with stochastic trajectories (TWIST) [29, 30] achieves volumetric 3D coverage at high temporal resolution at a cost of lower signal-tonoise ratio and temporal blurring due to view sharing. The abdominal aorta and both kidneys are covered in the coronal plane. The contrast dose of approximately 4 ml gadopentetate dimeglumine (Magnevist, Bayer HealthCare) is administered at a rate of 2 ml/s followed by a 20-mL saline flush. Imaging can begin 5 seconds after contrast administration. For patients undergoing partial nephrectomy, postoperative MRR may be performed alone or with other clinical imaging sequences to assess for recurrent or metastatic disease. MRI Postprocessing The greatest challenge with MRR is the conversion of signal intensities measured on the images to estimates of GFR. In most approaches, measurement of changes in signal intensity in both the kidney and the aorta are B D AJR:200, June 2013 1207

Kang et al. necessary because dispersion of the IV injected bolus will affect the pattern of enhancement in the kidney. Because patients breathe during acquisition, the initial step of image analysis for MRR typically involves image registration and segmentation so that regions of interest can be used to sample aortic and renal cortical and medullary signal intensity versus time curves [31] (Fig. 1). The renal parenchymal volume of each kidney can also be automatically generated with the same software program. In MRI, unlike CT, signal intensities are not linearly related to gadolinium contrast concentration. Therefore in the second step, aortic and renal signal intensities are converted to T1 values and then to gadolinium tracer concentration versus time curves. One reliable approach uses the additivity of relaxivity to convert gadolinium concentration to T1 with the following formula: [Gd] = (1/T1 1/T1 0 ) / r 1, where [Gd] is gadolinium concentration, r 1 is the relaxivity of gadolinium (4.5 mm 1 s 1 ), and T1 0 is the measured or estimated unenhanced T1 value for the aorta, renal cortex, and medulla [32]. Gadolinium concentration versus time curves can be used to derive single-kidney GFR by use of a tracer kinetic model. Although many models have been proposed [33 37], a comparison of them yielded modest differences. For our routine renal mass evaluation with 3D MRR, we implemented a corticomedullary tracer kinetic model of three compartments that yields single-kidney GFR and perfusion parameters for each kidney [25, 26, 32, 38]. The total MRI-GFR represents the sum of single-kidney GFR in the two kidneys. Single-kidney GFR and MRI- GFR are normalized to a patient s body surface area, akin to serum creatinine concentration based estimates of GFR. Potential Importance of MR Renography to Partial Nephrectomy Patients MRR can be performed as an adjunct to the standard MRI protocol for renal mass evaluation. It takes less than 10 minutes of additional imaging time to obtain a single-kidney GFR for each kidney. Use of low-dose gadolinium contrast medium for MRR does not interfere with subsequent contrast-enhanced imaging of the abdomen [28]. In partial nephrectomy patients, MRR may be used preoperatively and postoperatively to monitor changes in renal function in the kidney that was operated on and the contralateral kidney. For example, MRR can be used to examine the reversibility of functional loss in the kidney that was operated on and to measure compensatory increases in GFR of the contralateral kidney both in the immediately postoperative period and in the long term [39]. Because functioning parenchyma can be lost to resection and ischemic injury, MRR assessment of volume changes in the renal parenchyma are also important (Fig. 2). In the urologic literature, the most important factors, both modifiable and nonmodifiable, for predicting the development of CKD in patients undergoing partial nephrectomy are hotly debated. Parenchymal volume loss is one of the most important suspected risk factors, but studies of this parameter are weakened by inability to delineate the contribution of the contralateral kidney to estimates of GFR [19, 40]. Preoperative kidney function may play an important role in postsurgical development of CKD. Underlying disease may predispose a patient to irreversible ischemic injury in the kidney being resected, and reduced compensatory reserve may affect the contralateral kidney. In the near future it may be possible to use MRR to guide patient selection by using the findings to categorize postoperative risk of CKD and to assess the need for renal protective techniques based on preoperative renal functional status. Operative management of renal lesions can also be affected by MRR findings, which may be useful for guiding operative management in a number of ways. Single-kidney GFR measurements are helpful for assessing the contribution of the diseased kidney to overall GFR. Selection of an open or a laparoscopic approach and the associated type and duration of ischemic risk to the resected kidney may depend on baseline renal function. Last, lesion characteristics, including endophytic location, size, and proximity to the collecting system or hilum, may influence approach. Tumor characteristics have been found to correlate with longer ischemia times during surgery [41] (Fig. 3). 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Mayer WA, Godoy G, Choi JM, Goh AC, Bian SX, Link RE. Higher renal nephrometry score is predictive of longer warm ischemia time and collecting system entry during laparoscopic and robotic-assisted partial nephrectomy. Urology 2012; 79:1052 1056 FOR YOUR INFORMATION This article is available for CME/SAM credit. To access the exam for this article, follow the prompts associated with the online version of the article. AJR:200, June 2013 1209