Renal cell cancer: pathologic and prognostic factors and new staging strategies

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1 ORIGINAL ARTICLE Renal cell cancer: pathologic and prognostic factors and new staging strategies Zael Santana-Ríos, Alejandro Urdiales-Ortíz, Héctor Camarena-Reynoso, Santiago Fulda-Graue, Rodrigo Pérez-Becerra, Claudio Merayo-Chalico, Víctor Hernández-Castellanos, Dorian Saavedra-Briones, Gustavo Sánchez-Turati, Gerardo Fernández-Noyola, Samuel Ahumada-Tamayo, Ángel Martínez, Alberto Camacho- Castro, Erik Muñoz-Ibarra, Francisco García-Salcido, Mauricio Cantellano-Orozco, Gustavo Morales-Montor, Sara Parraguirre, Carlos Pacheco-Gahbler Abstract Renal cell cancer has been staged using anatomical classification. After classification controversies, the Seventh Edition of the 2010 American Joint Committee on Cancer has shown changes in accordance with pathological characteristics and prognostic factors. Objective: To become familiar with clinical and pathological behavior of and prognostic factors in renal cell carcinoma, reclassifying them in accordance with 2010 Amercian Joint Committee on Cancer TNM staging. Methods: A retrospective study was carried out in which one hundred cases of renal cell cancer were reviewed in patients operated on from Their pathological characteristics, prognostic factors, and survival were analyzed and then reclassified according to 2010 American Joint Committee on Cancer TNM staging. Results: Overall survival was 74% and specific cancer survival was 8%. Poor prognosis factors were: Furhman III-IV, tumor size >10cm, vena cava Resumen El cáncer de células renales (CCR) ha sido estadificado utilizando una clasificación anatómica. Después de controversias en la estadificación, la séptima edición de la AJCC 2010 muestra cambios de acuerdo a características patológicas y factores pronósticos. Objetivo: Conocer el comportamiento clínico, patológico y factores pronósticos en CCR, reclasificándolos de acuerdo al TNM según la AJCC Métodos: Estudio retrospectivo, se revisaron 100 casos de CCR operados entre 1997 y De acuerdo a sus características patológicas se analizaron los factores pronósticos, la sobrevida y se reclasificaron con el TNM según AJCC Resultados: Supervivencia global 74% con supervivencia cáncer específica (SCE) 8%. Los factores de mal pronóstico fueron: Furhman III-IV, tamaño tumoral mayor a 10 cm, involucro de vena cava, infiltración adrenal o de ganglios linfáticos, así como presencia de metástasis (p <0.05). Fueron reclasificados 5% con TNM 2010, 5% sub estadificados y 6% sobre estadificados. Urology and Anatomical Pathology Divisions. Hospital General Dr. Manuel Gea González, SSA. Mexico City. Corresponding author: Dr. Zael Santana Ríos. Calzada de Tlalpan 4800, Col. Sección XVI. C. P Telephones: , , fax: zaelsantanar@yahoo.com. 218

2 involvement, adrenal gland or lymph node infiltration, and metastasis (P<0.05). A total of 5% were reclassified with TNM 2010, 5% were understaged and 6% were overstaged. Discussion: The importance is shown of being familiar with renal cell cancer prognostic factors and TNM staging according to the 2010 American Joint Committee on Cancer, with changes in stages T2, Ta, vascular involvement, and lymph node infiltration. Conclusions: Prognostic factors in renal cell cancer are defined in different studies and in accordance with them, recently published staging proposals were carried out. It is necessary to be familiar with the new TNM and to reclassify patients with renal cell carcinoma. Discusión: Se muestra la importancia del conocimiento de factores pronósticos en CCR y la estadificación TNM según AJCC 2010 que muestra cambios en estadios T2, Ta, involucro vascular e infiltración a ganglios linfáticos. Conclusiones: Las características pronosticas en CCR se encuentran definidas en estudios y se hicieron las propuestas para la estadificación recientemente publicada. Es necesario conocer el nuevo TNM y reclasificar a los pacientes con CCR. Palabras clave: Cáncer de células renales, supervivencia, estadificación, TNM, México. Key words: Renal cell cancer, survival, staging, TNM, Mexico. Introduction Renal cell cancer (RCC) represents % of malignant neoplasias and is the most lethal urological cancer with more than 1 thousand expected deaths in the last year. At the time of diagnosis, up to 0% of patients can present with metastatic disease, 25% with locally advanced disease, and 45% with organ-confined disease. 1, According to the international literature, the majority of these tumors are currently detected incidentally in asymptomatic patients. In contrast, in Mexico these tumors are usually detected in more advanced stages Staging depends on tumor size, invasion of adjacent structure, and vascular extension. Traditionally RCC has been staged using a purely anatomical classification. 12,1 Even though these classifications have provided us with good prognostic information, recently published data show some controversy in their regard, to the extent that the use of new classification systems has been mentioned, and especially prognostic factors that can be involved in,14-18 RCC management. In a study of 544 patients, Igor Frank et al. observed that an increase of 1 cm in tumor size increased mortality risk by 8% and tumors larger than 10 cm showed specific cancer survival reduction with a P<1. Therefore those authors proposed the T2 and T2a subclassification for tumors between 7-10 cm and the T2b subclassification for tumors larger than 10 cm. 1,14 In a study from the National Cancer Data Base (NCDB), Nese et al. reviewed 47,909 RCC cases and their pathological characteristics including tumor size. Tumors were divided into sizes of <4 cm, cm, cm and >10 cm. Accumulated survival reduction at 5 year follow-up was observed in 4 groups. 2 Leibovich et al. proposed an improvement for T classification of the 2002 TNM in relation to tumor thrombus. In a study of 675 cases of RCC he observed that patients with tumor thrombi according to Mayo Clinic classification (I, first 2 cm of the inferior vena cava; II, infradiaphragmatic vena cava; and III, supradiaphragmatic vena cava) had greater risk of dying from cancer compared with those that involved only level 0 (renal vein), with a P<01. Therefore he proposed classifying tumors with thrombi at the renal 4,17,19-22 vein level as Ta. In 2005 Thompson posed the question of whether direct invasion of the adrenal gland should continue to be classified as Ta. He studied 697 patients and observed that patients with adrenal gland invasion had a risk of death that was increased 2.9 times. He concluded that tumors with direct adrenal gland invasion behaved more aggressively than tumors with perirenal fat involvement or with renal sinus involvement. He noted a similar behavior in tumors that extended to Gerota s fascia (P=01). Therefore he proposed that adrenal gland invasion be classified as T4. 7,1,16 J. Michaelson et al. studied the prognostic significance of lymph node invasion in patients with metastatic RCC 219

3 and in 115 patients found no differences in cancerspecific mortality in patients with lymph node disease in relation to number of positive nodes. Therefore he proposed that the classification N in TNM be simplified to for positive nodes, regardless of number. 6,12 In the 2010 National Comprehensive Cancer Network (NCCN) guidelines, the Tumor, Node, Metastasis (TNM) system published in the RCC staging guidelines according to the American Joint Committee on Cancer (AJCC) in its 6th edition (2002) is observed. 11 However, in the 7th edition published in 2010, chapter IX shows the following TNM classification changes: T2 is subdivided into T2a for tumors between 7-10 cm and T2b for tumors greater than 10 cm that are confined to the kidney. Ipsilateral adrenal gland infiltration is reclassified as T4 if it is contiguous and as M1 if it is not contiguous. Renal vein involvement is reclassified as Ta and lymph node involvement is simplified to N0 and when they are positive, regardless of number, and remain as shown in Table 1. 8,9 Objective The objective of the present study was to know the clinical and pathological behavior of renal cell cancer patients that received medical attention at the Hospital General Dr. Manuel Gea González and reclassify them according to the new TNM published by the AJCC in its th edition. Methods A descriptive study was carried out that included all case records of patients diagnosed with renal cell cancer (RCC) who underwent radical nephrectomy (RN) or nephronsparing surgery (NSS) within the time frame of January 1997 to June 2010 at the Hospital General Dr. Manuel Gea González, evaluating long-term behavior in relation to pathological characteristics. All incomplete case records and those in which there was no oncological follow-up were eliminated from the study. Pathological characteristics and behavior during oncological follow-up were analyzed. The variables studied were sex, age, laterality, histological type (clear cell, papillary, tubular, granular, chromophil, collecting duct, sarcomatoid pattern, and others); Fuhrman grade (I-IV), tumor size (<4 cm, 4-7 cm, 7-10 cm, and >10 cm), renal capsule, perirenal fat, or renal sinus invasion; Gerota s capsule invasion, vascular involvement, tumor thrombi and their levels (0= renal vein, 1= first 2 cm of inferior vena cava, 2= infradiaphragmatic vena cava and = supradiaphragmatic vena cava); direct adrenal gland invasion, lymph node involvement, and distant metastasis. Table 1. TNM classification according to AJCC 2002 and T1a < 4cm T1b 4-7 cm T2 >7 cm Ta Perirenal fat AJCC 2002* AJCC 2010** Tb Infradiaphragmatic thrombus Tc Supradiaphragmatic thrombus T4 Gerota s fascia one regional lymph node N2 more than one regional lymph node Table 1.1. Clinical stages. T1a < 4cm T1b 4-7 cm T2a 7-10 cm T2 b >10 cm Ta Renal vein thrombus Perirenal fat Tb Thrombus in infradiaphragmatic cava Tc Supradiaphragmatic thrombus T4 Gerota s fascia positive lymph nodes (regardless of number) There is no N2 CLINICAL STAGE*** Stage I T1 N0 Stage II T2 N0 Stage III Stage IV T1 T2 T T T4 T4 Any T Any T *American Joint Committee on Cancer (AJCC) 6th edition, **American Joint Committee on Cancer (AJCC) 7th edition, ***NCCN 2010 N0 N0 N2 Any N M1 All cases were classified according to 2002 AJCC TNM and reclassified according to 2010 AJCC TNM and prognostic pathological characteristics and overall cancer-specific survival were described. Descriptive statistics, measures of central tendency and dispersion with Kaplan Meier curves and Log Rank test were used. Chi-square test was used for categorical survival and statistical significance was considered when P Type I error was controlled at 5%. 220

4 All procedures were carried out according to the General Health Law in Matters of Health Research guidelines. Second title, chapter I, article 17, section I, non-risk research, does not require informed consent. The study was accepted by the hospital ethics committee. Results A total of 100 cases of RCC patients that met inclusion criteria were analyzed. General characteristics of patients are listed in Table 2. Mean age was 59 years with a year range. Cases in men predominated (61% men vs 9% women). In regard to laterality there was slight predominance of the left kidney (5% left kidney vs 47% right kidney). Predominant histological type was clear cell cancer with 89%. At the time of diagnosis 10% of patients presented with metastatic disease. Mean patient follow-up was 47 months (-156) and a cut-off point at 120 months was used for survival analysis. Overall survival (OS) at 10 years was 74% and cancer-specific survival (CSS) was 8%. Overall mortality at 10 years was 6% and cancer-specific mortality was 17%. The predominant Fuhrman nuclear grade was grade II with 4%. Grades I and II had a cancer-specific survival rate of 97% in contrast to grades III and IV with a cancer-specific survival rate of 51% (P=01). In regard to size, 11% of tumors were smaller than 4 cm, 2% were between 4-7 cm, 26% were between 7-10 cm, and 40% were larger than 10 cm. Statistical analysis showed an inversely proportional tendency in relation to tumor size and disease prognosis in which greater size signified greater risk of death with a P=0.2 (Image 1). In relation to pathological characteristics of the surgical specimen, 51% were organ-confined tumors, there was renal capsule infiltration in 21%, and perirenal fat or renal sinus infiltration in 6%. Vascular involvement was observed in 12% of cases; in 9 of those cases, thrombus involved the renal vein (level 0), 2 cases involved the first 2 cm of the vena cava (level 1), and only 1 case had thrombus involving the infradiaphragmatic vena cava (level 2) (Table ). The adrenal gland was infiltrated in cases (%). There was extension to the Gerota s capsule in 4 cases (4%), and lymph node disease in % of cases (Table 2). Within the prognostic pathological characteristics, patients with organ-confined disease had cancerspecific survival rate (CSS) at 10 years of 89.4%, cases with perirenal fat infiltration had CSS of 8.5%, those Characteristic N % Total Sex M F Side Right Left Histology Clear cells Papillary Granular cells Sarcomatoid pattern Others Tumor size (cm) < >10 Infiltration level Organ-confined Capsule Perirenal fat or renal sinus Vascular involvement Gerota s fascia Lymph nodes Table 2. Pathological characteristics of study patients <4cm 4-7cm Image 1. Survival analysis in relation to tumor size cm >10cm =

5 Table. Tumor thrombi and their levels. Table 4. T 2002 and T 2010 Staging. Level N % Level 0 (renal vein) 9 75 Level 1 (IVC 2cm) Level 2 (VC infradiaphragmatic) 1 8. Level (VC supradiaphragmatic) 0 0 Thrombi total T 2002 N T 2010 N T1a 8 T1a 8 T1b 20 T1b 20 T2 4 T2a 21 T2b 21 Level 0 Level 1 Ta 11 Ta 15 Tb 14 Tb 8 Tc 0 Tc 0 T4 4 T4 7 Total 100 Total 100 p = 8 Level 2 Image 2. Survival analysis in relation to tumor thrombus level. Organ-confined Capsular inflitration Vascular involvement Perirenal fat Gerota s fascia p =0 Lympn nodes Image. Distribution and behavior in relation to infiltration level. with vascular involvement in general had CSS of 7.2% at 10 years; of those cases thrombus level was another factor that was analyzed and had mortality of.%. Thrombus level 0 (renal vein) had mortality of 15.% (n=2), tumor thrombus levels 1 and 2 (n= and n=1, respectively) had no 10-year survival, clearly demonstrating that vascular involvement of the renal vein behaves differently from other tumor thrombus levels at the vena cava level (P=8) (Image 2). In regard to adrenal gland infiltration (n=), CSS at 10 years was %, Gerota s capsule involvement had CSS of 25%, and lymph node involvement regardless of number showed CSS of only 5% at 120 months. This clearly showed that there was poorer prognosis when there was extrarenal infiltration with a P=0 (Image ). In regard to clinical stage, 28% of patients were in stage I, 4% in stage II, 25% in stage III, and 4% in stage IV (Table ). Statistical analysis showed that the more advanced the stage was the greater cancer-specific mortality there was. CSS at 10 years was near 100% in patients with clinical stage I, contrasting with CSS of 25% in patients with clinical stage IV (Images 4 and 5). When tumors were staged according to the 2002 TNM, the present authors found 8 cases in stage T1a, 20 cases in T1b, 4 cases in T2, 11 cases in Ta, 14 cases in Tb, and 4 cases in stage T4. When tumors were reclassified according to TNM 2010 there were 8 cases in T1a, 20 cases in T1b, 25 cases reclassified as T2a, 21 cases as T2b, 15 cases as Ta, 8 cases as Tb, and stage T4 increased to 7 cases (Table 4). 222

6 CLINICAL STAGE IV 4% Stage I Stage II III 25% I 28% Stage III II 4% Stage IV p =0 Image 4 and 5. Distribution and clinical behavior in relation to clinical stage T1a T1a T1b T1b T2 T2a T2b Ta Ta Tb Tb Tc Tc T4 T4 TMN 2002 TMN2010 Image 6. Comparison of and changes in 2002 and 2010 TNM staging. From the case total, 5% of patients were reclassified according to the new 2010 TNM, and 5% were understaged and 6% were overstaged. The remaining 42% were subclassifications corresponding to the new T2 tumor classification (Image 6). Discussion This work shows the importance of being familiar with prognostic pathological factors for RCC in relation to its long-term behavior. Histological type, Fuhrman nuclear grade, tumor size, and infiltration level of the tumor are factors that have an impact on patient survival. With these data the following prognosis factors in the present cases can be established: the presence of sarcomatoid pattern, high Fuhrman grade (III or IV), tumor size >10 cm, vena cava involvement, adrenal gland infiltration, lymph node disease, and metastasis at the time of diagnosis. 22

7 This is where the importance lies of being familiar with the new TNM staging according to the AJCC 7th edition (2010), because in the present study population 5% of patients were reclassified; 42% were subclassified according to the new T2 classification, 5% were understaged, and 6% were overstaged, all of which has prognostic implications for these patients. Conclusions Prognostic pathological characteristics in RCC are defined in different studies and taking them into account, new recently published staging was proposed. It is necessary to be familiar with the new TNM for RCC and each center should reclassify RCC patients in order to evaluate the prognostic impact of the disease. Bibliography 1. Igor F, Michael LB, et al. pt2 classification for renal cell carcinoma. Can its accuracy be improved? J Urol 2005;17: Nese N, Gladell P Paner, et al. Renal cell carcinoma: Assessment of key pathologic prognostic parameters and patient characteristics in cases using the national cancer data base. Ann Diagn Pathol 2009;1:1-8. Lahm JS, Oleg S, et al. Renal cell carcinoma 2005: New frontiers in staging, prognostication and targeted molecular therapy. J Urol 2005;17: Leibovich B, Cheville J, et al. Cancer specific survival for patients with pt renal cell carcinoma Can the 2002 primary tumor classification be improved? J Urol 2005;17: Bukowsky R, et al. Prognostic factors for survival in metastasic renal cell carcinoma. Cancer 2009;115(10Suppl): Michaelson J, Chen LL, et al. How cancer at the primary site and in the lymph nodes contributes to the risk of cancer death. Cancer 2009;115: Thompson H, Bradley, L, et al. Should direct ipsilateral adrenal invasion from renal cell carcinoma be classified as pta? J Urol. 2005;17: American Joint Comitee on Cancer (AJCC), 6th Ed. Cap. 4, Kidney American Joint Comitee on Cancer (AJCC), 7a Ed. Cap 4, Kidney. 2010;pp: Campbell SC, Novick AC, Bukowsky. Renal Tumors. Campbell-Walsh. Urology 9a Ed. Chapter 46. Elsevier; National Comprehensive Cancer Network (NCCN). Practice Guidelines in Oncology; Dimashkieh H, Lohse, et al. Extranodal extension in regional lymph nodes is associated with outcome in patients with renal cell carcinoma. J Urol 2006;176: Han KR, Bui MH, et al. TNM Ta Renal cell carcinoma: adrenal gland involvement is not the same as renal fat invasion. J Urol 200;169: Klatte T, Patard JJ, et al. Prognostic impact of tumor size on pt2 renal cell carcinoma: An international multicenter experience. J Urol 2007;178:5-40; 15. Kontak JA, Campbell SC. Prognostic factors in renal cell carcinoma. Urol Clin North Am 200;0: Lam JS, Patard JJ, et al. Prognostic significance of Ta renal cell carcinoma with adrenal gland involvement: An international multicenter experience. Eur Urol 2007;52: Moinzadeh RJ, Mazumar M. Prognostic significance of tumor thrombus level in patients with renal cell carcinoma and venous tumor thrombus extension. Is all Tb the same? J Urol 2004;171(2Pt1): Nguyen C, Campbell SC, et al. Staging of renal cell carcinoma: Past, present and future. Clin Genitourin Cancer 2006;5: Pantuck AJ, Zisman A, et al. Renal cell carcinoma with retroperitoneal lymph nodes. Impact on survival and benefits of inmunotherapy. Cancer 200;97: Patard JJ, Kim HL, Lam JS, et al. Use of University of California-Los Angeles integrated staging system to predict survival in renal cell carcinoma: An international multicenter study. J Clin Oncol 2004;22: Phillips CK, Taneja SS, et al. The role of lymphadenectomy in the surgical management of renal cell carcinoma. Urol Oncol 2004;22: Thompson R, Cheville J, et al. Reclassification of patients with pt and pt4 renal cell carcinoma improves prognostic accuracy. Cancer 2005;104:

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