REVIEW
Staging of prostate cancer
Liang Cheng,
Rodolfo Montironi,
David G Bostwick, Antonio Lopez-Beltran,
Daniel M Berney,
Liang Cheng
Departments of Pathology and Laboratory Medicine
Urology, Indiana University School of Medicine, Indianapolis, IN, USA
Search for more papers by this authorRodolfo Montironi
Institute of Pathological Anatomy and Histopathology, Polytechnic University of the Marche Region (Ancona), United Hospitals, Ancona, Italy
Search for more papers by this authorAntonio Lopez-Beltran
Department of Pathology, Cordoba University, Cordoba, Spain
Search for more papers by this authorDaniel M Berney
Department of Medical Oncology, Barts Cancer Centre, Barts and the London School of Medicine and Dentistry, London, UK
Search for more papers by this authorLiang Cheng,
Rodolfo Montironi,
David G Bostwick, Antonio Lopez-Beltran,
Daniel M Berney,
Liang Cheng
Departments of Pathology and Laboratory Medicine
Urology, Indiana University School of Medicine, Indianapolis, IN, USA
Search for more papers by this authorRodolfo Montironi
Institute of Pathological Anatomy and Histopathology, Polytechnic University of the Marche Region (Ancona), United Hospitals, Ancona, Italy
Search for more papers by this authorAntonio Lopez-Beltran
Department of Pathology, Cordoba University, Cordoba, Spain
Search for more papers by this authorDaniel M Berney
Department of Medical Oncology, Barts Cancer Centre, Barts and the London School of Medicine and Dentistry, London, UK
Search for more papers by this authorL Cheng, Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, 350 West 11th Street, Room 4010, Indianapolis, IN 46202, USA. e-mail: [email protected]
Abstract
Cheng L, Montironi R, Bostwick D G, Lopez-Beltran A & Berney D M (2012) Histopathology 60, 87–117 Staging of prostate cancer
Prostatic carcinoma (PCa) is a significant cause of cancer morbidity and mortality worldwide. Accurate staging is critical for prognosis assessment and treatment planning for PCa. Despite the large volume of clinical activity and research, the challenge to define the most appropriate and clinically relevant staging system remains. The pathologically complex and uncertain clinical course of prostate cancer further complicates the design of staging classification and a substaging system suitable for individualized care. This review will focus on recent progress and controversial issues related to prostate cancer staging. The 2010 revision of the American Joint Committee on Cancer/Union Internationale Contre le Cancer (AJCC/UICC) tumour, node and metastasis (TNM) system is the most widely used staging system at this time. Despite general acceptance of the system as a whole, there is controversy and uncertainty about its application, particularly for T2 subclassification. The three-tiered T2 classification system for organ-confined prostate cancer is superfluous, considering the biology and anatomy of PCa. A tumour size-based substaging system may be considered in the future TNM subclassification of pT2 cancer. Lymph node status is one of the most important prognostic factors for prostate cancer. Nevertheless, clinical outcomes in patients with positive lymph nodes are variable. Identification of patients at the greatest risk of systemic progression helps in the selection of appropriate therapy. The data suggest that the inherent aggressiveness of metastatic prostate cancer is closely linked to the tumour volume of lymph node metastasis. We recommend that a future TNM staging system should consider subclassification of node-positive cancer on the basis of nodal cancer volume, using the diameter of the largest nodal metastasis and/or the number of positive nodes.
References
- 1 Siegel R , Ward E , Brawley O , Jemal A . Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths . CA Cancer J. Clin. 2011 ; 61 ; 212 – 236 .
- 2 Beahrs OH , Henson DE , Hutter RVP , Kennedy BJ . American Joint Committee on Cancer staging manual for staging of cancer , 4th edn . Philadelphia, PA : Lippincott , 1992 .
- 3 Edge S , Byrd DR , Compton CC et al. American Joint Committee on Cancer staging manual , 7th edn . New York : Springer , 2010 .
- 4 Cheng L , Song SY , Pretlow TG et al. Evidence of independent origin of multiple tumors from patients with prostate cancer . J. Natl Cancer Inst. 1998 ; 90 ; 233 – 237 .
- 5
Ohori M
,
Wheeler TM
,
Scardino PT
.
The New American Joint Committee on Cancer and International Union Against Cancer TNM classification of prostate cancer. Clinicopathologic correlations
.
Cancer
1994
;
74
;
104
–
114
.
10.1002/1097-0142(19940701)74:1<104::AID-CNCR2820740119>3.0.CO;2-5 CAS PubMed Web of Science® Google Scholar
- 6 Montie JE . Staging prostate cancer: current TNM classification and future prospects for prognostic factors . Cancer (Suppl.) 1994 ; 75 ; 1814 – 1818 .
- 7 Andreoiu M , Cheng L . Multifocal prostate cancer: biologic, prognostic, and therapeutic implications . Hum. Pathol. 2010 ; 41 ; 781 – 793 .
- 8 Campbell T , Blasko J , Crawford ED et al. Clinical staging of prostate cancer: reproducibility and clarification of issues . Int. J. Cancer 2001 ; 96 ; 198 – 209 .
- 9 Abdellaoui A , Iyengar S , Freeman S . Imaging in prostate cancer . Future Oncol. 2011 ; 7 ; 679 – 691 .
- 10 Heidenreich A , Bellmunt J , Bolla M et al. EAU guidelines on prostate cancer. Part 1: screening, diagnosis, and treatment of clinically localised disease . Eur. Urol. 2011 ; 59 ; 61 – 71 .
- 11
Grignon DJ
,
Sakr WA
.
Pathologic staging of prostate carcinoma: what are the issues?
Cancer
1996
;
78
;
337
–
340
.
10.1002/(SICI)1097-0142(19960715)78:2<337::AID-CNCR23>3.0.CO;2-W PubMed Web of Science® Google Scholar
- 12 Bostwick DG , Myers RP , Oesterling JE . Staging of prostate cancer . Semin. Surg. Oncol. 1994 ; 10 ; 60 – 72 .
- 13 Descazeaud A , Peyromaure M , Salin A et al. Predictive factors for progression in patients with clinical stage T1a prostate cancer in the PSA era . Eur. Urol. 2008 ; 53 ; 355 – 361 .
- 14 Cheng L , Neumann RM , Blute ML , Zincke H , Bostwick DG . Long-term follow-up of untreated stage T1a prostate cancer . J. Natl Cancer Inst. 1998 ; 90 ; 1105 – 1107 .
- 15
Cheng L
,
Bergstralh EJ
,
Scherer BG
et al.
Predictors of cancer progression in T1a prostate adenocarcinoma
.
Cancer
1999
;
85
;
1300
–
1304
.
10.1002/(SICI)1097-0142(19990315)85:6<1300::AID-CNCR12>3.0.CO;2-# CAS PubMed Web of Science® Google Scholar
- 16 Rajab R , Fisher G , Kattan MW et al. An improved prognostic model for stage T1a and T1b prostate cancer by assessments of cancer extent . Mod. Pathol. 2011 ; 24 ; 58 – 63 .
- 17 Capitanio U . Contemporary management of patients with T1a and T1b prostate cancer . Curr. Opin. Urol. 2011 ; 21 ; 252 – 256 .
- 18 Cantrell BB , DeKlerk DP , Eggleston JC , Boitnott JK , Walsh PC . Pathological factors that influence prognosis in stage A prostatic cancer: the influence of extent versus grade . J. Urol. 1981 ; 125 ; 516 – 520 .
- 19 Koch MO , Gardner T , Cheng L , Fedewa RJ , Seip R , Sanghvi NT . Phase I/II trial of high intensity focused ultrasound for the treatment of previously untreated localized prostate cancer . J. Urol. 2007 ; 178 ; 2366 – 2371 .
- 20 Kattan MW , Wheeler TM , Scardino PT . Postoperative nomogram for disease recurrence after radical prostatectomy for prostate cancer . J. Clin. Oncol. 1999 ; 17 ; 1499 – 1507 .
- 21 Partin AW , Mangold LA , Lamm DM , Walsh PC , Epstein JI , Pearson JD . Contemporary update of prostate cancer staging nomograms (Partin Tables) for the new millennium . Urology 2001 ; 58 ; 843 – 848 .
- 22 Loeb S , Roehl KA , Helfand BT , Catalona WJ . Complications of open radical retropubic prostatectomy in potential candidates for active monitoring . Urology 2008 ; 72 ; 887 – 891 .
- 23
Douglas TH
,
McLeod DG
,
Mostofi FK
et al.
Prostate-specific antigen-detected prostate cancer (stage T1c): an analysis of whole-mount prostatectomy specimens
.
Prostate
1997
;
32
;
59
–
64
.
10.1002/(SICI)1097-0045(19970615)32:1<59::AID-PROS8>3.0.CO;2-7 CAS PubMed Web of Science® Google Scholar
- 24 Armatys S , Koch MO , Bihrle R , Gardner TA , Cheng L . Is it necessary to separate clinical stage T1c from T2 prostate adenocarcinoma? BJU Int. 2005 ; 96 ; 777 – 780 .
- 25 Furuya Y , Ohta S , Sato N , Kotake T , Masai M . Comparison of T1c versus T2 prostate cancers in Japanese patients undergoing radical prostatectomy . Int. Urol. Nephrol. 2002 ; 33 ; 73 – 76 .
- 26 Cookson MS , Fleshner NE , Soloway SM , Fair WR . Prognostic significance of prostate-specific antigen in stage T1c prostate cancer treated by radical prostatectomy . Urology 1997 ; 49 ; 887 – 893 .
- 27 Oesterling JE , Suman VJ , Zincke H , Bostwick DG . PSA-detected (clinical stage T1c or B0) prostate cancer. Pathologically significant tumors . Urol. Clin. North Am. 1993 ; 20 ; 687 – 693 .
- 28 Matthews GJ , Fracchia JA . PSA-detected prostate cancer: contrasts with palpable disease . J. Surg. Oncol. 1995 ; 59 ; 28 – 30 .
- 29 Stamey TA , Donaldson AN , Yemoto CE , McNeal JE , Sozen S , Gill H . Histological and clinical findings in 896 consecutive prostates treated only with radical retropubic prostatectomy: epidemiologic significance of annual changes . J. Urol. 1998 ; 160 ; 2412 – 2417 .
- 30 Ramos CG , Carvalhal GF , Smith DS , Mager DE , Catalona WJ . Clinical and pathological characteristics, and recurrence rates of stage T1c versus T2a or T2b prostate cancer . J. Urol. 1999 ; 161 ; 1525 – 1529 .
- 31 Freedland SJ , Presti JCJ , Terris MK et al. Improved clinical staging system combining biopsy laterality and TNM stage for men with T1c and T2 prostate cancer: results from the SEARCH database . J. Urol. 2003 ; 171 ; 1246 – 1247 .
- 32 Lerner SE , Seay TM , Blute ML , Bergstralh EJ , Barrett D , Zincke H . Prostate-specific antigen detected prostate cancer (clinical stage T1c): an interim analysis . J. Urol. 1996 ; 1996 ; 821 – 826 .
- 33 Ghavamian R , Blute ML , Bergstralh EJ , Slezak J , Zincke H . Comparison of clinically nonpalpable prostate-specific antigen-detected (cT1c) versus palpable (cT2) prostate cancers in patients undergoing radical retropubic prostatectomy . Urology 1999 ; 54 ; 105 – 110 .
- 34 Obek C , Louis P , Civantos F , Soloway MS . Comparison of digital rectal examination and biopsy results with the radical prostatectomy specimen . J. Urol. 1999 ; 161 ; 494 – 498 .
- 35 Buyyounouski MK , Horwitz EM , Hanlon AL , Uzzo RG , Hanks GE , Pollack A . Positive prostate biopsy laterality and implications for staging . Urology 2003 ; 62 ; 298 – 303 .
- 36 Eichelberger LE , Cheng L . Does pT2b prostate carcinoma exist? Critical appraisal of the 2002 TNM classification of prostate carcinoma . Cancer 2004 ; 100 ; 2573 – 2576 .
- 37 Han M , Walsh PC , Partin AW , Rodriguez R . Ability of the 1992 and 1997 American Joint Committee on Cancer Staging Systems for prostate cancer to predict progression-free survival after radical prostatectomy for stage T2 disease . J. Urol. 2000 ; 164 ; 89 – 92 .
- 38
Iyer RV
,
Hanlon AL
,
Pinover WH
,
Hanks GE
.
Outcome evaluation of the 1997 American Joint Committee on Cancer staging system for prostate carcinoma treated by radiation therapy
.
Cancer
1999
;
85
;
1816
–
1821
.
10.1002/(SICI)1097-0142(19990415)85:8<1816::AID-CNCR23>3.0.CO;2-U CAS PubMed Web of Science® Google Scholar
- 39 Cagiannos I , Graefen M , Karakiewicz PI et al. Analysis of clinical stage T2 prostate cancer: do current subclassifications represent an improvement? J. Clin. Oncol. 2002 ; 20 ; 2025 – 2030 .
- 40 Kordan Y , Chang SS , Salem S et al. Pathological stage T2 subgroups to predict biochemical recurrence after prostatectomy . J. Urol. 2009 ; 182 ; 2291 – 2295 .
- 41 Chun FK , Briganti A , Lebeau T et al. The 2002 AJCC pT2 substages confer no prognostic information on the rate of biochemical recurrence after radical prostatectomy . Eur. Urol. 2006 ; 49 ; 273 – 278 ; discussion 78–79 .
- 42 Cheng L , Jones TD , Pan CX , Barbarin A , Eble JN , Koch MO . Anatomic distribution and pathologic characterization of small volume prostate cancer (<0.5 ml) in whole-mount prostatectomy specimens . Mod. Pathol. 2005 ; 18 ; 1022 – 1026 .
- 43 Cheng L , Poulos CK , Pan CX et al. Preoperative prediction of small volume cancer (less than 0.5 ml) in radical prostatectomy specimens . J. Urol. 2005 ; 174 ; 898 – 902 .
- 44 Greene DR , Wheeler TM , Egawa S , Weaver RP , Scardino PT . Relationship between clinical stage and histological zone of origin in early prostate cancer: morphometric analysis . Br. J. Urol. 1991 ; 68 ; 499 – 509 .
- 45
Villers A
,
McNeal JE
,
Freiha FS
,
Stamey TA
.
Multiple cancers in the prostate
.
Cancer
1992
;
70
;
2313
–
2318
.
10.1002/1097-0142(19921101)70:9<2313::AID-CNCR2820700917>3.0.CO;2-T CAS PubMed Web of Science® Google Scholar
- 46
Bostwick DG
,
Shan A
,
Qian J
et al.
Independent origin of multiple foci of prostatic intraepithelial neoplasia: comparison with matched foci of prostate carcinoma
.
Cancer
1998
;
83
;
1995
–
2002
.
10.1002/(SICI)1097-0142(19981101)83:9<1995::AID-CNCR16>3.0.CO;2-2 CAS PubMed Web of Science® Google Scholar
- 47 Masterson TA , Cheng L , Mehan RM , Koch MO . Tumor focality does not predict biochemical recurrence after radical prostatectomy in men with clinically localized prostate cancer . J. Urol. 2011 ; 186 ; 506 – 510 .
- 48 Masterson TA , Cheng L , Koch MO . Pathological characterization of unifocal prostate cancers in whole-mount radical prostatectomy specimens . BJU Int. 2010 ; 107 ; 1587 – 1591 .
- 49 Eichelberger LE , Koch MO , Daggy JK , Ulbright TM , Eble JN , Cheng L . Predicting tumor volume in radical prostatectomy specimens from patients with prostate cancer . Am. J. Clin. Pathol. 2003 ; 120 ; 386 – 391 .
- 50 Eichelberger LE , Koch MO , Eble JN , Ulbright TM , Juliar BE , Cheng L . Maximum tumor diameter is an independent predictor of prostate specific antigen recurrence in prostate cancer . Mod. Pathol. 2005 ; 18 ; 886 – 890 .
- 51 Marks RA , Lin H , Koch MO , Cheng L . Positive-block ratio in radical prostatectomy specimens is an independent predictor of prostate-specific antigen recurrence . Am. J. Surg. Pathol. 2007 ; 31 ; 311 – 318 .
- 52
Cheng L
,
Darson MF
,
Bergstralh EJ
,
Slezak J
,
Myers RP
,
Bostwick DG
.
Correlation of margin status and extraprostatic extension with progression of prostate carcinoma
.
Cancer
1999
;
86
;
1775
–
1782
.
10.1002/(SICI)1097-0142(19991101)86:9<1775::AID-CNCR20>3.0.CO;2-L CAS PubMed Web of Science® Google Scholar
- 53 McNeal JE , Bostwick DG , Kindrachuk RA , Redwine EA , Freiha FS , Stamey TA . Patterns of progression in prostate cancer . Lancet 1986 ; 1 ; 60 – 63 .
- 54 Ohori M , Wheeler TM , Kattan MW , Goto Y , Scardino PT . Prognostic significance of positive surgical margins in radical prostatectomy specimens . J. Urol. 1995 ; 154 ; 1818 – 1824 .
- 55 Epstein JI , Partin AW , Sauvageot J , Walsh PC . Prediction of progression following radical prostatectomy. A multivariate analysis of 721 men with long-term follow-up . Am. J. Surg. Pathol. 1996 ; 20 ; 286 – 292 .
- 56 Bostwick DG . Staging prostate cancer – 1997: current methods and limitations . Eur. Urol. 1997 ; 32 ; 2 – 14 .
- 57 Ayala AG , Ro JY , Babaian R , Troncoso P , Grignon DJ . The prostatic capsule: does it exist? Its importance in the staging and treatment of prostatic carcinoma . Am. J. Surg. Pathol. 1989 ; 13 ; 21 – 27 .
- 58
Sakr WA
,
Wheeler TM
,
Blute M
et al.
Staging and reporting of prostate cancer – sampling of the radical prostatectomy specimen
.
Cancer
1996
;
78
;
366
–
368
.
10.1002/(SICI)1097-0142(19960715)78:2<366::AID-CNCR29>3.0.CO;2-T CAS PubMed Web of Science® Google Scholar
- 59 Hong H , Koch MO , Foster RS , Bihrle R , Gardner TA , Fyffe J . Anatomic distribution of periprostatic adipose tissue: a mapping study of 100 radical prostatectomy specimens . Cancer 2003 ; 97 ; 1639 – 1643 .
- 60 Blute ML , Bostwick DG , Bergstralh EJ et al. Anatomic site-specific positive margins in organ-confined prostate cancer and its impact on outcome after radical prostatectomy . Urology 1997 ; 50 ; 733 – 739 .
- 61 Fesseha T , Sakr W , Grignon D , Banerjee M , Wood DP , Pontes JE . Prognostic implications of a positive apical margin in radical prostatectomy specimens . J. Urol. 1997 ; 158 ; 2176 – 2179 .
- 62 Wieder JA , Soloway MS . Incidence, etiology, location, prevention and treatment of positive surgical margins after radical prostatectomy for prostate cancer . J. Urol. 1998 ; 160 ; 299 – 315 .
- 63 Tan PH , Cheng L , Srigley JR et al. International Society of Urological Pathology (ISUP) Consensus Conference on Handling and Staging of Radical Prostatectomy Specimens. Working group 5: surgical margins . Mod. Pathol. 2011 ; 24 ; 48 – 57 .
- 64 Magi-Galluzzi C , Evans AJ , Delahunt B et al. International Society of Urological Pathology (ISUP) Consensus Conference on Handling and Staging of Radical Prostatectomy Specimens. Working group 3: extraprostatic extension, lymphovascular invasion and locally advanced disease . Mod. Pathol. 2011 ; 24 ; 26 – 38 .
- 65 Epstein JI , Carmichael MJ , Pizov G , Walsh PC . Influence of capsular penetration on progression following radical prostatectomy: a study of 196 cases with long-term followup . J. Urol. 1993 ; 150 ; 135 – 141 .
- 66 Steuber T , Erbersdobler A , Graefen M , Haese A , Huland H , Karakiewicz PI . Comparative assessment of the 1992 and 2002 pathologic T3 substages for the prediction of biochemical recurrence after radical prostatectomy . Cancer 2006 ; 106 ; 775 – 782 .
- 67
Zagars GK
,
Geara FB
,
Pollack A
,
von Eschenbach AC
.
The T classification of clinically localized prostate cancer. An appraisal based on disease outcome after radiation therapy
.
Cancer
1994
;
73
;
1904
–
1912
.
10.1002/1097-0142(19940401)73:7<1904::AID-CNCR2820730722>3.0.CO;2-6 CAS PubMed Web of Science® Google Scholar
- 68 May F , Hartung R , Breul J . The ability of the American Joint Committee on Cancer Staging system to predict progression-free survival after radical prostatectomy . BJU Int. 2001 ; 88 ; 702 – 707 .
- 69 Sung MT , Lin H , Koch MO , Davidson DD , Cheng L . Radial distance of extraprostatic extension measured by ocular micrometer is an independent predictor of prostate-specific antigen recurrence: a new proposal for the substaging of pT3a prostate cancer . Am. J. Surg. Pathol. 2007 ; 31 ; 311 – 318 .
- 70 Wheeler TM , Dillioglugil O , Kattan MW et al. Clinical and pathological significance of the level and extent of capsular invasion in clinical stage T1–2 prostate cancer . Hum. Pathol. 1998 ; 29 ; 856 – 862 .
- 71 Poulos CK , Koch MO , Eble JN , Daggy JK , Cheng L . Bladder neck invasion is an independent predictor of prostate-specific antigen recurrence . Cancer 2004 ; 101 ; 1563 – 1568 .
- 72 Pierorazio PM , Epstein JI , Humphreys E , Han M , Walsh PC , Partin AW . The significance of a positive bladder neck margin after radical prostatectomy: the American Joint Committee on Cancer Pathological Stage T4 designation is not warranted . J. Urol. 2010 ; 183 ; 151 – 157 .
- 73 Zhou M , Reuther AM , Levin HS et al. Microscopic bladder neck involvement by prostate carcinoma in radical prostatectomy specimens is not a significant independent prognostic factor . Mod. Pathol. 2009 ; 22 ; 385 – 392 .
- 74 Yossepowitch O , Engelstein D , Konichezky M , Sella A , Livne PM , Baniel J . Bladder neck involvement at radical prostatectomy: positive margins or advanced T4 disease? Urology 2000 ; 56 ; 448 – 452 .
- 75 Yossepowitch O , Sircar K , Scardino PT et al. Bladder neck involvement in pathologic stage pT4 radical prostatectomy specimens is not an independent prognostic factor . J. Urol. 2002 ; 168 ; 2011 – 2015 .
- 76 Dash A , Sanda MG , Yu M , Taylor JMG , Fecko A , Rubin MA . Prostate cancer involving the bladder neck: recurrence free survival and implications for AJCC staging modification . Urology 2002 ; 60 ; 276 – 280 .
- 77 Obek C , Sadek S , Lai S , Civantos F , Rubinowicz D , Soloway MS . Positive surgical margins with radical retropubic prostatectomy: anatomic site-specific pathologic analysis and impact on prognosis . Urology 1999 ; 54 ; 682 – 688 .
- 78 Berney DM , Wheeler TM , Grignon DJ et al. International Society of Urological Pathology (ISUP) Consensus Conference on Handling and Staging of Radical Prostatectomy Specimens. Working group 4: seminal vesicles and lymph nodes . Mod. Pathol. 2011 ; 24 ; 39 – 47 .
- 79 Ohori M , Scardino PT , Lapin SL , Seale-Hawkins C , Link J , Wheeler TM . The mechanisms and prognostic significance of seminal vesicle involvement by prostate cancer . Am. J. Pathol. 1993 ; 17 ; 1252 – 1261 .
- 80 Epstein JI , Partin AW , Potter SR , Walsh PC . Adenocarcinoma of the prostate invading the seminal vesicle: prognostic stratification based on pathologic parameters . Urology 2000 ; 56 ; 283 – 288 .
- 81 Billis A , Teixeira DA , Stelini RF , Quintal MM , Guimaraes MS , Ferreira U . Seminal vesicle invasion in radical prostatectomies: which is the most common route of invasion? Int. Urol. Nephrol. 2007 ; 39 ; 1097 – 1102 .
- 82 Yamadori K , Uda R , Oka M , Son H , Akatsuka M , Watsuji T . Anesthetic management for high-intensity focused ultrasound (HIFU) therapy in prostate cancer patients . Masui 2007 ; 56 ; 446 – 449 .
- 83 Pierorazio PM , Ross AE , Schaeffer EM et al. A contemporary analysis of outcomes of adenocarcinoma of the prostate with seminal vesicle invasion (pT3b) after radical prostatectomy . J. Urol. 2011 ; 185 ; 1691 – 1697 .
- 84 Fleming ID , Cooper JS , Henson DE et al. AJCC cancer staging manual . Philadelphia, PA : Lippincott Raven , 1997 .
- 85 Greene FL , Page DL , Flemming ID et al. AJCC cancer staging manual , 6th edn . New York : Springer-Verlag , 2002 .
- 86 Hsiao W , Moses KA , Goodman M , Jani AB , Rossi PJ , Master VA . Stage IV prostate cancer: survival differences in clinical T4, nodal and metastatic disease . J. Urol. 2010 ; 184 ; 512 – 518 .
- 87 Goldstein NS , Begin LR , Grody WW , Novak JM , Qian J , Bostwick DG . Minimal or no cancer in radical prostatectomy specimens. Report of 13 cases of the ‘vanishing cancer phenomenon’ . Am. J. Surg. Pathol. 1995 ; 19 ; 1002 – 1009 .
- 88 Gross JL , Masterson TA , Cheng L , Johnstone PA . pT0 prostate cancer after radical prostatectomy . J. Surg. Oncol. 2010 ; 102 ; 331 – 333 .
- 89 Montironi R , Cheng L , Lopez-Beltran A et al. Stage pT0 in radical prostatectomy with no residual carcinoma and with a previous positive biopsy conveys a wrong message to clinicians and patients: why is cancer not present in the radical prostatectomy specimen? Eur. Urol. 2009 ; 56 ; 272 – 274 .
- 90 Descazeaud A , Zerbib M , Flam T , Vieillefond A , Debre B , Peyromaure M . Can pT0 stage of prostate cancer be predicted before radical prostatectomy? Eur. Urol. 2006 ; 50 ; 1248 – 1252 ; discussion 53 .
- 91 Bostwick DG , Bostwick KC . ‘Vanishing’ prostate cancer in radical prostatectomy specimens: incidence and long-term follow-up in 38 cases . BJU Int. 2004 ; 94 ; 57 – 58 .
- 92 Cao D , Hafez M , Berg K , Murphy K , Epstein JI . Little or no residual prostate cancer at radical prostatectomy: vanishing cancer or switched specimen?: a microsatellite analysis of specimen identity . Am. J. Surg. Pathol. 2005 ; 29 ; 467 – 473 .
- 93 Humphrey PA . Complete histologic serial sectioning of a prostate gland with adenocarcinoma . Am. J. Surg. Pathol. 1993 ; 17 ; 468 – 472 .
- 94 von Bodman C , Godoy G , Chade DC et al. Predicting biochemical recurrence-free survival for patients with positive pelvic lymph nodes at radical prostatectomy . J. Urol. 2010 ; 184 ; 143 – 148 .
- 95 Messing EM , Manola J , Yao J et al. Immediate versus deferred androgen deprivation treatment in patients with node-positive prostate cancer after radical prostatectomy and pelvic lymphadenectomy . Lancet Oncol. 2006 ; 7 ; 472 – 479 .
- 96 Boormans JL , Wildhagen MF , Bangma CH , Verhagen PC , van Leenders GJ . Histopathological characteristics of lymph node metastases predict cancer-specific survival in node-positive prostate cancer . BJU Int. 2008 ; 102 ; 1589 – 1593 .
- 97 Ghavamian R , Bergstralh EJ , Blute ML , Slezak J , Zincke H . Radical retropubic prostatectomy plus orchiectomy versus orchiectomy alone for pTxN+ prostate cancer: a matched comparison . J. Urol. 1999 ; 161 ; 1223 – 1228 .
- 98
Zincke H
.
Is long-term survival possible with external beam irradiation for stage D1 adenocarcinoma of the prostate?
Cancer
1992
;
70
;
2742
–
2743
.
10.1002/1097-0142(19921201)70:11<2742::AID-CNCR2820701129>3.0.CO;2-E CAS PubMed Web of Science® Google Scholar
- 99
Zincke H
,
Bergstralh EJ
,
Larson-Keller JJ
et al.
Stage D1 prostate cancer treated by radical prostatectomy and adjuvant hormonal treatment: evidence for favorable survival in patients with DNA diploid tumors
.
Cancer
1992
;
70
;
311
–
323
.
10.1002/1097-0142(19920701)70:1+<311::AID-CNCR2820701320>3.0.CO;2-T CAS PubMed Web of Science® Google Scholar
- 100 Cheng L , Bergstralh EJ , Cheville JC et al. Cancer volume of lymph node metastasis predicts progression in prostate cancer . Am. J. Surg. Pathol. 1998 ; 22 ; 1491 – 1500 .
- 101
Cheng L
,
Slezak J
,
Bergstralh EJ
et al.
Dedifferentiation in the metastatic progression of prostate cancer
.
Cancer
1999
;
86
;
657
–
663
.
10.1002/(SICI)1097-0142(19990815)86:4<657::AID-CNCR15>3.0.CO;2-9 CAS PubMed Web of Science® Google Scholar
- 102
Cheng L
,
Leibovich BC
,
Bergstralh EJ
et al.
p53 alteration in regional lymph node metastases from prostate carcinoma: a marker for progression?
Cancer
1999
;
85
;
2455
–
2459
.
10.1002/(SICI)1097-0142(19990601)85:11<2455::AID-CNCR22>3.0.CO;2-C CAS PubMed Web of Science® Google Scholar
- 103
Cheng L
,
Bostwick DG
,
Li G
et al.
Allelic imbalance in the clonal evolution of prostate carcinoma
.
Cancer
1999
;
85
;
2017
–
2022
.
10.1002/(SICI)1097-0142(19990501)85:9<2017::AID-CNCR20>3.0.CO;2-V CAS PubMed Web of Science® Google Scholar
- 104 Cheng L , Zincke H , Blute ML , Bergstralh EJ , Scherer B , Bostwick DG . Risk of prostate carcinoma death in patients with lymph node metastasis . Cancer 2001 ; 91 ; 66 – 73 .
- 105 Briganti A , Karnes RJ , Da Pozzo LF et al. Combination of adjuvant hormonal and radiation therapy significantly prolongs survival of patients with pT2-4 pN+ prostate cancer: results of a matched analysis . Eur. Urol. 2011 ; 59 ; 832 – 840 .
- 106 Briganti A , Karnes JR , Da Pozzo LF et al. Two positive nodes represent a significant cut-off value for cancer specific survival in patients with node positive prostate cancer. A new proposal based on a two-institution experience on 703 consecutive N+ patients treated with radical prostatectomy, extended pelvic lymph node dissection and adjuvant therapy . Eur. Urol. 2009 ; 55 ; 261 – 270 .
- 107 Alexander RE , Sung MT , Cheng L . Lymphadenectomy in urologic oncology: pathologic considerations . Urol. Clin. North Am. 2011 ; 38 ; 483 – 495 .
- 108 Sung MT , Cheng L . Contemporary approaches for processing and handling of radical prostactomy specimens . Histol. Histopathol. 2010 ; 25 ; 259 – 265 .
- 109 Montironi R , Cheng L , Lopez-Beltran A et al. Joint appraisal of the radical prostatectomy specimen by the urologist and the uropathologist: together, we can do it better . Eur. Urol. 2009 ; 56 ; 951 – 955 .
- 110 Briganti A , Blute ML , Eastham JH et al. Pelvic lymph node dissection in prostate cancer . Eur. Urol. 2009 ; 55 ; 1251 – 1265 .
- 111 Masterson TA , Bianco FJ Jr , Vickers AJ et al. The association between total and positive lymph node counts, and disease progression in clinically localized prostate cancer . J. Urol. 2006 ; 175 ; 1320 – 1324 ; discussion 24–25 .
- 112 Touijer K , Eastham JA , Secin FP et al. Comprehensive prospective comparative analysis of outcomes between open and laparoscopic radical prostatectomy conducted in 2003 to 2005 . J. Urol. 2008 ; 179 ; 1811 – 1817 .
- 113 Touijer K , Rabbani F , Otero JR et al. Standard versus limited pelvic lymph node dissection for prostate cancer in patients with a predicted probability of nodal metastasis greater than 1% . J. Urol. 2007 ; 178 ; 120 – 124 .
- 114 Heidenreich A , Varga Z , Von Knobloch R . Extended pelvic lymphadenectomy in patients undergoing radical prostatectomy: high incidence of lymph node metastasis . J. Urol. 2002 ; 167 ; 1681 – 1686 .
- 115 Allaf ME , Palapattu GS , Trock BJ , Carter HB , Walsh PC . Anatomical extent of lymph node dissection: impact on men with clinically localized prostate cancer . J. Urol. 2004 ; 172 ; 1840 – 1844 .
- 116 Weingartner K , Ramaswamy A , Bittinger A , Gerharz EW , Voge D , Riedmiller H . Anatomical basis for pelvic lymphadenectomy in prostate cancer: results of an autopsy study and implications for the clinic . J. Urol. 1996 ; 156 ; 1969 – 1971 .
- 117 Epstein JI , Oesterling JE , Eggleston JC , Walsh PC . Frozen section detection of lymph node metastases in prostatic carcinoma: accuracy in grossly uninvolved pelvic lymphadenectomy specimens . J. Urol. 1986 ; 136 ; 1234 – 1237 .
- 118 Montironi R , van der Kwast T , Boccon-Gibod L , Bono AV . Handling and pathology reporting of radical prostatectomy specimens . Eur. Urol. 2003 ; 44 ; 626 – 636 .
- 119 Tokuda Y , Carlino LJ , Gopalan A et al. Prostate cancer topography and patterns of lymph node metastasis . Am. J. Surg. Pathol. 2010 ; 34 ; 1862 – 1867 .
- 120
Hutterer GC
,
Briganti A
,
Chun F
et al.
The evolution of staging of lymph node metastases in clinically localized prostate cancer
.
EAU-EBU Update Series
2007
;
5
;
153
–
162
.
10.1016/j.eeus.2007.04.003 Google Scholar
- 121 Gjertson CK , Asher KP , Sclar JD et al. Local control and long-term disease-free survival for stage D1 (T2-T4N1-N2M0) prostate cancer after radical prostatectomy in the PSA era . Urology 2007 ; 70 ; 723 – 727 .
- 122 Fujisawa M , Miyake H . Significance of micrometastases in prostate cancer . Surg. Oncol. 2008 ; 17 ; 247 – 252 .
- 123 Fleischmann A , Schobinger S , Markwalder R et al. Prognostic factors in lymph node metastases of prostatic cancer patients: the size of the metastases but not extranodal extension independently predicts survival . Histopathology 2008 ; 53 ; 468 – 475 .
- 124 Fleischmann A , Schobinger S , Schumacher M , Thalmann GN , Studer UE . Survival in surgically treated, nodal positive prostate cancer patients is predicted by histopathological characteristics of the primary tumor and its lymph node metastases . Prostate 2009 ; 69 ; 352 – 362 .
- 125 Weckermann D , Dorn R , Trefz M , Wagner T , Wawroschek F , Harzmann R . Sentinel lymph node dissection for prostate cancer: experience with more than 1,000 patients . J. Urol. 2007 ; 177 ; 916 – 920 .
- 126 Wawroschek F , Wagner T , Hamm M et al. The influence of serial sections, immunohistochemistry, and extension of pelvic lymph node dissection on the lymph node status in clinically localized prostate cancer . Eur. Urol. 2003 ; 43 ; 132 – 136 ; discussion 37 .
- 127 Steinberg GD , Epstein JI , Piantadosi S , Walsh PC . Management of stage D1 adenocarcinoma of the prostate: the Johns Hopkins experience 1974 to 1987 . J. Urol. 1990 ; 144 ; 1425 – 1432 .
- 128 Schmid H-P , Mihatsch MJ , Hering F , Rutishauser G . Impact of minimal lymph node metastasis on long-term prognosis after radical prostatectomy . Eur. Urol. 1997 ; 31 ; 11 – 16 .
- 129 Sgrignoli AR , Walsh PC , Steinberg GD , Steiner MS , Epstein JI . Prognostic factors in men with stage D1 prostate cancer: identification of patients less likely to have prolonged survival after radical prostatectomy . J. Urol. 1994 ; 152 ; 1077 – 1081 .
- 130 Palapattu GS , Singer EA , Messing EM . Controversies surrounding lymph node dissection for prostate cancer . Urol. Clin. North Am. 2010 ; 37 ; 57 – 65 .
- 131 Cai T , Nesi G , Tinacci G et al. Clinical importance of lymph node density in predicting outcome of prostate cancer patients . J. Surg. Res. 2011 ; 167 ; 267 – 272 .
- 132 Cheng L , Pisansky TM , Ramnani DM et al. Extranodal extension in lymph node-positive prostate cancer . Mod. Pathol. 2000 ; 13 ; 113 – 118 .
- 133 Griebling TL , Ozkutlu D , See WA , Cohen MB . Prognostic implications of extracapsular extension of lymph node metastases in prostate cancer . Mod. Pathol. 1997 ; 10 ; 804 – 809 .
- 134 Cher ML , Stephenson RA , James BC , Carroll PR . Cellular proliferative fraction of metastatic lymph nodes predicts survival in stage D1 (TxN+M0) prostate cancer . J. Urol. 1996 ; 155 ; 1674 – 1677 .
- 135 Hofer MD , Kuefer R , Huang W et al. Prognostic factors in lymph node-positive prostate cancer . Urology 2006 ; 67 ; 1016 – 1021 .
- 136 Da Pozzo LF , Cozzarini C , Briganti A et al. Long-term follow-up of patients with prostate cancer and nodal metastases treated by pelvic lymphadenectomy and radical prostatectomy: the positive impact of adjuvant radiotherapy . Eur. Urol. 2009 ; 55 ; 1003 – 1011 .
- 137 McCullough DL , Leadbetter WF . Radical pelvic surgery for locally extensive carcinoma of the prostate . J. Urol. 1972 ; 108 ; 939 – 943 .
- 138 Schumacher MC , Burkhard FC , Thalmann GN , Fleischmann A , Studer UE . Good outcome for patients with few lymph node metastases after radical retropubic prostatectomy . Eur. Urol. 2008 ; 54 ; 344 – 352 .
- 139 Schumacher MC , Burkhard FC , Thalmann GN , Fleischmann A , Studer UE . Is pelvic lymph node dissection necessary in patients with a serum PSA < 10 ng/ml undergoing radical prostatectomy for prostate cancer? Eur. Urol. 2006 ; 50 ; 272 – 279 .
- 140 Abdollah F , Sun M , Thuret R et al. Decreasing rate and extent of lymph node staging in patients undergoing radical prostatectomy may undermine the rate of diagnosis of lymph node metastases in prostate cancer . Eur. Urol. 2010 ; 58 ; 882 – 892 .
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