Lymphadenectomy in the Surgical Management of Penile Cancer

European Urology

Volumn 55, Issue 5, 2009, Pages 1075-1088

  Protzel, Chris ^a   Alcaraz, Antonio ^b   Horenblas, Simon ^c   Pizzocaro, Giorgio ^d   Zlotta, Alexandre ^e   Hakenberg, Oliver W ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b UNIVERSITY OF BARCELONA   (Spain)

^c ANTONI VAN LEEUWENHOEK HOSPITAL   (Netherlands)

^d Department of Urology   (Italy)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Lymph node metastases; Lymphadenectomy; Penile carcinoma; Recurrence

Indexed keywords

ADVANCED CANCER; CANCER ADJUVANT THERAPY; CANCER DIAGNOSIS; CANCER RISK; CANCER STAGING; CANCER SURGERY; CANCER SURVIVAL; DIAGNOSTIC ACCURACY; ENDOSCOPIC SURGERY; HISTOPATHOLOGY; HUMAN; INGUINAL LYMPH NODE; LYMPH NODE METASTASIS; LYMPHADENECTOMY; MEDLINE; MORBIDITY; PATIENT COMPLIANCE; PELVIS LYMPH NODE; PELVIS LYMPHADENECTOMY; PENIS CARCINOMA; PHYSICAL EXAMINATION; POSTOPERATIVE COMPLICATION; PRIORITY JOURNAL; REVIEW; SENTINEL LYMPH NODE BIOPSY; SURGICAL TECHNIQUE;

DISEASE-FREE SURVIVAL; HUMANS; INGUINAL CANAL; LYMPH NODE EXCISION; LYMPH NODES; LYMPHATIC METASTASIS; MALE; NEOPLASM INVASIVENESS; NEOPLASM RECURRENCE, LOCAL; NEOPLASM STAGING; PENILE NEOPLASMS; PROGNOSIS; RISK ASSESSMENT; SURVIVAL ANALYSIS;

EID: 62649128863     PISSN: 03022838     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.eururo.2009.02.021     Document Type: Review

References (93)

1. Jemal A., Siegel R., Ward E., Murray T., Xu J., and Thun M.J. Cancer statistics, 2007. CA Cancer J Clin 57 (2007) 43-66
2. Hakenberg O.W., Nippgen J.B., Froehner M., Zastrow S., and Wirth M.P. Cisplatin, methotrexate and bleomycin for treating advanced penile carcinoma. BJU Int 98 (2006) 1225-1227
3. Pizzocaro G., Nicolai N., and Milani A. Taxanes in combination with cisplatin and fluorouracil for advanced penile cancer: preliminary results. Eur Urol 55 (2009) 546-551
4. Horenblas S. Lymphadenectomy for squamous cell carcinoma of the penis. Part 2: the role and technique of lymph node dissection. BJU Int 88 (2001) 473-483
5. Spiess PE, Hernandez MS, Pettaway CA. Contemporary inguinal lymph node dissection: minimizing complications. World J Urol. In press.
6. Ornellas A.A., Seixas A.L., Marota A., Wisnescky A., Campos F., and de Moraes J.R. Surgical treatment of invasive squamous cell carcinoma of the penis: retrospective analysis of 350 cases. J Urol 151 (1994) 1244-1249
7. Naumann C.M., Filippow N., Seif C., et al. Penile carcinoma (pT1 G2): surveillance or inguinal lymph node dissection?. Onkologie 28 (2005) 135-138
8. Doehn C., Baumgartel M., and Jocham D. Surgical therapy of penis carcinoma. Urologe A 40 (2001) 303-307
9. Ficarra V., Zattoni F., Cunico S.C., et al. Lymphatic and vascular embolizations are independent predictive variables of inguinal lymph node involvement in patients with squamous cell carcinoma of the penis: Gruppo Uro-Oncologico del Nord Est (Northeast Uro-Oncological Group) Penile Cancer data base data. Cancer 103 (2005) 2507-2516
10. Daseler E.H., Anson B.J., and Reimann A.F. Radical excision of the inguinal and iliac lymph glands; a study based upon 450 anatomical dissections and upon supportive clinical observations. Surg Gynecol Obstet 87 (1948) 679-694
11. Cabanas R.M. An approach for the treatment of penile carcinoma. Cancer 39 (1977) 456-466
12. Horenblas S., Jansen L., Meinhardt W., Hoefnagel C.A., de Jong D., and Nieweg O.E. Detection of occult metastasis in squamous cell carcinoma of the penis using a dynamic sentinel node procedure. J Urol 163 (2000) 100-104
13. Kroon B.K., Horenblas S., Meinhardt W., et al. Dynamic sentinel node biopsy in penile carcinoma: evaluation of 10 years experience. Eur Urol 47 (2005) 601-606 discussion 606
14. Leijte J.A.P., Valdés Olmos R.A., Nieweg O.E., and Horenblas S. Anatomical mapping of lymphatic drainage in penile carcinoma with SPECT-CT: implications for the extent of inguinal lymph node dissection. Eur Urol 54 (2008) 885-892
15. Horenblas S. Lymphadenectomy for squamous cell carcinoma of the penis. Part 1: diagnosis of lymph node metastasis. BJU Int 88 (2001) 467-472
16. Culkin D.J., and Beer T.M. Advanced penile carcinoma. J Urol 170 (2003) 359-365
17. Lopes A., Hidalgo G.S., Kowalski L.P., Torloni H., Rossi B.M., and Fonseca F.P. Prognostic factors in carcinoma of the penis: multivariate analysis of 145 patients treated with amputation and lymphadenectomy. J Urol 156 (1996) 1637-1642
18. Naumann C.M., Alkatout I., Al-Najar A., et al. Lymph-node metastases in intermediate-risk squamous cell carcinoma of the penis. BJU Int 102 (2008) 1102-1106
19. Ficarra V., Zattoni F., Artibani W., et al. Nomogram predictive of pathological inguinal lymph node involvement in patients with squamous cell carcinoma of the penis. J Urol 175 (2006) 1700-1704 discussion 1704-5
20. Berdjis N., Meye A., Nippgen J., et al. Expression of Ki-67 in squamous cell carcinoma of the penis. BJU Int 96 (2005) 146-148
21. Lont A.P., Kroon B.K., Gallee M.P., van Tinteren H., Moonen L.M., and Horenblas S. Pelvic lymph node dissection for penile carcinoma: extent of inguinal lymph node involvement as an indicator for pelvic lymph node involvement and survival. J Urol 177 (2007) 947-952 discussion 952
22. Hegarty P.K., Kayes O., Freeman A., Christopher N., Ralph D.J., and Minhas S. A prospective study of 100 cases of penile cancer managed according to European Association of Urology guidelines. BJU Int 98 (2006) 526-531
23. Leijte JA, Horenblas S. Shortcomings of the current TNM classification for penile carcinoma: time for a change? World J Urol. In press.
24. Theodorescu D., Russo P., Zhang Z.F., Morash C., and Fair W.R. Outcomes of initial surveillance of invasive squamous cell carcinoma of the penis and negative nodes. J Urol 155 (1996) 1626-1631
25. Slaton J.W., Morgenstern N., Levy D.A., et al. Tumor stage, vascular invasion and the percentage of poorly differentiated cancer: independent prognosticators for inguinal lymph node metastasis in penile squamous cancer. J Urol 165 (2001) 1138-1142
26. Kroon B.K., Horenblas S., Lont A.P., Tanis P.J., Gallee M.P., and Nieweg O.E. Patients with penile carcinoma benefit from immediate resection of clinically occult lymph node metastases. J Urol 173 (2005) 816-819
27. Solsona E., Iborra I., Rubio J., Casanova J.L., Ricos J.V., and Calabuig C. Prospective validation of the association of local tumor stage and grade as a predictive factor for occult lymph node micrometastasis in patients with penile carcinoma and clinically negative inguinal lymph nodes. J Urol 165 (2001) 1506-1509
28. Solsona E., Algaba F., Horenblas S., Pizzocaro G., and Windahl T. EAU guidelines on penile cancer. Eur Urol 46 (2004) 1-8
29. Leijte J.A.P., Kroon B.K., Valdés Olmos R.A., Nieweg O.E., and Horenblas S. Reliability and safety of current dynamic sentinel node biopsy for penile carcinoma. Eur Urol 52 (2007) 170-177
30. Protzel C., Knoedel J., Wolf E., Kleist B., Poetsch M., and Giebel J. Prognostic parameters of penis carcinoma. Urologe A 46 (2007) 1162
31. Kayes O., Ahmed H.U., Arya M., and Minhas S. Molecular and genetic pathways in penile cancer. Lancet Oncol 8 (2007) 420-429
32. Protzel C., Kakies C., Kleist B., Poetsch M., and Giebel J. Down-regulation of the metastasis suppressor protein KAI1/CD82 correlates with occurrence of metastasis, prognosis and presence of HPV DNA in human penile squamous cell carcinoma. Virchows Arch 452 (2008) 369-375
33. Lont A.P., Kroon B.K., Horenblas S., et al. Presence of high-risk human papillomavirus DNA in penile carcinoma predicts favorable outcome in survival. Int J Cancer 119 (2006) 1078-1081
34. Bezerra A.L., Lopes A., Santiago G.H., Ribeiro K.C., Latorre M.R., and Villa L.L. Human papillomavirus as a prognostic factor in carcinoma of the penis: analysis of 82 patients treated with amputation and bilateral lymphadenectomy. Cancer 91 (2001) 2315-2321
35. Protzel C., Knoedel J., Zimmermann U., Woenckhaus C., Poetsch M., and Giebel J. Expression of proliferation marker Ki67 correlates to occurrence of metastasis and prognosis, histological subtypes and HPV DNA detection in penile carcinomas. Histol Histopathol 22 (2007) 1197-1204
36. Guimaraes G.C., Leal M.L., Campos R.S., et al. Do proliferating cell nuclear antigen and MIB-1/Ki-67 have prognostic value in penile squamous cell carcinoma?. Urology 70 (2007) 137-142
37. Lopes A., Bezerra A.L., Pinto C.A., Serrano S.V., de Mell O.C., and Villa L.L. p53 as a new prognostic factor for lymph node metastasis in penile carcinoma: analysis of 82 patients treated with amputation and bilateral lymphadenectomy. J Urol 168 (2002) 81-86
38. Martins A.C., Faria S.M., Cologna A.J., Suaid H.J., and Tucci Jr. S. Immunoexpression of p53 protein and proliferating cell nuclear antigen in penile carcinoma. J Urol 167 (2002) 89-92 discussion 92-3
39. Zhu Y., Zhou X.Y., Yao X.D., Dai B., and Ye D.W. The prognostic significance of p53, Ki-67, epithelial cadherin and matrix metalloproteinase-9 in penile squamous cell carcinoma treated with surgery. BJU Int 100 (2007) 204-208
40. Persky L., and deKernion J. Carcinoma of the penis. CA Cancer J Clin 36 (1986) 258-273
41. Singh A.K., Gonzalez-Torrez P., Kaewlai R., Tabatabaei S., and Harisinghani M.G. Imaging of penile neoplasm. Semin Ultrasound CT MR 28 (2007) 287-296
42. Mueller-Lisse U.G., Scher B., Scherr M.K., and Seitz M. Functional imaging in penile cancer: PET/computed tomography, MRI, and sentinel lymph node biopsy. Curr Opin Urol 18 (2008) 105-110
43. Tabatabaei S., Harisinghani M., and McDougal W.S. Regional lymph node staging using lymphotropic nanoparticle enhanced magnetic resonance imaging with ferumoxtran-10 in patients with penile cancer. J Urol 174 (2005) 923-927 discussion 927
44. Scher B., Seitz M., Reiser M., et al. 18F-FDG PET/CT for staging of penile cancer. J Nucl Med 46 (2005) 1460-1465
45. Scher B., Seitz M., Albinger W., et al. Value of PET and PET/CT in the diagnostics of prostate and penile cancer. Recent Results Cancer Res 170 (2008) 159-179
46. Saisorn I., Lawrentschuk N., Leewansangtong S., and Bolton D.M. Fine-needle aspiration cytology predicts inguinal lymph node metastasis without antibiotic pretreatment in penile carcinoma. BJU Int 97 (2006) 1225-1228
47. Kroon B.K., Horenblas S., Deurloo E.E., Nieweg O.E., and Teertstra H.J. Ultrasonography-guided fine-needle aspiration cytology before sentinel node biopsy in patients with penile carcinoma. BJU Int 95 (2005) 517-521
48. Lont A.P., Horenblas S., Tanis P.J., Gallee M.P., van Tinteren H., and Nieweg O.E. Management of clinically node negative penile carcinoma: improved survival after the introduction of dynamic sentinel node biopsy. J Urol 170 (2003) 783-786
49. Leijte J.A.P., Kirrander P., Antonini N., Windahl T., and Horenblas S. Recurrence patterns of squamous cell carcinoma of the penis: recommendations for follow-up based on a two-centre analysis of 700 patients. Eur Urol 54 (2008) 161-169
50. In: Wein A.J., Kavoussi L.R., Novick A.C., Partin A.W., and Peters C.A. (Eds). Campbell-Walsh Urology. 9th ed. (2007), Saunders Elsevier, Philadelphia, PA
51. Bevan-Thomas R., Slaton J.W., and Pettaway C.A. Contemporary morbidity from lymphadenectomy for penile squamous cell carcinoma: the M.D. Anderson Cancer Center Experience. J Urol 167 (2002) 1638-1642
52. Ravi R. Morbidity following groin dissection for penile carcinoma. Br J Urol 72 (1993) 941-945
53. Catalona W.J. Modified inguinal lymphadenectomy for carcinoma of the penis with preservation of saphenous veins: technique and preliminary results. J Urol 140 (1988) 306-310
54. Bouchot O., Rigaud J., Maillet F., Hetet J.F., and Karam G. Morbidity of inguinal lymphadenectomy for invasive penile carcinoma. Eur Urol 45 (2004) 761-766 discussion 765-6
55. Lopes A., Rossi B.M., Fonseca F.P., and Morini S. Unreliability of modified inguinal lymphadenectomy for clinical staging of penile carcinoma. Cancer 77 (1996) 2099-2102
56. Wespes E., Simon J., and Schulman C.C. Cabanas approach: is sentinel node biopsy reliable for staging penile carcinoma?. Urology 28 (1986) 278-279
57. Allen B., Campbell I., Desai S., Dray M., and Scarlet J. Pilot study comparing the accuracy of lymphoscintigraphy sentinel lymph node localisation with axillary node dissection in women with operable breast cancer. N Z Med J 114 (2001) 233-236
58. Statius Muller M.G., van Leeuwen P.A., Borgstein P.J., Pijpers R., and Meijer S. The sentinel node procedure in cutaneous melanoma: an overview of 6 years' experience. Eur J Nucl Med 26 (1999) S20-S25
59. Tanis P.J., Lont A.P., Meinhardt W., Olmos R.A., Nieweg O.E., and Horenblas S. Dynamic sentinel node biopsy for penile cancer: reliability of a staging technique. J Urol 168 (2002) 76-80
60. Kroon B.K., Horenblas S., Estourgie S.H., Lont A.P., Valdes Olmos R.A., and Nieweg O.E. How to avoid false-negative dynamic sentinel node procedures in penile carcinoma. J Urol 171 (2004) 2191-2194
61. Ficarra V., and Galfano A. Should the dynamic sentinel node biopsy (DSNB) be considered the gold standard in the evaluation of lymph node status in patients with penile carcinoma?. Eur Urol 52 (2007) 17-19 discussion 20-1
62. Tobias-Machado M., Tavares A., Ornellas A.A., Molina Jr. W.R., Juliano R.V., and Wroclawski E.R. Video endoscopic inguinal lymphadenectomy: a new minimally invasive procedure for radical management of inguinal nodes in patients with penile squamous cell carcinoma. J Urol 177 (2007) 953-957 discussion 958
63. Sotelo R., Sanchez-Salas R., Carmona O., et al. Endoscopic lymphadenectomy for penile carcinoma. J Endourol 21 (2007) 364-367 discussion 367
64. Tobias-Machado M., Tavares A., Silva M.N., et al. Can video endoscopic inguinal lymphadenectomy achieve a lower morbidity than open lymph node dissection in penile cancer patients?. J Endourol 22 (2008) 1687-1691
65. Lopes A., Bezerra A.L., Serrano S.V., and Hidalgo G.S. Iliac nodal metastases from carcinoma of the penis treated surgically. BJU Int 86 (2000) 690-693
66. Zhu Y., Zhang S.L., Ye D.W., Yao X.D., Jiang Z.X., and Zhou X.Y. Predicting pelvic lymph node metastases in penile cancer patients: a comparison of computed tomography, Cloquet's node, and disease burden of inguinal lymph nodes. Onkologie 31 (2008) 37-41
67. Johnson D.E., and Lo R.K. Management of regional lymph nodes in penile carcinoma. Five-year results following therapeutic groin dissections. Urology 24 (1984) 308-311
68. Hakenberg O.W., and Wirth M.P. Issues in the treatment of penile carcinoma. A short review. Urol Int 62 (1999) 229-233
69. Ornellas A.A., Seixas A.L., and de Moraes J.R. Analyses of 200 lymphadenectomies in patients with penile carcinoma. J Urol 146 (1991) 330-332
70. Loughlin K.R. Surgical atlas. Surgical management of penile carcinoma: the inguinal nodes. BJU Int 97 (2006) 1125-1134
71. Nelson B.A., Cookson M.S., Smith Jr. J.A., and Chang S.S. Complications of inguinal and pelvic lymphadenectomy for squamous cell carcinoma of the penis: a contemporary series. J Urol 172 (2004) 494-497
72. Perdona S., Autorino R., De Sio M., et al. Dynamic sentinel node biopsy in clinically node-negative penile cancer versus radical inguinal lymphadenectomy: a comparative study. Urology 66 (2005) 1282-1286
73. Preis E., and Jakse G. The significance of inguinal lymphadenectomy in carcinoma of the penis. Urologe A 45 (2006) 176-180
74. Hungerhuber E., Schlenker B., Frimberger D., et al. Lymphoscintigraphy in penile cancer: limited value of sentinel node biopsy in patients with clinically suspicious lymph nodes. World J Urol 24 (2006) 319-324
75. Pizzocaro G., and Piva L. Adjuvant and neoadjuvant vincristine, bleomycin, and methotrexate for inguinal metastases from squamous cell carcinoma of the penis. Acta Oncol 27 (1988) 823-824
76. Bermejo C., Busby J.E., Spiess P.E., Heller L., Pagliaro L.C., and Pettaway C.A. Neoadjuvant chemotherapy followed by aggressive surgical consolidation for metastatic penile squamous cell carcinoma. J Urol 177 (2007) 1335-1338
77. Leijte J.A.P., Kerst J.M., Bais E., Antonini N., and Horenblas S. Neoadjuvant chemotherapy in advanced penile carcinoma. Eur Urol 52 (2007) 488-494
78. Horenblas S., van Tinteren H., Delemarre J.F., Moonen L.M., Lustig V., and van Waardenburg E.W. Squamous cell carcinoma of the penis. III. Treatment of regional lymph nodes. J Urol 149 (1993) 492-497
79. Narayana A.S., Olney L.E., Loening S.A., Weimar G.W., and Culp D.A. Carcinoma of the penis: analysis of 219 cases. Cancer 49 (1982) 2185-2191
80. Solsona E., Iborra I., Ricos J.V., et al. Corpus cavernosum invasion and tumor grade in the prediction of lymph node condition in penile carcinoma. Eur Urol 22 (1992) 115-118
81. Parra R.O. Accurate staging of carcinoma of the penis in men with nonpalpable inguinal lymph nodes by modified inguinal lymphadenectomy. J Urol 155 (1996) 560-563
82. Colberg J.W., Andriole G.L., and Catalona W.J. Long-term follow-up of men undergoing modified inguinal lymphadenectomy for carcinoma of the penis. Br J Urol 79 (1997) 54-57
83. Coblentz T.R., and Theodorescu D. Morbidity of modified prophylactic inguinal lymphadenectomy for squamous cell carcinoma of the penis. J Urol 168 (2002) 1386-1389
84. d'Ancona C.A., de Lucena R.G., Querne F.A., Martins M.H., Denardi F., and Netto Jr. N.R. Long-term followup of penile carcinoma treated with penectomy and bilateral modified inguinal lymphadenectomy. J Urol 172 (2004) 498-501 discussion 501
85. Wawroschek F., Vogt H., Bachter D., Weckermann D., Hamm M., and Harzmann R. First experience with gamma probe guided sentinel lymph node surgery in penile cancer. Urol Res 28 (2000) 246-249
86. Spiess P.E., Izawa J.I., Bassett R., et al. Preoperative lymphoscintigraphy and dynamic sentinel node biopsy for staging penile cancer: results with pathological correlation. J Urol 177 (2007) 2157-2161
87. Gonzaga-Silva L.F., Tavares J.M., Freitas F.C., Tomas Filho M.E., Oliveira V.P., and Lima M.V. The isolated gamma probe technique for sentinel node penile carcinoma detection is unreliable. Int Braz J Urol 33 (2007) 58-63 discussion 64-7
88. Hernandez-Toris N., Quintero-Becerra J., Gallegos-Hernandez J.F., et al. Lymphatic mapping and sentinel node biopsy in penis cancer. Feasibility study and preliminary report [in Spanish]. Cir Cir 75 (2007) 87-91
89. Hadway P., Smith Y., Corbishley C., Heenan S., and Watkin N.A. Evaluation of dynamic lymphoscintigraphy and sentinel lymph-node biopsy for detecting occult metastases in patients with penile squamous cell carcinoma. BJU Int 100 (2007) 561-565
90. Jacobellis U. Modified radical inguinal lymphadenectomy for carcinoma of the penis: technique and results. J Urol 169 (2003) 1349-1352
91. Milathianakis C., Bogdanos J., and Karamanolakis D. Morbidity of prophylactic inguinal lymphadenectomy with saphenous vein preservation for squamous cell penile carcinoma. Int J Urol 12 (2005) 776-778
92. Heyns C.F., and Theron P.D. Evaluation of dynamic sentinel lymph node biopsy in patients with squamous cell carcinoma of the penis and palpable inguinal nodes. BJU Int 102 (2008) 305-309
93. Protzel C., and Hakenberg O.W. Chemotherapy in patients with penile carcinoma. Urol Int 82 (2009) 1-7