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Published in: EJNMMI Research 1/2023

Open Access 01-12-2023 | Computed Tomography | Original research

Accuracy of dynamic sentinel lymph node biopsy for inguinal lymph node staging in cN0 penile cancer

Authors: Juanito Gebruers, Laura Elst, Marcella Baldewijns, Liesbeth De Wever, Koen Van Laere, Maarten Albersen, Karolien Goffin

Published in: EJNMMI Research | Issue 1/2023

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Abstract

Background

Penile cancer is characterized by an early lymphatic dissemination. In intermediate and high-risk primary tumors without palpable inguinal lymph nodes, there is a 6–30% risk of micro-metastatic disease. Invasive lymph node staging in these patients is performed using dynamic sentinel lymph node biopsy (DSNB). In this study, the role of DSNB in cN0 penile cancer was studied, evaluating features of sentinel lymph node (SN) visualization and outcome parameters. Patients with penile cancer without inguinal lymph node metastases who were referred for DSNB at our center between January 2015 and May 2021 and had a follow-up period of at least 18 months, were retrospectively included. After injection of 85 ± 20 MBq [99mTc]Tc-nanocolloid peritumorally, dynamic, static planar and SPECT/CT imaging was performed. Primary endpoints were sensitivity of the diagnostic procedure, disease-free survival and DSNB-related adverse events. Secondary endpoints were SN detection rate, number of SNs and the number of counts of the most active SN.

Results

Seventy-seven penile DSNB procedures in 75 patients (67 ± 11 years) were included. The detection rate of DSNB was 91% and 96% per procedure and groin, respectively. Sensitivity, specificity, negative predictive value (NPV) and positive predictive value (PPV) were 79%, 100%, 97% and 100%, respectively. More SNs were seen on SPECT/CT than on static planar imaging (1.33 vs. 1.17, p = 0.001). The mean counts per SN on static planar imaging was lower compared to SPECT/CT (1343 vs. 5008; p < 0.0001). There was a positive correlation between the total counts of the SN on the static planar image and the SPECT/CT (r = 0.79, p < 0.0001). Only one out of seventy-five patients (1%) experienced DSNB-related adverse events. After 18 months, 58 patients remained disease free (77%), 13 developed local recurrence (17%), and 4 developed lymphatic or distant metastases (5%).

Conclusion

DNSB is a safe diagnostic procedure with a good detection rate and in particular high negative predictive value. It can therefore prevent overtreatment of patients with negative inguinal groins on clinical examination and DSNB examination. Finally, DSNB enables an early detection of occult metastases which would not be visualized with standardized imaging modalities.
Literature
1.
go back to reference Brouwer OR, Albersen M, Parnham A, Protzel C, Pettaway CA, Ayres B, Antunes-Lopes T, Barreto L, Campi R, Crook J, Fernández-Pello S, Greco I, van der Heijden MS, Johnstone PAS, Kailavasan M, Manzie K, Marcus JD, Necchi A, Oliveira P, Osborne J, Pagliaro LC, Garcia-Perdomo HA, Rumble RB, Sachdeva A, Sakalis VI, Zapala Ł, Sánchez Martínez DF, Spiess PE, Tagawa ST. European association of urology-american society of clinical oncology collaborative guideline on penile cancer: 2023 update. Eur Urol. 2023;83(6):548–60.CrossRefPubMed Brouwer OR, Albersen M, Parnham A, Protzel C, Pettaway CA, Ayres B, Antunes-Lopes T, Barreto L, Campi R, Crook J, Fernández-Pello S, Greco I, van der Heijden MS, Johnstone PAS, Kailavasan M, Manzie K, Marcus JD, Necchi A, Oliveira P, Osborne J, Pagliaro LC, Garcia-Perdomo HA, Rumble RB, Sachdeva A, Sakalis VI, Zapala Ł, Sánchez Martínez DF, Spiess PE, Tagawa ST. European association of urology-american society of clinical oncology collaborative guideline on penile cancer: 2023 update. Eur Urol. 2023;83(6):548–60.CrossRefPubMed
2.
go back to reference Horenblas S, Van Tinteren H. Squamous cell carcinoma of the penis. IV. Prognostic factors of survival: analysis of tumor, nodes and metastasis classification system. J Urol. 1994;151(5):1239–43.CrossRefPubMed Horenblas S, Van Tinteren H. Squamous cell carcinoma of the penis. IV. Prognostic factors of survival: analysis of tumor, nodes and metastasis classification system. J Urol. 1994;151(5):1239–43.CrossRefPubMed
3.
go back to reference Thomas A, Necchi A, Muneer A, Tobias-Machado M, Tran ATH, Van Rompuy AS, Spiess PE, Albersen M. Penile cancer. Nat Rev Dis Primers. 2021;7(1):11.CrossRefPubMed Thomas A, Necchi A, Muneer A, Tobias-Machado M, Tran ATH, Van Rompuy AS, Spiess PE, Albersen M. Penile cancer. Nat Rev Dis Primers. 2021;7(1):11.CrossRefPubMed
4.
go back to reference Wever L, de Vries HM, Dell’Oglio P, van der Poel HG, Donswijk ML, Sikorska K, van Leeuwen FWB, Horenblas S, Brouwer OR. Incidence and risk factor analysis of complications after sentinel node biopsy for penile cancer. BJU Int. 2022;130(4):486–95.CrossRefPubMed Wever L, de Vries HM, Dell’Oglio P, van der Poel HG, Donswijk ML, Sikorska K, van Leeuwen FWB, Horenblas S, Brouwer OR. Incidence and risk factor analysis of complications after sentinel node biopsy for penile cancer. BJU Int. 2022;130(4):486–95.CrossRefPubMed
5.
go back to reference Stuiver MM, Djajadiningrat RS, Graafland NM, Vincent AD, Lucas C, Horenblas S. Early wound complications after inguinal lymphadenectomy in penile cancer: a historical cohort study and risk-factor analysis. Eur Urol. 2013;64(3):486–92.CrossRefPubMed Stuiver MM, Djajadiningrat RS, Graafland NM, Vincent AD, Lucas C, Horenblas S. Early wound complications after inguinal lymphadenectomy in penile cancer: a historical cohort study and risk-factor analysis. Eur Urol. 2013;64(3):486–92.CrossRefPubMed
6.
go back to reference Fankhauser CD, de Vries HM, Roussel E, Jakobsen JK, Issa A, Lee EWC, Schifano N, Alnajjar H, Castiglione F, Antonelli L, Oliveira P, Lau M, Parnham A, Albersen M, Watkin NA, Muneer A, Ayres BE, Brouwer OR, Sangar V. Lymphovascular and perineural invasion are risk factors for inguinal lymph node metastases in men with T1G2 penile cancer. J Cancer Res Clin Oncol. 2022;148(9):2231–4.CrossRefPubMed Fankhauser CD, de Vries HM, Roussel E, Jakobsen JK, Issa A, Lee EWC, Schifano N, Alnajjar H, Castiglione F, Antonelli L, Oliveira P, Lau M, Parnham A, Albersen M, Watkin NA, Muneer A, Ayres BE, Brouwer OR, Sangar V. Lymphovascular and perineural invasion are risk factors for inguinal lymph node metastases in men with T1G2 penile cancer. J Cancer Res Clin Oncol. 2022;148(9):2231–4.CrossRefPubMed
7.
go back to reference Ficarra V, Akduman B, Bouchot O, Palou J, Tobias-Machado M. Prognostic factors in penile cancer. Urology. 2010;76(2 Suppl 1):S66-73.CrossRefPubMed Ficarra V, Akduman B, Bouchot O, Palou J, Tobias-Machado M. Prognostic factors in penile cancer. Urology. 2010;76(2 Suppl 1):S66-73.CrossRefPubMed
8.
9.
go back to reference Wever L, de Vries HM, van der Poel H, van Leeuwen F, Horenblas S, Brouwer O. Minimally invasive evaluation of the clinically negative inguinal node in penile cancer: dynamic sentinel node biopsy. Urol Oncol. 2022;40(6):209–14.CrossRefPubMed Wever L, de Vries HM, van der Poel H, van Leeuwen F, Horenblas S, Brouwer O. Minimally invasive evaluation of the clinically negative inguinal node in penile cancer: dynamic sentinel node biopsy. Urol Oncol. 2022;40(6):209–14.CrossRefPubMed
10.
go back to reference Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibañes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250(2):187–96.CrossRefPubMed Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibañes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250(2):187–96.CrossRefPubMed
11.
go back to reference Fallara G, Pozzi E, Onur Cakir O, Tandogdu Z, Castiglione F, Salonia A, Alnajjar HM, Muneer A; EAU-YAU Penile and Testis Cancer Working Group. Diagnostic accuracy of dynamic sentinel lymph node biopsy for penile cancer: a systematic review and meta-analysis. Eur Urol Focus. 2022;S2405–4569(22):00277–2. Fallara G, Pozzi E, Onur Cakir O, Tandogdu Z, Castiglione F, Salonia A, Alnajjar HM, Muneer A; EAU-YAU Penile and Testis Cancer Working Group. Diagnostic accuracy of dynamic sentinel lymph node biopsy for penile cancer: a systematic review and meta-analysis. Eur Urol Focus. 2022;S2405–4569(22):00277–2.
12.
go back to reference Sedigh O, Preto M, Soleimanzadeh F, Marra G, Falcone M, Rolle L, Ceruti C, Timpano M, Sibona M, Dalmasso E, Delmonte S, Caliendo V, Frea B, Gontero P. Role of perioperative dynamic sentinel node biopsy for cN0 penile cancer management: experience from an Italian tertiary referral center. Tumori. 2018;104(1):66–70.CrossRefPubMed Sedigh O, Preto M, Soleimanzadeh F, Marra G, Falcone M, Rolle L, Ceruti C, Timpano M, Sibona M, Dalmasso E, Delmonte S, Caliendo V, Frea B, Gontero P. Role of perioperative dynamic sentinel node biopsy for cN0 penile cancer management: experience from an Italian tertiary referral center. Tumori. 2018;104(1):66–70.CrossRefPubMed
13.
go back to reference Valdés Olmos RA, Tanis PJ, Hoefnagel CA, Jansen L, Nieweg OE, Meinhardt W, Horenblas S. Penile lymphoscintigraphy for sentinel node identification. Eur J Nucl Med. 2001;28(5):581–5.CrossRefPubMed Valdés Olmos RA, Tanis PJ, Hoefnagel CA, Jansen L, Nieweg OE, Meinhardt W, Horenblas S. Penile lymphoscintigraphy for sentinel node identification. Eur J Nucl Med. 2001;28(5):581–5.CrossRefPubMed
14.
go back to reference Sahdev V, Albersen M, Christodoulidou M, Parnham A, Malone P, Nigam R, Bomanji J, Muneer A. Management of non-visualization following dynamic sentinel lymph node biopsy for squamous cell carcinoma of the penis. BJU Int. 2017;119(4):573–8.CrossRefPubMed Sahdev V, Albersen M, Christodoulidou M, Parnham A, Malone P, Nigam R, Bomanji J, Muneer A. Management of non-visualization following dynamic sentinel lymph node biopsy for squamous cell carcinoma of the penis. BJU Int. 2017;119(4):573–8.CrossRefPubMed
15.
go back to reference Saad ZZ, Omorphos S, Michopoulou S, Gacinovic S, Malone P, Nigam R, Muneer A, Bomanji J. Investigating the role of SPECT/CT in dynamic sentinel lymph node biopsy for penile cancers. Eur J Nucl Med Mol Imaging. 2017;44(7):1176–84.CrossRefPubMedPubMedCentral Saad ZZ, Omorphos S, Michopoulou S, Gacinovic S, Malone P, Nigam R, Muneer A, Bomanji J. Investigating the role of SPECT/CT in dynamic sentinel lymph node biopsy for penile cancers. Eur J Nucl Med Mol Imaging. 2017;44(7):1176–84.CrossRefPubMedPubMedCentral
16.
go back to reference Jimenez-Heffernan A, Ellmann A, Sado H, Huić D, Bal C, Parameswaran R, Giammarile F, Pruzzo R, Kostadinova I, Vorster M, Almeida P, Santiago J, Gambhir S, Sergieva S, Calderon A, Young GO, Valdes-Olmos R, Zaknun J, Magboo VP, Pascual TN. Results of a prospective multicenter international atomic energy agency sentinel node trial on the value of SPECT/CT over planar imaging in various malignancies. J Nucl Med. 2015;56(9):1338–44.CrossRefPubMed Jimenez-Heffernan A, Ellmann A, Sado H, Huić D, Bal C, Parameswaran R, Giammarile F, Pruzzo R, Kostadinova I, Vorster M, Almeida P, Santiago J, Gambhir S, Sergieva S, Calderon A, Young GO, Valdes-Olmos R, Zaknun J, Magboo VP, Pascual TN. Results of a prospective multicenter international atomic energy agency sentinel node trial on the value of SPECT/CT over planar imaging in various malignancies. J Nucl Med. 2015;56(9):1338–44.CrossRefPubMed
17.
go back to reference Leijte JA, Kroon BK, Valdes Olmos RA, Nieweg OE, Horenblas S. Reliability and safety of current dynamic sentinel node biopsy for penile carcinoma. Eur Urol. 2007;52:170–7.CrossRefPubMed Leijte JA, Kroon BK, Valdes Olmos RA, Nieweg OE, Horenblas S. Reliability and safety of current dynamic sentinel node biopsy for penile carcinoma. Eur Urol. 2007;52:170–7.CrossRefPubMed
18.
go back to reference Hadway P, Smith Y, Corbishley C, Heenan S, Watkin NA. Evaluation of dynamic lymphoscintigraphy and sentinel lymph-node biopsy for detecting occult metastases in patients with penile squamous cell carcinoma. BJU Int. 2007;100:561–5.CrossRefPubMed Hadway P, Smith Y, Corbishley C, Heenan S, Watkin NA. Evaluation of dynamic lymphoscintigraphy and sentinel lymph-node biopsy for detecting occult metastases in patients with penile squamous cell carcinoma. BJU Int. 2007;100:561–5.CrossRefPubMed
19.
go back to reference Zou ZJ, Liu ZH, Tang LY, Wang YJ, Liang JY, Zhang RC, Tang YQ, Lu YP. Radiocolloid-based dynamic sentinel lymph node biopsy in penile cancer with clinically negative inguinal lymph node: an updated systematic review and meta-analysis. Int Urol Nephrol. 2016;48(12):2001–13.CrossRefPubMed Zou ZJ, Liu ZH, Tang LY, Wang YJ, Liang JY, Zhang RC, Tang YQ, Lu YP. Radiocolloid-based dynamic sentinel lymph node biopsy in penile cancer with clinically negative inguinal lymph node: an updated systematic review and meta-analysis. Int Urol Nephrol. 2016;48(12):2001–13.CrossRefPubMed
20.
go back to reference Lam W, Alnajjar HM, La-Touche S, Perry M, Sharma D, Corbishley C, Pilcher J, Heenan S, Watkin N. Dynamic sentinel lymph node biopsy in patients with invasive squamous cell carcinoma of the penis: a prospective study of the long-term outcome of 500 inguinal basins assessed at a single institution. Eur Urol. 2013;63(4):657–63.CrossRefPubMed Lam W, Alnajjar HM, La-Touche S, Perry M, Sharma D, Corbishley C, Pilcher J, Heenan S, Watkin N. Dynamic sentinel lymph node biopsy in patients with invasive squamous cell carcinoma of the penis: a prospective study of the long-term outcome of 500 inguinal basins assessed at a single institution. Eur Urol. 2013;63(4):657–63.CrossRefPubMed
21.
go back to reference Dimopoulos P, Christopoulos P, Shilito S, Gall Z, Murby B, Ashworth D, Taylor B, Carrington B, Shanks J, Clarke N, Ramani V, Parr N, Lau M, Sangar V. Dynamic sentinel lymph node biopsy for penile cancer: a comparison between 1- and 2-day protocols. BJU Int. 2016;117(6):890–6.CrossRefPubMed Dimopoulos P, Christopoulos P, Shilito S, Gall Z, Murby B, Ashworth D, Taylor B, Carrington B, Shanks J, Clarke N, Ramani V, Parr N, Lau M, Sangar V. Dynamic sentinel lymph node biopsy for penile cancer: a comparison between 1- and 2-day protocols. BJU Int. 2016;117(6):890–6.CrossRefPubMed
22.
go back to reference Leijte JA, Hughes B, Graafland NM, Kroon BK, Olmos RA, Nieweg OE, Corbishley C, Heenan S, Watkin N, Horenblas S. Two-center evaluation of dynamic sentinel node biopsy for squamous cell carcinoma of the penis. J Clin Oncol. 2009;27(20):3325–9.CrossRefPubMed Leijte JA, Hughes B, Graafland NM, Kroon BK, Olmos RA, Nieweg OE, Corbishley C, Heenan S, Watkin N, Horenblas S. Two-center evaluation of dynamic sentinel node biopsy for squamous cell carcinoma of the penis. J Clin Oncol. 2009;27(20):3325–9.CrossRefPubMed
23.
go back to reference Kroon BK, Horenblas S, Meinhardt W, van der Poel HG, Bex A, van Tinteren H, Valdés Olmos RA, Nieweg OE. Dynamic sentinel node biopsy in penile carcinoma: evaluation of 10 years experience. Eur Urol. 2005;47(5):601–6.CrossRefPubMed Kroon BK, Horenblas S, Meinhardt W, van der Poel HG, Bex A, van Tinteren H, Valdés Olmos RA, Nieweg OE. Dynamic sentinel node biopsy in penile carcinoma: evaluation of 10 years experience. Eur Urol. 2005;47(5):601–6.CrossRefPubMed
Metadata
Title
Accuracy of dynamic sentinel lymph node biopsy for inguinal lymph node staging in cN0 penile cancer
Authors
Juanito Gebruers
Laura Elst
Marcella Baldewijns
Liesbeth De Wever
Koen Van Laere
Maarten Albersen
Karolien Goffin
Publication date
01-12-2023
Publisher
Springer Berlin Heidelberg
Published in
EJNMMI Research / Issue 1/2023
Electronic ISSN: 2191-219X
DOI
https://doi.org/10.1186/s13550-023-01013-1

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