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Clinical note

The contribution of 18 F-FDG PET/CT in a patient with cutaneous metastases of squamous cell carcinoma of the penis J. Banzo a,∗ , M.A. Ubieto a , A. Andrés b , L. Tardín b , E.F. Rambalde b , L.F. Cancer b , P. Razola b , E. Prats b a b

Unidad PET/TAC, Grupo Hospitalario Quirón La Floresta, Zaragoza, Spain Servicio de Medicina Nuclear, HCU Lozano Blesa, Zaragoza, Spain

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Article history: Received 3 March 2014 Accepted 7 April 2014 Available online xxx Keywords: Squamous cell carcinoma of the penis Cutaneous metastases 18 F-FDG PET/CT

a b s t r a c t A 61-year-old patient was diagnosed with squamous cell carcinoma of the penis (SCCP) and treated with partial penectomy (pT1,N0,M0,G2). Seven months later, a palpable adenopathy was found in the left inguinal region. An 18 F-FDG PET/CT exploration showed hypermetabolic lymphadenopathies in inguinal, pelvic, retroperitoneal regions, in both lung hila and in the left supraclavicular regions. At the end of the 4th cycle of chemotherapy (cisplatin + 5FU) the patient developed numerous skin metastases at the root of the left thigh and a pleural effusion in the right lung. In a new exploration with 18 F-FDG PET/CT the number, size and metabolic activity of known lymphadenopathies decreased. Right pleural carcinomatosis and intense FDG uptake in cutaneous metastases were observed. Weeks later, the patient died. 18 F-FDG-PET/TC may be useful in patients with SCCP and metastatic inguinal lymphadenopathies, to assess the response to chemotherapy and to detect other unsuspected metastases in the rare cases of cutaneous metastases. © 2014 Elsevier España, S.L. and SEMNIM. All rights reserved.

Aportación de la 18 F-FDG PET/TC en un paciente con metástasis cutáneas de un carcinoma de células escamosas de pene r e s u m e n Palabras clave: Carcinoma de células escamosas de pene Metástasis cutáneas 18 F-FDG PET/TC

˜ Paciente de 61 anos diagnosticado de carcinoma de células escamosas de pene (CCEP) tratado mediante penectomía parcial (pT1,N0,M0,G2). Siete meses más tarde, se constata una adenopatía palpable en la región inguinal izquierda. Una exploración 18 F-FDG PET/TC demostró adenopatías hipermetabólicas inguinales, pélvicas, retroperitoneales, en ambos hilios pulmonares y en la región supraclavicular izquierda. Al finalizar el 4◦ ciclo de quimioterapia (cisplatino + 5FU) el paciente desarrolla numerosas letálides en la raíz del muslo izquierdo y un derrame pleural derecho. En una nueva exploración 18 F-FDG ˜ y actividad metabólica de las adenopatías conocidas, PET/TC se apreció disminución del número, tamano carcinomatosis pleural derecha e intensa captación de FDG en las metástasis cutáneas. El paciente fallece semanas más tarde. La 18 F-FDG-PET/TC puede ser útil en pacientes con CCEP y adenopatías inguinales metastásicas, para valorar la respuesta al tratamiento quimioterápico y en los raros casos de metástasis cutáneas para detectar otras metástasis no sospechadas. © 2014 Elsevier España, S.L. y SEMNIM. Todos los derechos reservados.

Introduction Penile cancer is a rare malignancy in Western Europe and USA that supposes the 0.4–0.6% of all tumors, with a higher incidence in the sixth decade of life. Most penile cancers have a squamous epithelial origin, including cancer in situ and the invasive squamous cell carcinoma. Risk factors such as lack of circumcision at an early age, phimosis, smegma accumulation by poor hygiene, infection with the human papilloma virus and xerotic balanitis (lichen sclerosus) are recognized.1 The correct tumor staging according to the TNM classification is essential for

∗ Corresponding author. E-mail addresses: [email protected], alejandro a [email protected] (J. Banzo).

treatment planning and establishing a prognosis. Imaging techniques provide information on the degree of tumor invasion (T), presence of lymph node metastasis (N) and distant metastasis (M). Although there are few data to support the use of 18 F-FDG PET/CT in squamous cell carcinoma of the penis (SCCP), the clinical guidelines developed by the EAU (European Association of Urology)2 and the recommendations of the 2013 CCAFU (Comité Cancérologie de l’Association Franc¸aise d’Urologie)3 include PET/CT as a diagnostic procedure in patients with inguinal lymph node metastases to detect possible pelvic lymph node metastases and distant metastases. We present the findings of an 18 F-FDG PET/CT in a patient with SCCP surgically operated, developing inguinal nodal relapse and subsequently cutaneous metastases and pleural carcinomatosis after four cycles of first-line chemotherapy.

http://dx.doi.org/10.1016/j.remn.2014.04.002 2253-654X/© 2014 Elsevier España, S.L. and SEMNIM. All rights reserved.

Please cite this article in press as: Banzo J, et al. The contribution of 18 F-FDG PET/CT in a patient with cutaneous metastases of squamous cell carcinoma of the penis. Rev Esp Med Nucl Imagen Mol. 2014. http://dx.doi.org/10.1016/j.remn.2014.04.002

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Fig. 1. Exploration 18 F-FDG PET/CT. (A) Maximum intensity projection image: multiple hypermetabolic lymph nodes inguinal, pelvic, retroperitoneal, in both lung hila and in the left supraclavicular region (black arrows). Left uretero-pyelectasis secondary to pelvic limphadenopathies. Reactive bone marrow related to anemia. (B) Images of PET/CT fusion: detail of left supraclavicular lymph node metastasis, retroperitoneal and pelvic (white arrows). (C) CT of PET/CT: edema of the proximal end of the left thigh.

Clinical case A 61-year-old patient diagnosed with SCCP was treated by partial penectomy (pT1, N0, M0, G2). Seven months later, in the follow-up, a palpable adenopathy in the left inguinal region was found. An abdominal-pelvic CT showed multiple left inguinal lymph nodes, the largest of 15 mm in diameter, located ahead of the vascular bundle, without forming a defined conglomerate. An 18 F-FDG PET/CT (Fig. 1) was requested identifying in addition to

inguinal lymphadenopathy associated with edema in the upper third of the thigh, hypermetabolic pelvic lymph nodes along the left iliac region, common, internal and external, and extrapelvic ones in the retroperitoneum, in both lung hila and in the left supraclavicular region (Virchow’s node). Performing a lymphadenectomy was rejected by the Urology Department, so it was decided to start palliative first-line chemotherapy with cisplatin and 5-FU. At the end of the 4th cycle, the patient complained of pain of the left inguinal region and dyspnea of small efforts. Physical examination

Fig. 2. Exploration 18 F-FDG PET/CT after 4 cycles of chemotherapy (cisplatin + 5-FU). (A) Maximum intensity projection image: decreased number, size and metabolic activity of metastatic lymph nodes, numerous skin metastases at the root of the left thigh (black arrows) and right pleural carcinomatosis (white arrow). The left uretero-pyelectasis has been solved. (B) CT of the PET/CT and fusion PET/CT chest image showing hypermetabolic thickening of the thoracic pleura at the middle lobe (white arrow) associated with pleural effusion. (C) Image of fusion PET/CT: detail of the numerous hypermetabolic skin lesions on the root of the left thigh (white arrows). Increased edema of the left thigh.

Please cite this article in press as: Banzo J, et al. The contribution of 18 F-FDG PET/CT in a patient with cutaneous metastases of squamous cell carcinoma of the penis. Rev Esp Med Nucl Imagen Mol. 2014. http://dx.doi.org/10.1016/j.remn.2014.04.002

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revealed numerous skin metastases at the root of the left thigh, and chest radiography showed a right pleural effusion. In a new 18 F-FDG PET/CT scan (Fig. 2) a decrease in the number, size and metabolic activity of known lymphadenopathy, a hypermetabolic thickening of the parietal pleura of the middle lobe accompanied by pleural effusion, and intense FDG uptake in cutaneous metastases and increased edema in the thigh were detected. The patient underwent thoracentesis with a positive pathologic report of squamous carcinoma tumor cells. The pleural effusion progressed and it was necessary to place a permanent drainage. In the following weeks a progressive worsening of the general condition of the patient was observed, and finally he died of acute pulmonary edema. Discussion Unresolved controversies about which imaging procedures should be included in the diagnosis and staging of the SCCP. In this topic has influenced the relatively low incidence of the tumor, the limited number of publications and the absence of randomized clinical trials. The EAU recommends MRI with pharmacologically induced erection by injection into the corpora cavernosa of 10 mg of prostaglandin E1 2 in order to determine the local extent of the tumor. The combination of physical examination and MRI provides the best correlation with histological stage. Histological and molecular characteristics of primary tumor such as histological subtype and grade, lymphatic embolization and/or venous thickness and pattern of tumor growth are the most important variables for predicting inguinal lymph node involvement. The presence of metastases in regional lymph nodes, considering the number and size of involved nodes, both unilateral and bilateral inguinal lymph node metastases, infiltration of the pelvic lymph nodes and the presence of capsular invasion are the main factors to establish an unfavorable prognosis.4 Between 12 and 20% of patients with inguinal clinically palpable lymph nodes (cN0) have occult metastases. Although in these patients the complete inguinal lymph node dissection allows accurate nodal staging in addition to improving survival, the high number of lymphadenectomies without infiltrated lymph nodes and postsurgical complications limit its systematic application without applying risk stratification criteria. The EAU recommends fine needle aspiration (FNA) guided by ultrasound in patients with palpable and non-palpable lymph nodes, and the inguinal lymphadenectomy must be performed when the results of FNA confirmed metastatic lymph node involvement.2,5 In cN0 and FNA negative patients, a selective sentinel node biopsy is the procedure of choice.5 Both CT and MRI have not been recommended in cN0 patients, since they do not detect nodal metastases with low tumor burden and there is low incidence of pelvic lymph node metastases and distant metastases in this group of patients.1 In a recent meta-analysis on the accuracy of 18 F-FDG PET/CT in the diagnosis of inguinal lymph node metastases in the SCCP, Sadeghi et al.6 indicate that the low sensitivity of PET in cN0 patients do not justify its use. Although MRI with lymphotropic nanoparticle can detect subcentimeter lymph node metastases with high sensitivity and specificity, there is insufficient evidence on its clinical implementation.1,5 There is a controversy regarding the need to perform a pelvic lymph node dissection (LND) in patients with SCCP and inguinal lymph node metastases. In a prospective study conducted by Hegarty and colleagues7 of 100 patients with SCCP who were treated according to the recommendations of the UAE, the LND showed metastasis in only 17% of patients; therefore, it is necessary to strengthen the prognostic indicators to improve patient selection. In a group of 142 consecutive patients diagnosed with SCCP, Lughezzani et al.8 analyzed the relationship between the

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characteristics of the inguinal lymph nodes and metastatic pelvic lymph nodes, studying three parameters: number of inguinal nodes involved, the maximum diameter of the nodes and the presence of extracapsular extension. Inguinal metastases in three or more nodes, a diameter equal to or greater than 30 mm in the infiltrated lymph nodes and the extracapsular extension emerge as independent predictors of pelvic lymph node involvement. CT has a low sensitivity for detecting pelvic lymph node metastases, ranging from 20 to 37.5%. In this sense, as noted by Graafland et al.,9 the 18 FFDG PET/CT may be an alternative to CT in detecting pelvic lymph node metastases and even distant metastases in patients with palpable inguinal nodes and positive FNA, particularly in patients who meet the risk criteria. In our patient who presented inguinal nodal relapse 7 months after surgery, the 18 F-FDG PET/CT demonstrated extended pelvic lymph node involvement in the common, internal and external iliac ipsilateral territories and extrapelvic retroperitoneal regions, both lung hila and the left supraclavicular region (Virchow’s node). After 4 cycles of first-line chemotherapy, the patient developed regional cutaneous metastases and right pleural effusion. A new PET/CT showed a partial response of known metastatic lymphadenopathy, pleural carcinomatosis and intense FDG uptake in cutaneous metastases. The skin metastases of SCCP, regional as well as distant, are rare, have a poor prognosis and are often associated with metastases to other organs.10,11 Of the 111 cases of cutaneous metastases secondary to neoplasms of the genitourinary system collected in the review work of Mueller et al.,12 only one case of penile carcinoma is included. The visceral malignancies that most frequently lead to cutaneous metastases arise from breast, lung, colon and ovarian cancer in women, while in man they correspond to colon and head and neck. Moreover, many tumors can metastasize to the penis.13 In conclusion, the 18 F-FDG-PET/CT may be useful in patients with SCCP and metastatic inguinal nodes, to assess the response to chemotherapy and in the rare cases of cutaneous metastases to detect other unsuspected metastases. References 1. Kimberly L, Brady MD, Mercurio MG, Brown MD. Malignant tumors of the penis. Dermatol Surg. 2013;39:527–47. 2. Pizzocaro G, Algaba F, Horenblas S, Solsona E, Tana S, Van Der Poel H, et al. EAU penile cancer guidelines 2009. Eur Urol. 2010;57:1002–12. 3. Rigaud J, Acancès C, Camparo P, Durand X, Fléchon A, Murez T, et al. CCAFU recommendations 2013: penile cancer. Prog Urol. 2013;23 Suppl. 2:S133–44. 4. Ficarra V, Akduman B, Bouchot O, Palou J, Tobías-Machado M. Prognostic factors in penile cancer. Urology. 2010;76 Suppl. 2A:S66–73. 5. Heyns CF, Mendoza-Valdés A, Pompeo ACL. Diagnosis and staging of penile cancer. Urology. 2010;76 Suppl. 2A:S15–23. 6. Sadeghi R, Gholami H, Zakavi SR, Kakhki VRD, Horenblas S. Accuracy of 18 F-FDG PET/CT for diagnosing inguinal lymph node involvement in penile squamous cell carcinoma. Systematic review and meta-analysis of the literature. Clin Nucl Med. 2012;37:436–41. 7. Hegarty PK, Kayes O, Freeman A, Christopher N, Ralph DJ, Minhas S. A prospective study of 100 cases of penile cancer managed according to European Association of Urology guidelines. BJU Int. 2006;98:526–31. 8. Lughezzani G, Catanzano M, Torelli T, Piva L, Biasoni D, Stagni S, et al. The relationship between characteristics of inguinal lymph nodes and pelvis lymph node involvement in penile squamous cell carcinoma: a single institution experience. J Urol. 2014, http://dx.doi.org/10.1016/j.juro.2013.10.140. 9. Graafland NM, Leijte JAP, Valdés Olmos RA, Hoefnagel CA, Teertstra HJ, Horenblas S. Scanning with 18 F-FDG-PET/CT for detection of pelvic nodal involvement in inguinal node-positive penile carcinoma. Eur Urol. 2009;56:339–45. 10. Padmavathy L, Rao LL, Sylvester, Lakshmi MA, Ethirajan N. In-transit metastases from squamous cell carcinoma penis. Indian J Dermatol. 2012;57:291–3. 11. Van der Merwe A, Zarrabi A, Basson J, Stander J, Heyns CF. Distant cutaneous metastases secondary to squamous carcinoma of the penis. Can J Urol. 2009;16:4498–501. 12. Mueller TJ, Wu H, Greenberg RE, Hudes G, Topham N, Lessin SR, et al. Cutaneous metastases from genitourinary malignancies. Urology. 2004;63:1021–6. ˜ F. Diagnóstico de metástasis 13. García JR, Aguilo JJ, Marco V, Valls E, Soler M, Lomena peneana de origen prostático con 11 C-Colina PET. Rev Esp Med Nucl Imagen Mol. 2012;31:295–6.

Please cite this article in press as: Banzo J, et al. The contribution of 18 F-FDG PET/CT in a patient with cutaneous metastases of squamous cell carcinoma of the penis. Rev Esp Med Nucl Imagen Mol. 2014. http://dx.doi.org/10.1016/j.remn.2014.04.002

CT in a patient with cutaneous metastases of squamous cell carcinoma of the penis.

A 61-year-old patient was diagnosed with squamous cell carcinoma of the penis (SCCP) and treated with partial penectomy (pT1,N0,M0,G2). Seven months l...
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