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European Urology
Volume 56, issue 2, pages 237-406, August 2009Penile Cancer
Scanning with 18F-FDG-PET/CT for Detection of Pelvic Nodal Involvement in Inguinal Node-Positive Penile Carcinoma
Niels M. Graafland a 1, Joost A.P. Leijte a 1, Renato A. Valdés Olmos b, Cornelis A. Hoefnagel b, Hendrik J. Teertstra c, Simon Horenblas a 
, 1
Accepted 6 May 2009, Published online 19 May 2009, pages 339 - 345
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Abstract
Background
Penile carcinoma patients with inguinal lymph node involvement (LNI) have an increased risk for pelvic nodal involvement with or without distant metastases.
Objective
To evaluate the diagnostic accuracy of fluorine-18 fluorodeoxyglucose (18F-FDG) positron emission tomography (PET) with computed tomography (CT; 18F-FDG PET/CT) scanning in determining further metastatic spread in patients with tumour-positive inguinal nodes.
Design, setting, and participants
Eighteen patients with penile squamous cell carcinoma with unilateral or bilateral cytologically tumour-positive inguinal disease underwent whole-body 18F-FDG-PET/CT scanning for tumour staging.
Measurements
Images were blindly assessed by two nuclear medicine physicians. All scans were evaluated for pelvic nodal involvement per basin and for distant metastases. Histopathology (when available), radiologic imaging, and clinical follow-up (with a minimum of 1 yr) served as a reference standard. The diagnostic value of PET/CT scanning for predicting pelvic nodal involvement was evaluated using standard statistical methods.
Results and limitations
The reference was available in 28 of the 36 pelvic basins. Of the 11 tumour-positive pelvic basins, 10 were correctly predicted by PET/CT scan, as were all 17 tumour-negative pelvic basins. PET/CT scan showed a sensitivity of 91%, a specificity of 100%, a diagnostic accuracy of 96%, a positive predictive value of 100%, and a negative predictive value of 94% in detecting pelvic nodal involvement. Additionally, PET/CT scans showed distant metastases in five patients. In four patients, the presence of distant metastases could be confirmed, while in one patient, no radiologic confirmation was found for that particular lesion. A potential limitation is that the diagnostic accuracy of PET/CT scanning was calculated on 28 pelvic basins only. Furthermore, no comparison was made with conventional CT scans, as not all patients had undergone contrast-enhanced CT scans.
Conclusions
PET/CT scanning appears promising for detecting pelvic lymph node metastases with great accuracy, and it identifies distant metastases in penile carcinoma patients with inguinal LNI. In our practice, PET/CT scanning has become part of routine staging in such patients.
Keywords: Inguinal node-positive penile cancer, Neoplasm staging, Penile carcinoma, Penile neoplasms, PET/CT scan.
Article Outline
1. Introduction
Penile carcinoma patients with inguinal lymph node involvement (LNI) have an increased risk for further lymphatic spread to the pelvic nodes with or without distant metastases [1], [2], and [3]. The assessment of the pelvic lymph nodes poses a clinical problem. They are not accessible for physical examination, and the role of conventional imaging techniques such as computerized tomography (CT) scans to detect pelvic nodal involvement in penile cancer is limited [4], and [5].
Scanning with fluorine-18-fluorodeoxyglucose (18F-FDG) positron emission tomography (PET) provides functional data on tumour metabolism. This technique identifies areas with increased cellular uptake of glucose and the glucose analogue fluorodeoxyglucose (FDG), one of the key alterations associated with the high glycolytic rate of cancer cells [6]. Although PET has been demonstrated to be of complementary value to morphologic imaging in a number of malignancies [7], and [8], its use in urologic cancers is hampered by the physiologic renal excretion of FDG [9].
In recent years, PET/CT scanners have become available. These modalities acquire both FDG-PET and low-dose CT images with a single scanner, and the data are fused into one image containing both functional and anatomic information. The accuracy of the combined images is reported to be higher than assessment of separate PET and conventional CT images [10], [11], and [12]. It could offer a solution to the problems associated with the renal excretion of FDG by providing anatomic landmarks.
The feasibility of PET/CT scanning in staging penile cancer patients has been demonstrated in a pilot study [13]. The value of this dual-modality imaging in clinically node-negative patients, however, seems limited. In a recent prospective evaluation in staging such patients, only one out of five occult metastases was depicted by PET/CT scans [14]. The aim of the current study was to evaluate the diagnostic accuracy of PET/CT scanning for detecting pelvic nodal involvement and distant metastases in penile carcinoma patients with unilateral or bilateral cytologically proven tumour-positive inguinal nodes.
2. Patients and methods
Between August 2005 until December 2008, 21 penile cancer patients with cytologically proven inguinal LNI (unilateral or bilateral) underwent 18F-FDG-PET/CT scanning for staging in a tertiary referral hospital. Tumour staging was done using the current TNM classification system [15].
Of the 21 patients, three patients with insufficient clinical data (defined as no histopathology of the pelvic nodal basins and no clinical and radiologic follow-up of at least 1 yr) were excluded from the study (see Fig. 1 for an overview). One patient died of pulmonary embolisms 2 wk after inguinal node dissection, and in two patients, no curative treatment was possible because of locally advanced disease. In all three cases, PET/CT scanning and conventional imaging depicted no suspicious pelvic nodes.
00520-X/assets/gr1.jpg)
Fig. 1 Detailed overview of patient inclusion and management. RT = radiotherapy.
Thus, 18 patients were included for this retrospective analysis comprising 12 patients with unilateral tumour-positive inguinal nodes and 6 with bilateral disease. Fourteen patients presented with metastatic disease, and four patients developed an inguinal recurrence after previous treatment for penile cancer. Median age was 62 yr (range: 46–73), and median follow-up was 7 mo (range: 1–31).
2.1. Positron emission tomography/computed tomography scanning
PET/CT scanning was performed using two different hybrid systems. Until September 2006, a mobile PET/CT scanner was used (Biograph II, Siemens, Erlangen, Germany). This scanner has since been replaced by a nonmobile system (Gemini TF, Philips, Amsterdam, Netherlands). Six patients were examined with the mobile system, the remainder with the other system. Both systems permit the acquisition of coregistered CT and PET images in one session. Patients fasted for at least 6 h before intravenous injection of 300–400 MBq (Biograph II) or 180–240 MBq (Gemini TF) of FDG. Approximately 60 min after injection, the images were acquired with the patient in a supine position. No intravenous or oral contrast agents were used. First, a low-dose CT scan (dose modulated with an average of 40-mAs, 140-kV, 5-mm section thickness) from the knee to the head was performed. Immediately after the low-dose CT scan, an FDG-PET emission scan on the basis of 2–3 min per bed position was acquired. PET data were corrected for attenuation using CT.
2.2. Image evaluation
PET/CT images were evaluated for qualitative analysis by two nuclear medicine physicians (RVO and CH) who were unaware of the reference. All scans were assessed for pelvic nodal involvement and for the presence of distant metastases. A lesion was considered malignant if its FDG uptake was found to be above the levels of surrounding tissue on qualitative analysis. Lesions were marked 0, +1, +2, and +3, based on the intensity. Only +2 and +3 lesions were assumed to be malignant.
2.3. Standard of reference
PET/CT scan results were compared with the histopathology of the surgical pelvic nodal specimens. Standard treatment consisted of an inguinal node dissection at the cytologically tumour-positive side. The contralateral node-negative groin was staged using dynamic sentinel node biopsy, which has previously been described in detail [16]. The indication for subsequent pelvic node dissection was made after histopathologic analysis of the removed inguinal specimen. When histopathology revealed extranodal extension of a metastatic node or more than two involved nodes, an ipsilateral pelvic node dissection was performed [17]. All pelvic lymph nodes were analyzed with standardized processing of the specimen with haematoxylin and eosin colouring. The size (ie, the largest diameter) of the nodal metastases was recorded by the pathologist. The technique of an inguinal and pelvic node dissection has been described in detail before [18].
Patients with inguinally confined disease based on the histopathology of the sentinel node or the inguinal node dissection and without evidence of pelvic nodal involvement on the PET/CT scan were observed without pelvic node dissection. In these patients, a minimum follow-up of 12 mo was required as reference.
No histopathology was available of the pelvic basins in patients with disease disseminated beyond the locoregional lymph nodes or patients who received palliative treatment only. PET/CT scan results in these patients were considered true positive when follow-up with conventional radiologic imaging according to the Response Evaluating Criteria in Solid Tumours (RECIST) criteria showed progression of disease [19]. All available radiologic imaging was reviewed by a radiologist (JT) who was unaware of the clinical outcome.
2.4. Statistical analysis
Results of PET/CT scanning were compared with the reference. Using standard statistical methods, we calculated sensitivity, specificity, accuracy, positive predictive value (PPV), and negative predictive value (NPV).
3. Results
After the PET/CT scan, 13 patients were operated on with curative intent, 4 patients were scheduled for chemotherapy (with palliative intent in 1 and neoadjuvant intent in 3), and 1 patient was scheduled for palliative radiotherapy (Fig. 1). All cytologically and clinically tumour-positive inguinal lymph nodes of the 18 patients showed increased FDG uptake. In eight unilateral pelvic basins, no reference was available because of early death in seven and insufficient follow-up in one without histopathology of that basin (Table 1). They were excluded from data analysis. Thus, 28 of the 36 pelvic basins were included in the present study.
Table 1 Details of patients with excluded pelvic basins.
| No. | PET/CT pelvic basin | Ipsilateral inguinal basin | Available clinical data for staging (imaging plus histopathology) | 2002 NM stage* | Clinical outcome | FU, mo | Status** |
|---|---|---|---|---|---|---|---|
| 1 | Nonsuspicious | SN negative | ILND contralateral: positive | cN1M0-pN1Mx | Groin recurrence (tumour-positive side) | 9 | DOD |
| PLND contralateral: negative | |||||||
| No suspicious distant lesions | |||||||
| 2 | Nonsuspicious | SN negative | ILND contralateral: positive | cN3M0-pN3Mx | Pelvic recurrence (tumour-positive side) plus lung metastases | 6 | DOD |
| PLND contralateral: positive | |||||||
| No suspicious distant lesions | |||||||
| 3† | Nonsuspicious | SN negative | ILND contralateral: positive | cN1M0-pN3Mx | Lung metastases | 11 | DOD |
| PLND contralateral: positive | |||||||
| No suspicious distant lesions | |||||||
| 4 | Nonsuspicious | SN negative | ILND contralateral: positive | cN3M0-pN3Mx | Pelvic recurrence (tumour-positive side) | 3 | DOD |
| PLND contralateral: positive | |||||||
| No suspicious distant lesions | |||||||
| 5 | Suspicious | FNAC positive | FNAC contralateral groin: positive | cN3M0-pN + Mx | Chemotherapy failure | 3 | DOD |
| CT contralateral pelvic: positive | |||||||
| Distant lesion: suspicious | |||||||
| MRI: negative | |||||||
| 6 | Nonsuspicious | US negative | FNAC contralateral groin: positive | cN3M1-pN + M1 | Palliative chemotherapy | 8 | DOD |
| CT contralateral pelvic: positive | |||||||
| FNAC distant lesion: positive | |||||||
| 7 | Nonsuspicious | Clinically positive | FNAC contralateral groin: positive | cN3M1-pN + Mx | Palliative RT | 3 | DOD |
| CT contralateral pelvic: positive | |||||||
| CT distant lesions: positive | |||||||
| 8 | Nonsuspicious | SN positive | ILND contralateral groin: positive | cN3M0-pN3Mx | Adjuvant treatment | 1 | Alive |
| PLND contralateral pelvic: positive | |||||||
| No suspicious distant lesions |
CT = computerized tomography; DOD = death of disease; FNAC = fine-needle aspiration cytology; FU = follow-up; ILND = inguinal lymph node dissection; MRI = magnetic resonance imaging; PET = positron emission tomography; PLND = pelvic lymph node dissection; RT = radiotherapy; SN = sentinel node; US = ultrasound.
*
**
†
3.1. Diagnostic accuracy of positron emission tomography/computed tomography scanning in the pelvic region
Of the 11 tumour-positive pelvic basins, 10 were correctly predicted by PET/CT scan, as were all 17 tumour-negative pelvic basins. The calculated sensitivity was 91% (95% confidence interval [CI]: 58–100), with a specificity of 100% (95% CI: 80–100) and a diagnostic accuracy of 96% (95% CI: 82–100). PPVs and NPVs were 100% (95% CI: 69–100) and 94% (95% CI: 73–100), respectively. An example of a true-positive case is provided in Fig. 2. An overview of the PET/CT scan results in relation to the size of the metastases in the pelvic nodes is provided in Table 2.
00520-X/assets/gr2/gr2_584x466.jpg)
Fig. 2 Suspicious lesion in right inguinal region and right pelvic region confirmed by inguinal and pelvic lymph node dissection (big arrows): (A) Overview of positron emission tomography (PET) image (physiologic uptake of fluorodeoxyglucose is seen in both kidneys and the right ureter; see small arrows). Detailed image of the pelvic region by (B) low-dose computed tomography (CT); (C) PET; and (D) PET/CT.
Table 2 Overview of positron emission tomography (PET) with computed tomography (CT) scan results in relation to the size of the tumour in pelvic metastases.
| PET/CT result | Largest diameter of tumour in lymph node |
|---|---|
| False negative | 5 |
| True positives | 9 |
| 23 | |
| 30 | |
| 35 | |
| N/A* |
N/A = not assessable.
*
3.2. Positron emission tomography/computed tomography scanning in screening distant metastases
PET/CT scanning identified areas with increased uptake of FDG thought to represent distant lesions in five patients (see Fig. 3 for an example). In four of these cases, distant metastases were confirmed with fine-needle aspiration cytology (n = 1), thoracic metastasectomy (n = 1), and conventional CT (n = 2). In the remaining 13 patients, no suspicious distant lesions were visualized with PET/CT scans.
00520-X/assets/gr3/gr3_584x473.jpg)
Fig. 3 Suspicious lesion in the left groin but also in the left lung confirmed by histopathology after thoracic metastasectomy (see arrows). (A) Overview of positron emission tomography (PET) image (physiologic uptake of fluorodeoxyglucose is seen in the heart, the stomach, and the small bowel). Detailed image of the lung lesion by (B) low-dose computed tomography (CT); (C) PET; and (D) PET/CT image (respiratory motion has led to a small difference between the CT image and the PET image, which is inevitable).
4. Discussion
Treatment of inguinal metastases from squamous cell carcinoma of the penis is straightforward and consists of inguinal lymph node dissection [2]. Controversy exists on the need for removal of the lymph nodes in the pelvic region. Conventional staging with CT scan is of limited value, with a sensitivity of 37.5% for the identification of pelvic nodal involvement in penile carcinoma [5]. In our practice, the indication for additional pelvic node dissection is based primarily on the histopathologic results of the removed inguinal specimen [17]. With neoadjuvant chemotherapy gaining acceptance in the management of penile cancer patients with pelvic nodal involvement, a need is felt for more accurate staging. This study shows promising results with a sensitivity of 91% and a specificity of 100% in identifying pelvic nodal involvement in penile cancer patients with cytologically proven inguinal LNI.
Although the literature of PET/CT scanning in penile carcinoma is limited, studies evaluating the role of PET/CT scanning in other tumours have shown its superiority compared with CT alone and PET alone [10], [11], and [12]. For example, in 260 patients with solid tumours, the nodal status identified by PET/CT scan was significantly more accurate compared to CT scan (92% vs 76%) [11].
Despite the high accuracy, false-negative findings are inevitable for PET/CT scans because of restricted spatial resolution. In particular, microscopic nodal involvement (<2 mm) cannot be seen with contemporary techniques. The sensitivity increases with the size of the nodal lesion: 16.7% for lesions ≤4 mm, 66.7% for lesions 5–9 mm, and 93.3% for lesions ≥10 mm, as was shown in pelvic and para-aortic nodes of endometrial cancer [20]. The sensitivity is particularly dependent on intranodal tumour burden [12].
An extra advantage of screening patients with whole-body imaging is identification of suspicious distant lesions. In this study, PET/CT scanning was able to visualize suspicious areas eligible for histopathologic confirmation or radiologic follow-up. It is important to consider confirmation of suspicious areas given the potential of false-positive results and excluding a patient from a potentially curative disease [21].
This study has several limitations. First, the retrospective study design and the use of two different PET/CT scanners may have led to bias. Second, the diagnostic accuracy of PET/CT scans was calculated on 28 pelvic basins only. No comparison was made with conventional CT images, as not all the patients underwent contrast-enhanced CT. Based on current knowledge, however, no differences are to be expected in favour of contrast-enhanced CT scan images [10], [11], and [12]. Furthermore, histopathologic analysis of the pelvic basins was available in approximately half of the included basins, as no attempt for surgery was done in patients with overt pelvic or distant disease. Also, consistent with our treatment protocol, no pelvic node dissection was performed when inguinal nodal involvement was negative or minimal. We relied on a follow-up of at least 1 yr in these cases for the assessment of PET/CT scan results. Considering the relatively short follow-up, the diagnostic accuracy could be overestimated.
It has recently been suggested that magnetic resonance imaging with lymphotropic ultrasmall superparamagnetic particles of iron oxide (USPIO) agent ferumoxtran-10 might be highly accurate for staging of both primary penile carcinoma and its lymph node metastases, turning out to be a powerful tool for a one-stop modality in the staging of penile cancer [22]. Recently, this method has also shown potential in detecting pelvic lymph node metastases in normal-sized nodes of bladder or prostate cancer patients [23]. However, these promising data need confirmation in larger studies and particularly in penile carcinoma patients. Furthermore, USPIO is not yet available on the market and is not worthwhile for distant staging, contrary to 18F-FDG-PET/CT scans.
Notwithstanding the aforementioned limitations regarding this study, the encouraging results have led us to incorporate PET/CT scanning in the staging of penile cancer patients with inguinal LNI.
5. Conclusions
PET/CT scanning appears promising in detecting pelvic lymph node metastases with great accuracy and identifies distant metastases in penile carcinoma patients with inguinal LNI. In our practice, PET/CT scanning has become part of routine staging in such patients.
Author contributions: Niels M. Graafland had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Graafland, Leijte, Valdés Olmos, Horenblas.
Acquisition of data: Graafland, Leijte, Valdés Olmos, Hoefnagel, Teertstra, Horenblas.
Analysis and interpretation of data: Graafland, Leijte.
Drafting of the manuscript: Graafland, Leijte.
Critical revision of the manuscript for important intellectual content: Valdés Olmos, Hoefnagel, Teertstra, Horenblas.
Statistical analysis: Graafland, Leijte.
Obtaining funding: None.
Administrative, technical, or material support: None.
Supervision: Horenblas.
Other (specify): None.
Financial disclosures: I certify that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/ affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None.
Funding/Support and role of the sponsor: None.
Acknowledgment statement: The authors acknowledge Hester van Boven (pathologist) for her contribution in analyzing the pathologic data.
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Footnotes
a Department of Urology, The Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands
b Department of Nuclear Medicine, The Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands
c Department of Radiology, The Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands
Corresponding author. Department of Urology, The Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands. Tel. +31 (0)20 5122559; Fax: +31 (0)20 5122554.
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