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Reliability of positron emission tomography-computed tomography in evaluation of testicular carcinoma patients/Pouzdanost pozitronske emisione tomografije--kompjuterizovane tomografije uevaluaciji obolelih od karcinoma testisa.

UDK 616.681-006.6-073

Introduction

Testicular carcinoma represents 1% of all cancers in men and it is most common in the age group from 15 to 35 years. Although it is a significant cause of death in this age population, testicular carcinoma is considered curable in more than 90% of all cases [1]. The incidence of testicular cancer has doubled in the last 40 years, with the highest rates in developed countries especially affecting population of white Caucasians [2, 3]. In Europe, the highest incidence has been observed in Denmark with 9.2/100,000 [4].

Generally, all testicular carcinomas are divided into seminomas and nonseminomas. The accurate classification is important because it determines the type of treatment [5]. Seminomas originate from immature reproductive cells; they are usually well differentiated and most commonly seen in the fourth decade of life. Nonseminomas are developed from mature reproductive cells, usually seen in the third decade of life and histologically they represent a mixed type of tumors, such as embryonal cell carcinoma, choriocarcinoma, yolk sac tumor and teratoma. Teratomas are further divided into mature and immature teratomas [5, 6].

Alfa-fetoprotein (AFP), human chorionic gonadotropin (HCG) and lactate dehydrogenaze (LDH) are routinely used tumor markers to make diagnosis, determine prognosis and follow up testicular cancer. AFP is synthesized in the liver cells and the gastrointestinal tract of the fetus. High values of this marker in adults raise suspicion of nonseminoma (AFP is elevated in 65% of patients with nonseminoma), although it can be elevated in seminoma with some elements of nonseminoma [7]. AFP is usually not elevated in pure seminomatous tumors. Placental trophoblast produces HCG immediately after the implantation of a fertilized egg into the uterine wall. HCG is a more specific tumor marker for nonseminomas (elevated in 60% of patients with advanced nonseminoma), but is also raised in 10-20% of seminomas [8, 9]. Although LDH is a less specific marker, its level reflects the growth rate and tumor burden. A high level of LDH is seen in most patients with the advanced stage of seminoma or nonseminoma [10].

In addition to the levels of AFP, HCG and LDH, physical examination of the patient and testicuar ultrasound are necessary to diagnose testicular cancer. It has been reported that magnetic resonance imaging (MRI) can distinguish between seminomas and nonseminomas; however, this is not clinically relevant since orchiectomy is performed as primary treatment [11, 12].

Computed tomography (CT) is still the imaging modality of choice in determining the stage of testicular cancer. The main pattern of metastatic spread for testicular cancer is through the lymphatic system from testicular lymph vessels to the retroperitoneal lymph nodes. The size of metastatic lymph node can be from 1 cm up to the large retroperitoneal masses. Huge retroperitoneal masses are easily seen and diagnosed by CT scan, but the determination of a small single lymph node suspicious for metastatic disease is usually extremely difficult. This problem is critical in situations when further patient management depends on a distinction like this, such as distinguishing of stage I from stage II. In the patients with stage I disease, only surveillance is recommended, but the patients with stage II usually need chemotherapy. A great number of studies have reported that between 25% and 30% of patients with testicular cancer have occult metastatic lymph node disease that cannot be detected by CT [13-15].

Rare testicular neoplasms, such as testicular lymphoma, could be evaluated using technetium-99m methoxyisobutyl isonitrile ([sup.99m]Tc-MIBI). This radiopharmaceutical, known for its role in myocardial perfusion scintigraphy, has demonstrated an increased uptake in the skeletal/bone marrow metastases as diffuse and/or focal increased uptake, especially focal/tubular MIBI activity of the femoral marrow [16, 17].

New imaging modalities, such as fluoro-deoxyglucose ([sup.18]F-FDG) positron emission tomographycomputed tomography (PET-CT) may overcome these limitations of CT in detecting small lymph node metastases. Although [sup.18]F-FDG is inferior to other tracers for primary staging of cancers such as testicular, prostate and bladder one, it may be useful in the selected patients with suspected high-grade cancer [18]. The main advantage of [sup.18]F-FDG PET-CT compared to CT is that it is a functional imaging thus providing information about metabolically active lymph nodes. A potential advantage is the ability of [sup.18]F-FDG PET-CT to detect small lymph node metastases that are not identified as enlarged on CT, which could influence the future clinical decision.

The aim of this study was to assess if [sup.18]F-FDG PET-CT scan is reliable in evaluation of testicular carcinoma patients. The study represents a retrospective review of [sup.18]F-FDG PET-CT scans which were recommended by oncologists to be performed in the patients with testicular cancer.

Material and Methods

This retrospective study included the patients with testicular carcinoma referred for PET-CT scan to the Oncology Institute of Vojvodina in a 3-year period (from 2011-2014). A total of 1090 [sup.18]F-FDG PET-CT scans were performed in 850 patients, among them were 26 studies in 23 patients (aged 20-54, their mean age being 35.5 years) with testicular carcinoma. PET-CT was performed following the injection of 241-370 megabecquerel (MBq) of [sup.18]F-FDG. The patients were prepared according to the instructions for fasting for at least 6 hours before the injection, with glucose level from 2.9--8.2 mmol/l at the time of injection. The patients were scanned according to the principles of previously described methodology [19]. All PET-CT scans were performed on 64-slice hybrid PET-CT scanner (Biograph, Siemens) 60-120 minutes after the injection. A 3-dimensional PET scan and low-dose unenhanced CT scan were acquired from the base of the scull to the proximal parts of the femur. CT, PET (attenuation-corrected) and combined PET-CT images were displayed for analysis and interpreted by two nuclear medicine physicians.

The clinical history data were examined in order to compare [sup.18]F-FDG PET-CT results with the pathohistology (PH) reports, clinical examination, CT or any other imaging modality for a minimum of 6 months after [sup.18]F-FDG PET-CT scanning. If there were no data of pathohistology, a stable disease was assumed if CT scan showed no progression of previously known abnormality or if the serum tumor markers were not elevated (AFP, HCG or LDH). Progressive disease was assumed in the patients with an enlargement of previously known CT abnormality, detection of new lesions on any imaging modality or elevation of tumor markers.

The sensitivity, specificity, accuracy, positive and negative predictive values were calculated to determine the diagnostic significance of [sup.18]F-FDG PET-CT in the evaluation of testicular carcinoma.

Results

Clinical data were collected for 23 patients; only one patient was lost for follow up. In most patients, the initial treatment prior to PET-CT was orchiectomy + chemotherapy (17 patients; 73.9%), 2 patients (8.7%) had orchiectomy + chemotherapy + retroperitoneal lymph nodes dissection (RPLND), 3 patients (13.1%) had orchiectomy only (followed by chemotherapy after PET-CT) and only one patient (4.3%) was treated with chemotherapy only (extragonadal seminoma). The pathohistology type of cancer included seminoma (14 patients; 60.9%), nonseminoma (7 patients; 30.4%) and a mixed histological type (2 patients; 8.7%).

The total number of scans performed in 23 patients was 26. The main cause for having been referred to [sup.18]F-FDG PET-CT scan by an oncologist was an abnormality registered on CT (in 19 scans; 73.1%), MRI abnormalities in 1 scan (3.8%), high level of tumor markers in 3 scans (11.5%) and 3 scans (11.5%) were performed for follow-up. Tumor markers were elevated in 3 patients, and two of them had elevated both AFP and HCG (mixed type, and in nonseminoma) and only AFP was elevated in one patient (seminoma). One patient with elevated tumor markers had positive PET scan, he was operated and pathohistology (PH) results confirmed metastases of testicular carcinoma. Two patients had negative scans, one was later assumed to have progressive disase according to much higher levels of tumor markers than at the time of the scan and one was clinically stable.

The results showed positive [sup.18]F-FDG PET-CT scan in 6 (23.1%) and normal in 20 (76.9%) patients. A true positive scan was found in 4 (66.7%), and PET-CT was false positive in two patients (33.3%). True positive [sup.18]F-FDG PET-CT findings were confirmed pathohistologically in two patients (one with seminoma and the other one with nonseminoma), and two patients (both seminoma) were treated with chemotherapy with a significant reduction in the size of retroperitoneal lymph nodes (Figures 1 and 2). The sites of [sup.18]F-FDG accumulation were retroperitoneal, inguinal lymph nodes and a bone (a rib).

A false positive [sup.18]F-FDG PET-CT scan (a patient with embryonal cell carcinoma) registered [sup.18]F-FDG-avid retroperitoneal lymph nodes, after PETCT RPLND was performed and there was no evidence of tumor cells (PH: necrosis) in the PH report (Figure 3). Another false positive [sup.18]F-FDG PET-CT scan reported [sup.18]F-FDG-avid mediastinal lymph nodes, mediastinoscopy of the paratracheal lymph nodes was performed and PH confirmed lymphadenitis granulomatosa non necroticans.

Twenty negative PET-CT scans were performed in 18 patients, one patient was lost for data analysis and the remaining 19 scans in 17 patients were further analyzed. The further follow up (6-36 months) showed clinicaly stable disease in 18 scans (performed in 16 patients) (88.9%) and those scans were considered to be true negative. Pathohistological proof of a [sup.18]F-FDG non-avid CT abnormality was found in one patient. Following a biopsy using bronchoscopy the histopathology showed no evidence of tumor (Figure 4). The patient with false negative [sup.18]F-FDG PET-CT scan (PH: yolk sac choriocarcinoma+mature teratoma) was reffered to [sup.18]F-FDG PET-CT because he had elevated tumor markers (HCG, 12 mU/mL; AFT, 14 IU/mL; LDH was normal). During the 13-month follow-up, tumor markers significantly increased: AFP was reported to be five times higher and HCG 150 times higher.

After [sup.18]F-FDG PET-CT, one out of 23 patients was lost for follow-up and the data were collected for 22 patients. When there was regression or no progression on CT abnormality and no elevation of tumor markers, the disease was clinically stable (14 patients; 63.6%). One of patients from this group was with negative [sup.18]F-FDG PET-CT scan but treated with chemotherapy after the scan because he was referred to chemotherapy by his urologist. If tumor markers continued to rise (1 patient; 4.5%) or there was evidence of progression previously diagnosed or newly detected abnormality on any imaging modality (none of the patients), the patient was considered to have clinically progressive disease. When the patient received chemotherapy after PET-CT with significant regression of tumor mass on any imaging modality, he was considered to have clinical response to therapy (2 patients after chemotherapy; 9.1%). In five patients (22.7%), PH was obtained as a result of operation (3) or invasive diagnostic procedures (2) (Table 1). The sensitivity, specificity, accuracy, positive and negative predictive values were 60%, 95%, 75%, 88% and 90.5%, respectively.

Discussion

The main way of metastatic spread of testicular carcinoma is through the lymphatic vessels. Most frequently, right-sided tumors spread to the aortocaval nodes, precaval nodes and right paracaval and retrocaval nodes, while left-sided tumors usually spread to the left paraaortic nodes and preaortic nodes. CT is still the main imaging modality for staging, evaluation and follow-up of testicular carcinoma patients [20, 21]. However, there are some limitations in the ability of CT to diagnose small volume metastatic disease [22, 23]. Further development in imaging methods may overcome these limitations, specially in the possibility to diagnose small metastases in retroperitoneal lymph nodes, such as [sup.18]F-FDG PET-CT and MRI with lymphotrophic nanoparticles. An important advantage of [sup.18]F-FDG PET-CT as a functional imaging over CT is the possibility to identify metabolically active disease. Albers et al. compared [sup.18]F-FDG PET-CT with CT in staging testicular carcinoma and have suggested that [sup.18]F-FDG PET-CT is useful for detecting viable tumor in lesions detected with CT and it may prevent false-positive diagnosis in stage II [24]. In the patients with testicular cancer in stage I, the same study has shown that PET does not improve staging over the CT [24].

The results of our study have shown that two patients with positive [sup.18]F-FDG PET-CT scan (both seminoma) were succesfully treated with chemotherapy after PET-CT scan. Seminoma is very sensitive to chemotherapy, and after the completion of treatment, residual mass (necrosis, fibrosis) is sometimes present. [sup.18]F-FDG PET-CT has shown to be the best imaging modality in differentiation of such residual mass [25]. De Santis et al. performed PET scan in this group of patients with PH verification after the scan and reported no false-positive findings, suggesting that PET scan is highly specific for tumor viability [25]. In our group of patients, there were two cases with false positive result, when PH confirmed necrotic or granulomatous tissue in [sup.18]F-FDG-avid lymph nodes of retroperitoneum and mediastinum. In the study of 24 PET scans performed in 19 patients, Lewis et al. reported that out of 12 positive scans there were 4 false positive scans that led to surgical resections of residual masses revealing only fibrosis, necrosis or inflammation [26]. Muggia et al. reported a case of false positive mediastinal finding in a patient with seminoma [27]. Many investigators have reported a certain number of false positive PET-CT findings in the follow-up of seminoma cancer patients [26, 28, 29]. In our study, there were 18 normal [sup.18]F-FDG PETCT scans performed in 16 patients, and most of them (15; 93.75%) were true negative, which suggests that normal PET scan was a good predictor of future stable disease. A high negative predictive value of our study (90.5%) suggests that there is a very small possibility for a patient to have future relapse of the disease after negative PET-CT study. Many studies recommend surveillance as a method of choice in the follow-up of patients with negative PET-CT scan because they are unlikely to relaps and do not require any further treatment [30, 31]. However, there are other studies, such as the study performed by Huddart et al, that report a high relapse rate in this group of patients [32]. In our study group, only one false negative [sup.18]F-FDG PET-CT scan was noted in a patient of nonseminoma who was reffered to PET-CT because he had elevated tumor markers. In the 13-month follow-up period, his tumor markers significantly increased since the time of [sup.18]F-FDG PET-CT scan, thus suggesting that the scan was false negative. However, we did not have a chance to perfom a follow-up scan, which is why this false negative scan should be understood tentativley. Hain et al. investigated 23 scans of testicular carcinoma with elevated tumor markers, and found that a subseqent PET-CT was positive in three out of five false negative cases and PET-CT was the first imaging technique to identify the site of recurrence [33]. Therefore, when tumor markers are elevated and imaging findings are normal (including negative PET-CT scan), the most appropriate follow-up imaging may be to repeat PET-CT.

Since patients suffering from testicular carcinoma are mainly young, they should be spared radiation burden as much as possible which is why it is important to choose those imaging techniques providing most appropriate information for future treatment options. Therefore, although CT is still a crucial technique, PET-CT can be helpful in certain clinical situations.

The major limitation of our investigation is a small number of patients as a result of not so frequent pathology among those who are referred to PET-CT. Another limitation is the fact that in some cases etiology was obtained with clinical follow-up instead of pathohistology report. We will try to overcome these limitations in our additional future research work.

Conclusion

The results of our study indicate that [sup.18]F-fluorodeoxyglucose positron emission tomography-computed tomography scan is recommended in the follow-up of patients with testicular carcinoma particularly due to the high probability of normal scan to assure oncologist of low likelihood of relapse of the disease. However, since the sensitivity and positive predictive values of the study are rather low, there are limitations of positive [sup.18]F-fluorodeoxyglucose positron emission tomography-computed tomography scan to suggest persistent disease. Therefore, the oncologist should not rely only on the results of the positron emission tomography-computed tomography scan in making decisions about future treatment of patients with positive positron emission tomography-computed tomography findings.

Abbreviations
AFP     -- [alpha]-fetoprotein
HCG     -- human chorionic gonadotropin
LDH     -- lactate dehydrogenaze
MRI     -- magnetic resonance imaging
CT      -- computed tomography
MIBI    -- methoxyisobutyl isonitrile
FDG     -- fluorodeoxyglucose
PET-CT  -- positron emission tomography--computed
           tomography
PH      -- pathohistology
RPLND   -- retroperitoneal lymph node dissection


DOI: 10.2298/MPNS1504109N

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Katarina NIKOLETIC (1), Jasna MIHAILOVIC1, Emil MATOVINA (1), Radmila ZERAVICA (2) and Dolores SRBOVAN (1)

Oncology Institute of Vojvodina, Sremska Kamenica, Serbia

Department of Nuclear Medicine (1)

Clinical Center of Vojvodina, Department of Nuclear Medicine, Novi Sad, Serbia (2)

Corresponding Author: Dr Katarina Nikoletic, Institut za onkologiju Vojvodine, Centar za nuklearnu medicinu, 21204 Sremska Kamenica, Put dr Goldmana 4, E-mail: ketins@yahoo.com

Rad je primljen 6. VIII 2014. Recenziran 12. I 2015. Prihvacen za stampu 18. II 2015. BIBLID.0025-8105:(2015):LXVIII:3-4:109-115.

Table 1. Characteristics of patients with testicular carcinoma
(S=seminoma, NS=nonseminoma, M=mixed type) according to type of
follow up.

Tabela 1. Karakteristike pacijenata sa testikularnim karcinomom (S =
seminom, NS = nonseminom, M = meso-viti tip) prema vrsti pracenja

Patients    PH tumor type     Type of follow up
Pacijenti   PH tip tumora     Vrsta pracenja
(22)        S     NS    M

                              PH verification
5           2     3     -     PH verifikacija

1           --    1     --    Clinical progression
                              Klinicka progresija

14          10    2     2     Clinically stable disease
                              Klinicki stabilna bolset

2           2     --    --    Clinical response to therapy
                              Klinicki odgovor na terapiju

Patients    Follow up (months)      Diagnostic significance
Pacijenti   Pracenje (meseci)    Dijagnostizka signifikantnost
(22)

                                              TP=2
5                  6-28                       FP=2
                                              TN=1

1                   13                         FN

14                 6-36                        TN

2                 10-15                        TP

PH--patohistoloski
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Title Annotation:PROFESSIONAL ARTICLES/STRUCNI CLANCI
Author:Nikoletic, Katarina; Mihailovic, Jasna; Matovina, Emil; Zeravica, Radmila; Srbovan, Dolores
Publication:Medicinski Pregled
Article Type:Report
Date:Mar 1, 2015
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