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Diagnostic Value of [.sup.18]F-FDG PET/CT in Patients with Carcinoma of Unknown Primary/Primeri Bilinmeyen Kanserlerde [.sup.18]F-FDG PET/BT'nin Tanisal Degeri.

Introduction

Carcinoma of unknown primary (CUP) refers to the presence of metastatic disease for which the site of the primary lesion remains unidentified after conventional diagnostic procedures. CUP accounts for approximately 2.3-4.2% of cancer in both men and women (1,2). The mean survival is between 3-11 months, and only 25% of patients survive over one year (3,4). Several studies have shown that survival of patients in whom the primary tumor has been detected was higher than that of patients in whom the primary tumor has remained unknown (5,6). Various radiologic methods and serum tumor markers can be used for primary tumor detection. However, the primary tumor could be detected in less than 20% of patients with CUP (1). Although spontaneous regression or immune-mediated destruction of primary tumor or the small size of a primary tumor may be an explanation, it is not yet fully understood why primary tumors remain undetected (2,7,8).

Several studies reported that [.sup.18]F-fluorodeoxyglucose (FDG) positron emission tomography/computed tomography (PET/CT) has higher sensitivity than other imaging methods for detection of the primary tumor (9,10,11).

The aim of this retrospective study is to evaluate to primary tumor detection efficiency of [.sup.18]F-FDG PET/CT in patients with CUP.

Materials and Methods

Patient Population

All patients who have been referred to our department for [.sup.18]F-FDG PET/CT with a diagnosis of CUP from April 2013 to March 2016 were retrospectively evaluated. Patients who had inadequate medical records or irregular clinical follow-up data and who had chemotherapy before imaging were excluded. 121 patients (79 men, 42 women, age range 30-86 years, mean 63[+ or -]12 years) were analyzed finally in the study. Ninety five out of 121 patients were proved to have metastases histopathologically and 26 patients had highly suspicious metastases by conventional imaging [8 patients with multiple lung metastases detected by C T, 10 patients with multiple bone metastases detected by scintigraphy and/or magnetic resonance imaging (MRI), 5 patients with multiple liver metastases by MRI and/or US, and 3 patients with brain metastases detected by MRI]. Locations of the metastatic foci that have been proven histologically were as follows; 36 in lymph nodes, (21 cervical, 6 supraclavicular, 4 axillary, 2 mediastinal, 2 inguinal, 1 retroperitoneal), 19 in liver, 13 in bone, 6 in brain, 3 in soft tissue, 1 in adrenal gland, 1 in lung, 9 patients had peritoneal implants or malignant ascites, 6 patients had malignant pleural effusion and 1 patient had malignant pericardial effusion. The study were approved by the Adnan Menderes University of Local Ethics Committee (protocol number: 2017/1043).

[.sup.18]F-FDG PET/CT Imaging

All patients underwent [.sup.18]F-FDG PET/CT imaging after 6-8 hours of fasting. Before injection of [.sup.18]F-FDG, the medical history, weight and blood sugar level of the patients were recorded. All patients' blood sugar levels were less than 180 mg/dL prior to imaging. Oral contrast was given to all patients. After intravenous administration of 270-370 MBq of [.sup.18]F-FDG, patients rested in a quiet room. Imaging was performed after a resting period of 60 minutes with (Siemens Biograph mCT 20 Excel) PET/CT scanner. Images were acquired from the head to the feet. The CT transmission scan was acquired with 140 kVp and 110 mA and 3 mm slice thickness. PET scan was acquired at 2-4 min per bed position. [.sup.18]F-FDG PET/CT images were evaluated both visually and semi-quantitatively by two nuclear medicine physicians. Abnormal [.sup.18]F-FDG uptake ([SUV.sub.max] [greater than or equal to]2.5) with an anatomical correlation in any tissue or organ other than the metastases sites was considered as the primary site. The final results were confirmed either histopathologically or by clinical follow up including other imaging methods.

Data Analysis and Statistical Evaluation

The final diagnosis was considered true-positive (TP) when [.sup.18]F-FDG PET/CT detected the primary tumor and it was confirmed histopathologically and/or by clinical follow up. If it was not confirmed to be malignant histopathologically then the result was considered as false-positive (FP). If [.sup.18]F-FDG PET/CT could not detect the primary tumor and it remained unknown in follow up, the result was considered true-negative (TN). When [.sup.18]F-FDG PET/CT did not suggest any primary tumor but it was diagnosed with conventional work-up or in the patient's follow-up, the result was considered as false-negative (FN).

Sensitivity, specificity rates and accuracy were calculated using standard statistical formulas:

Sensitivity=TP/(TP+FN), Specificity=TN/(TN+FP), Accuracy=(TP+TN)/(TP+FP+TN+FN).

Results

Primary tumors were correctly detected in 59 of 121 patients (49%) by [.sup.18]F-FDG PET/CT whole body imaging. The primary tumor locations were as follows; lung (n=31), breast (n=3), stomach (n=1), colon (n=4), pancreas (n=2), ovary (n=3), prostate (n=4), liver (n=2), endometrium (n=1), skin (n=2), thyroid (n=2), larynx (n=1), hypopharynx (n=1), salivary gland (n=1) and bone marrow (multiple myeloma; n=1). In a patient, two primary tumors (colon and prostate) were detected by PET/CT imaging both of which were confirmed histopathologically (Figure 1). In this patient, the bone marrow biopsy revealed metastatic prostate carcinoma thus the colon carcinoma was accepted as a synchronous second primary tumor. Fifty-nine TP results were selected for statistical evaluation. The [SUV.sub.max] of the hyper-metabolic lesions were between 3 to 27 (mean 11.57[+ or -]6.1). TP results are reported in Table 1.

The sensitivity, specificity rates and accuracy of [.sup.18]F-FDG PET/CT in detection of primary tumor were identified as 84%, 78% and 82%, respectively. When 36 patients with lymph node metastases were evaluated separately, primary tumors were correctly identified in 14 out of 36 patients. In these cases, the sensitivity, specificity and accuracy were calculated as 66%, 75% and 70%, respectively.

There were eleven patients in whom primary tumors were reported incorrectly by [.sup.18]F-FDG PET/CT imaging. These results were accepted as false-positive (Table 2). A false-positive case is presented in Figure 2.

The primary tumor could not be identified in 51 (42%) patients. Forty of these patients were TN. The remaining 11 patients, [.sup.18]F-FDG PET/CT did not detect any lesion but the primary tumors were detected during clinical follow-up (mean 6.8 months, range: 2-30 months). These FN results are listed in Table 3.

Additional distant metastases were detected in 45 out of 59 (76%) patients whose primary tumors were detected correctly by [.sup.18]F-FDG PET/CT. In patients with only lymph node metastases, additional solid organ metastases were detected in 5 patients out of 36 (14%) with PET/CT imaging.

Discussion

CT and MRI have been the imaging methods of choice in clinical practice in patients with CUP. Although they detect anatomical abnormalities with pathologic contrast enhancement, small or non-enhancing lesions can be overlooked (1). [.sup.18]F-FDG PET/CT is gaining acceptance as an imaging method to be used in the management of patients with CUP. Small lesions can be detected with higher sensitivity due to its high lesion-to-background contrast. Several studies reported that [.sup.18]F-FDG PET/CT is more sensitive than CT and MRI in the imaging of CUP. In a study, Gutzeit et al. (12) have shown that CT alone indicated a primary tumor in only 8 of 45 patients (18%) while [.sup.18]F-FDG PET/CT detected the primary site in 15 of 45 patients (33%). In another study, Roh et al. (13) have reported that the sensitivity rate of [.sup.18]F-FDG PET/CT (87.5%) was significantly higher than that of CT (43.7%) for the primary tumor in patients with cervical metastases from unknown origin. In several studies, primary tumor detection rate ranged between 24.5-53% for [.sup.18]F-FDG PET/CT in patients with CUP (11,14,15,16). Consistent with the literature, in this study, primary tumors were correctly detected in 59 of 121 patients (49%) by [.sup.18]F-FDG PET/CT whole body imaging. The sensitivity, specificity rates and accuracy of [.sup.18]F-FDG PET/CT in detection of primary tumor were identified as 84%, 78% and 82%, respectively. Han et al. (17) reported the sensitivity, specificity and accuracy of [.sup.18]F-FDG PET/CT in patients with CUP as 91.5%, 85.2% and 88.3%, respectively. In another study, the sensitivity, specificity and accuracy of [.sup.18]F-FDG PET/CT in detection of primary tumor were reported as 80%, 74% and 78%, respectively (18). In our study, [.sup.18]F-FDG PET/CT was the first imaging method used for detecting the primary in majority of the patients. Although the role of [.sup.18]F-FDG PET/CT as the first line imaging of patients with CUP is yet to be established, it has significant advantages. Whole body imaging demonstrates disease extent in addition to detection of the primary tumor, eliminates the need for further imaging and other invasive procedures. Thus, it prevents delay in starting appropriate treatment (19,20).

Lung, oropharyngeal and pancreatic cancers were reported to be most common primary tumors in patients with CUP (21). In our study, lung (52%) and colon (8%) were the most common sites for primary tumors. Colorectal cancer is the third most common cancer in women and the fourth in men in our country (22). Although there were 21 patients with cervical lymph node metastases in our study, we detected 5 head and neck tumors as true-positive. The most important limitation of [.sup.18]F-FDG PET/CT is that it's not a specific tumor imaging technique. Inflammatory lesions or benign tumors with high tracer uptake are the most common causes of false-positive results. In our study, there were eleven false-positive results related to benign tumors or inflammation. In a meta-analysis, authors reported that oropharynx and the lung are the two most common locations of false-positive [.sup.18]F-FDG PET/CT results (21). Inflammatory lesions, pulmonary infarction and emboli have been reported as etiologies for false-positive results in the lung (2,12). In this study, 3 out of the 11 false-positive results were detected in the lung. Pulmonary alveolar proteinosis, hamartoma and inflammation were the final diagnosis in these patients. PET/CT diagnosed a false-positive colon cancer in three patients. The final diagnoses were polyps in two patients and diverticulitis in one patient, that were confirmed histopathologically. In a study, the authors concluded that if [.sup.18]F-FDG PET/CT findings are positive, a confirmatory biopsy is necessary due to false-positive results (23).

In our study, [.sup.18]F-FDG PET/CT could not detect the primary tumor in 42% of patients. Primary tumors were detected on follow-up in 11 out of 51 patients and were considered as FN. Small and low grade tumors with low [.sup.18]F-FDG uptake may result in FN findings. Breast and oropharynx are the most common sites for FN [.sup.18]F-FDG PET/CT imaging (21). In this study, a small primary breast cancer was detected by MRI and was histopathologically diagnosed as invasive ductal cancer following a FN [.sup.18]F-FDG PET/CT imaging. In four patients, lung tumors with low [.sup.18]F-FDG avidity caused FN results.

Whole body [.sup.18]F-FDG PET/CT is also useful in detecting the extent of metastatic disease which may have important implications for clinical management. It is especially important in patients with initial lymph node metastases (2,24). We showed additional solid organ metastases in 5 out of 36 (14%) patients with CUP who presented with lymph node metastases on PET/CT imaging.

Conclusion

Whole body [.sup.18]F-FDG PET/CT is an effective method for detecting the primary tumors in patients with CUP. Additionally, it can also determine disease extent and contribute significantly to clinical patient management.

Ethics

Ethics Committee Approval: The study were approved by the Adnan Menderes University of Local Ethics Committee (protocol number: 2017/1043).

Informed Consent: Consent form was filled out by all participants.

Peer-review: Externally peer-reviewed.

Authorship Contributions

Surgical and Medical Practices: A.C., S.G., Y.Y., Concept: A.C., Design: A.C., S.G., Y.Y., Data Collection or Processing: A.C., S.G., Y.Y., Analysis or Interpretation: A.C., Y.Y., Literature Search: A.C., Writing: A.C., Y. Y.

Conflict of Interest: No conflict of interest was declared by the authors.

Financial Disclosure: The authors declared that this study received no financial support.

References

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(22.) Aykan N F, Yalcin S, Turhal NS, Ozdogan M, Demir G, Ozkan M, Yaren A, Camci C, Akbulut H, Artac M, Meydan N, Uygun K, Isikdogan A, Unsal D, Ozyilkan O, Arican A, Seyrek E, Tekin SB, Manavoglu O, Ozet A, Elkiran T, Disci R. Epidemiology of colorectal cancer in Turkey: A cross-sectional disease registry study (A Turkish Oncology Group trial). Turk J Gastroenterol 2015;26:145-153.

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iD Arzu Cengiz, iD Sibel Goksel, iD Yakup Yurekli

Adnan Menderes University Faculty of Medicine, Department of Nuclear Medicine, Aydin, Turkey

Address for Correspondence: Arzu Cengiz MD, Adnan Menderes University Faculty of Medicine, Department of Nuclear Medicine, Aydin, Turkey E-mail: arzukincengiz@gmail.com ORCID ID: orcid.org/0000-0003-2110-4450

Received: 22.04.2018 Accepted: 04.09.2018

[c]Copyright 2018 by Turkish Society of Nuclear Medicine Molecular Imaging and Radionuclide Therapy published by Galenos Yayinevi.

DOI:10.4274/mirt.64426
Table 1. There were fifty-nine patients with sixty true-positive
results diagnosed by [.sup.18]F-fuorodeoxyglucose positron emission
tomography/computed tomography

    Age and  Location of           Histopathologic/radiologic
    gender   metastases                   metastases

 1  68, M    Bone                Adenosquamous
 2  70, M    Liver               Malignant epithelial tumor met.
 3  49, M    Soft tissue         Malignant epithelial tumor met.
 4  51, F    Bone                Carcinoma
 5  65, F    Pleura              Signet-ring cell carcinoma
 6  59, F    Liver               Malignant epithelial tumor met.
 7  56, M    Bone                Adenocancer
 8  46, F    Supraclavicular LN  Malignant epithelial tumor met.
 9  60, F    Brain               Adenocancer
10  56, M    Liver               Adenocancer
11  68, M    Cervical LN         Neuroendocrine
12  59, F    Bone                Metastatic bone scintigraphy
13  46, M    Soft tissue         Adenocancer
14  59, M    Cervical LN         Squamous cell carcinoma
15  60, F    Bone                Metastatic bone scintigraphy
16  74, M    Cervical LN         Squamous cell carcinoma
17  75, F    Pleural effusion    Malignant
18  70, F    Bone                Malignant epithelial tumor met.
19  72, M    Liver               Malignant epithelial tumor met.
20  35, M    Liver               Adenocancer
21  53, M    Brain               Metastasis on brain MRI
22  39, M    Bone                Adenocancer
23  59, M    Adrenal             Neuroendocrine
24  75, M    Brain               Metastasis on brain MRI
25  52, M    Brain               Malignant epithelial tumor met.
26  74, M    Brain               Neuroendocrine
27  62, F    Liver               Malignant epithelial tumor met.
28  72, M    Liver               Small cell cancer
29  51, M    Liver               Malignant epithelial tumor met.
30  35, F    Pleural effusion    Malignant
31  58, M    Brain               Malignant epithelial tumor met.
32  58, M    Peritoneum          Adenocancer
33  30, M    Peritoneum          Mucinous adeno ca
34  54, M    Peritoneum          Adenocancer
35  63, M    Liver               Metastasis on CT
36  72, M    Bone                Malignant epithelial tumor met.
37  63, M    Bone                Metastasis on MRI
38  64, M    Cervical LN         Adenocancer
39  75, M    Bone                Metastasis on MRI
40  67, F    Axillary LN         Malignant epithelial tumor met.
41  75, F    Bone                Malignant epithelial tumor met.
42  56, F    Bone                Metastatic bone scintigraphy
43  58, F    Cervical LN         Squamous cell carcinoma
44  86, M    Cervical LN         Squamous cell carcinoma
45  69, M    Lung                Metastasis on thorax CT
46  79, F    Liver               Metastasis on MRI
47  75, F    Liver               Malignant epithelial tumor met.
48  77, F    Liver               Malignant epithelial tumor met.
49  66, F    Peritoneum          Malignant epithelial tumor met.
50  64, F    Liver               Malignant epithelial tumor met.
51  64, F    Peritoneum          Adenocancer
52  72, M    Cervical LN         Papillary cancer
53  76, M    Supraclavicular LN  Malignant epithelial tumor met.
54  72, M    Cervical LN         Squamous cell carcinoma
55  70, F    Peritoneum          Carcinomatosis
56  46, F    Supraclavicular LN  Malignant epithelial tumor met.
57  75, F    Lung                Metastasis on thorax CT
58  64, M    Cervical LN         Squamous cell carcinoma
59  63, M    Cervical LN         Squamous cell carcinoma


      Primary tumor

 1  Lung
 2  Lung
 3  Lung
 4  Lung
 5  Lung
 6  Lung
 7  Lung
 8  Lung
 9  Lung
10  Lung
11  Lung
12  Lung
13  Lung
14  Lung
15  Lung
16  Lung
17  Lung
18  Lung
19  Lung
20  Lung
21  Lung
22  Lung
23  Lung
24  Lung
25  Lung
26  Lung
27  Lung
28  Lung
29  Lung
30  Lung
31  Lung
32  Colon
33  Colon
34  Colon
35  Colon
36  Colon and prostate
37  Prostate
38  Prostate
39  Prostate
40  Breast
41  Breast
42  Breast
43  Skin
44  Skin
45  Liver
46  Liver
47  Pancreas
48  Pancreas
49  Ovary
50  Ovary
51  Ovary
52  Thyroid
53  Thyroid
54  Salivary gland
55  Stomach
56  Multiple myeloma
57  Endometrium
58  Larynx
59  Hypopharynx

LN: Lymph node, M: Male, F: Female, met: Metastasis, CT: Computed
tomography, 18F-FDG: 18F-fluorodeoxyglucose, PET/CT: Positron emission
tomography/computed tomography

Table 2. The eleven false-positive results diagnosed by
[.sup.18]F-fuorodeoxyglucose positron emission tomography/computed
tomography

    Age and gender  Location of metastases      PET/CT diagnosis

 1  46, M           Lung                        Hypopharynx cancer
 2  61, F           Inguinal LN                 Endometrial cancer
 3  44, M           Bone                        Lung cancer
 4  53, F           Cervical LN                 Cervix cancer
 5  48, M           Brain                       Lung cancer
 6  80, M           Bone                        Thyroid cancer
 7  85, M           Bone                        Lung cancer
 8  56, M           Liver                       Sigmoid cancer
 9  78, M           Malignant pleural effusion  Colon cancer
10  64, M           Cervical LN                 Colon cancer
11  50, F           Cervical LN                 Thyroid cancer

    Pathology of lesion             True primary site

 1  Cordoma                         CUP
 2  Myoma uteri                     CUP
 3  Pulmonary alveolar proteinosis  CUP
 4  Cervical polyp                  Thyroid papillary cancer
 5  Lung hamartoma                  CUP
 6  Benign nodule                   CUP
 7  Lung inflammation               CUP
 8  Diverticulitis                  CUP
 9  Polyp                           Urinary bladder cancer
10  Polyp                           Prostate cancer
11  Hashimato thyroiditis           CUP

LN: Lymph node, M: Male, F: Female, CUP: Carcinoma of unknown primary,
PET/CT: Positron emission tomography/computed tomography

Table 3. False-negative results of [.sup.18]F-fluorodeoxyglucose
positron emission tomography/computed tomography in patients with
carcinoma of unknown primary

    Age and gender  Location of metastases  Final diagnosis

 1  71, M           Supraclavicular LN      Lung cancer
 2  64, F           Peritoneum              Ovarian cancer
 3  78, M           Pleural fluid           Bladder cancer
 4  52, M           Cervical LN             Laryngeal cancer
 5  65, M           Cervical LN             Laryngeal cancer
 6  50, M           Brain                   Lung cancer
 7  60, F           Liver                   Breast cancer
 8  68, M           Axillary LN             Lung cancer
 9  65, M           Mediastinal LN          Lung cancer
10  60, F           Inguinal LN             Vulvar cancer
11  64, F           Cervical LN             Parotid tumor

    Pathology of primary tumor

 1  Neuroendocrine
 2  Clinical Follow-up
 3  Papillary urothelial low grade tumor
 4  Scc
 5  Scc
 6  Adenocarcinoma
 7  Invasive ductal
 8  Neuroendocrine
 9  Adenocarcinoma
10  Scc
11  Carcinoma ex pleomorphic adenoma

LN: Lymph node, M: Male, F: Female, Scc: Squamous cell carcinoma
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Title Annotation:Original Article; fluorodeoxyglucose; positron emission tomography/computed tomography
Author:Cengiz, Arzu; Goksel, Sibel; Yurekli, Yakup
Publication:Molecular Imaging and Radionuclide Therapy
Article Type:Report
Date:Oct 1, 2018
Words:3842
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