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.
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
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).
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.
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.
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 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.
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.
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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: firstname.lastname@example.org 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.
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|
|Date:||Oct 1, 2018|
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