Introduction. Methods and materials. 68 Ga-DOTATATE PET CT imaging in carotid body paragangliomas. Patients
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1 SHORT COMMUNICATION 68 Ga-DOTATATE PET CT imaging in carotid body paragangliomas Duygu Has Şimşek 1 Yasemin Şanlı 2 Serkan Kuyumcu 2 Bora Başaran 3 Ayşe Mudun 2 Received: 10 February 2018 / Accepted: 18 February 2018 / Published online: 21 February 2018 The Japanese Society of Nuclear Medicine 2018 Abstract Objective The aim of this study was to present our experience in the baseline evaluation of carotid body paragangliomas (CBP) with 68 Ga-DOTATATE PET CT. Methods Five patients (4F, 1M; age years) with CBPs who underwent 68 Ga-DOTATATE PET CT scan before the treatment were evaluated retrospectively. PET CT images were analyzed visually as well as semiquantitatively, with measurement of maximum standardized uptake value (SUV max ). Results All patients had unilateral CBP lesion, showed intense 68 Ga-DOTATATE uptake in PET CT. Additionally, 68 Ga- DOTATATE avid lesions were found in two patients. One of them had focal intense uptake in thyroid gland and frontal cerebrum. The other one had intense uptake in bone and adrenal mass. Four patients were operated for unilateral primary CBP. Last patient was treated with peptide receptor radionuclide therapy ( 177 Lu-DOTATATE) for both metastatic pheochromocytoma and CBP. Conclusions 68 Ga-DOTATATE PET CT is a valuable imaging modality for staging of CBPs, detecting unknown lesions and changing the management of patients. It is also useful in demonstrating expression of SSTRs for PRRT opportunity. Keywords Carotid body paragangliomas 68 Ga-DOTATATE PET CT Introduction Carotid body paragangliomas (CBP) are rarely seen tumors representing less than 0.5% of all head and neck tumors. Despite being rare, CBPs constitute the majority of head and neck paragangliomas (HNPs) [1]. CBPs arise from the parasympathetic paraganglia found at the carotid bifurcation which can cause pressure changes in hypoglossal vagal nerves and the sympathetic chain [2]. The extensive vascularity of these tumors can become challenging for surgery which is the gold standard for curative therapy. Most of the CBPs are benign lesions, but malignant forms are seen in approximately 5% of cases [3]. The accurate staging of CBPs * Duygu Has Şimşek dr.duyguhas@hotmail.com Department of Nuclear Medicine, Şişli Hamidiye Etfal Training and Research Hospital, Halaskargazi Street, Şişli, Istanbul, Turkey Department of Nuclear Medicine, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Turkey Department of Otorhinolaryngology, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Turkey is very important because the malignant potential of tumor is not predictable from histological characteristics, and malignancy is established with present locoregional or distant metastasis of tumor. Conventional imagings like ultrasound, CT, MRI and arteriography have been used for diagnosis of CBPs. Recently 68 Ga-DOTATATE are PET tracers for somatostatin receptor (SSTR) imaging and have been used widely in neuroendocrine tumors (NET) with higher sensitivity and specificity [4, 5]. Although the diagnostic power of 68 Ga-DOTATATE PET CT is well known in NETs, the role in CBPs is uncertain due to limited numbers of patients with these rarely tumors. Therefore, we aimed to show our 68 Ga-DOTATATE PET CT results for the baseline evaluation of CBP. Methods and materials Patients A total of 878 patients who underwent 68 Ga-DOTATATE PET CT scan at our institute between April 2012 and December 2017 were reviewed and five patients with CBPs Vol.:( )
2 298 Annals of Nuclear Medicine (2018) 32: (four females, one male) included this retrospective study. Written informed consent was obtained from all patients. All scans were done before the treatment. Conventional imagings including US, CT, MRI, CT angiography and 123 I-metaiodobenzylguanidine (MIBG) were also evaluated in addition to PET CT results. All patients had histologically confirmed CBP, one patient by biopsy, four patients by surgery. 68 Ga DOTATATE synthesis and PET CT acquisition We performed 68 Ga-DOTATATE labeling according to protocol as described in the literature [6]. 68 Ga-DOTATATE PET CT was performed at min after the intravenous injection of approximately 175 MBq of 68 Ga-DOTATATE on a dedicated PET CT scanner (Biograph TruePoint PET/ CT; Siemens Healthcare. Erlangen, Germany). An iodinebased oral contrast agent was administered to all patients. CT acquisition was performed on a spiral CT scanner, with a slice thickness of 4 mm and a pitch of 1. After CT scan, 3D-PET images were acquired for 4 min per bed (totally 6 8 beds) in the same position. CT-based attenuation correction of the emission images was used. PET images were reconstructed by the iterative method using ordered-subset expectation maximization (OSEM; two iterations and eight subsets). After completion of the PET acquisition, the reconstructed attenuation-corrected PET images, CT images, and fused images of PET and CT images were reviewed. Fig. 1 A 28-year-old woman with painless right carotid body mass was scanned with Ga68-DOTATATE PET CT. Axial CT (a), axial fusion (b) and maximum-intensity-projection image (c) of Ga68- DOTATATE PET CT scan showed intense uptake (SUV max 54.9) in right CBP and no other focus of abnormal tracer uptake is noted. The patient was operated successfully Image analysis The images were evaluated visually by two experienced nuclear medicine physicians. Areas of abnormally increased tracer uptake were documented. For semiquantitative analysis of activity, a regions of interest (ROIs) analysis was performed for the lesions on PET images and sizes were calculated for the lesions on CT images. Results All patients underwent 68 Ga-DOTATATE PET CT scans. Four of them were scanned for staging of primary CBPs. The last patient was evaluated with 68 Ga-DOTATATE for adrenal mass, which had showed mild uptake in 123 I-MIBG scintigraphy. All patients had unilateral CBP lesion, showed intense 68 Ga-DOTATATE uptake in PET CT (Figs. 1, 2, 3). Additional 68 Ga-DOTATATE avid lesions were found in two patients. One patient had focal intense uptake in thyroid gland and frontal cerebrum. Papillary thyroid cancer was confirmed with biopsy. The patient had undergone total thyroidectomy and received 131 I therapy. In addition, Fig. 2 A 37-year-old woman with right CBP was referred for Ga68- DOTATATE PET CT for baseline evaluation. Axial CT (a), axial fusion (b) and maximum-intensity-projection image (c) of Ga68- DOTATATE PET CT scan showed intense uptake (SUV max 153.4) in right carotid body mass. No other focus of abnormal tracer uptake is detected and tumor was resected totally 68 Ga-DOTATATE avid right frontal cerebrum lesion was accepted meningioma with MRI findings. Patient was
3 299 Fig. 3 A 40-year-old man with right CBP was referred for 68 Ga- DOTATATE PET CT for primary staging. Axial CT (a), axial fusion (b) and maximum-intensity-projection image (c) of 68-Ga-DOTA- TATE PET CT scan showed intense uptake (SUV max 127.9) in right carotid body mass. The patient was operated without any complication asymptomatic, evaluated by neurosurgery and decided to follow up without surgery (Fig. 4). In addition to unilateral CBP, intense uptake was observed in adrenal mass and bone lesions on the other patient. 68 Ga-DOTATATE avid right adrenal mass was found as pheochromocytoma and bone lesions were found pheochromocytoma metastasis by histopathologic confirmation (Fig. 5). Patient was treated with peptide receptor radionuclide therapy ( 177 Lu-DOTATATE) for both metastatic pheochromocytoma and CBP. All patients were followed up for at least 6 months with clinical and imaging findings. Details of patient findings are summarized in Table 1. Discussion CBPs are rare and mostly benign tumors but malignant forms can be seen in approximately 5% of patients [3]. The accurate staging of CBP is very important because the malignant potential of tumor is not predictable from histological characteristics, and malignancy is established in the presence of locoregional or distant metastasis. Conventional imagings like ultrasound, CT, MRI and arteriography have been used for diagnosis of CBPs. Despite the diagnostic advantages of these modalities, distant metastases can be missed in malignant forms. 123 I-MIBG and 111 In-pentetreotide scintigraphy have been used in paragangliomas, scanning whole body with high specificity. Fig. 4 A 73-year-old woman with left CBP underwent Ga68-DOTA- TATE PET CT scan for baseline evaluation. Axial fusion (a) and maximum-intensity-projection image (d) of 68-Ga-DOTATATE PET CT scan showed intense uptake (SUV max 97.5) in left carotid space mass. There was also Ga-68-DOTATATE (+) suspicious thyroid nodule in right lobe (axial fusion, c) diagnosed as papillary thyroid cancer by biopsy, and focal intense Ga68-DOTATATE uptake in right frontal cerebrum, diagnosed meningioma (axial fusion, b) with MRI findings. Patient was operated for CBP and papillary thyroid cancer, and received radioiodine therapy. Frontal meningioma was asymptomatic, decided to follow up without surgery However, the sensitivity was low in smaller lesions due to the limitations in the spatial resolution of gama cameras. Recently 68 Ga-DOTA peptides, PET tracers for SSTR imaging, have been used in NET with higher sensitivity and specificity, providing better resolution and quantification by PET technology [4, 5]. In present study, we retrospectively evaluated 68 Ga- DOTATATE PET CT scans of 5 patients diagnosed CBP. All CBPs and other lesions were detected with PET CT had intense 68 Ga-DOTATATE uptake. Four patients had surgery for primary unilateral CBP without metastasis according to PET CT results confirming benign form of disease. In addition to primary CBP, incidental papillary thyroid cancer and cerebral meningioma were found in a patient, after the evaluation of 68 Ga-DOTATATE uptakes in PET CT scan. That patient had total thyroidectomy and received 30 mci I-131 therapy for pt2n0m0 tumor. The frontal lobe meningioma was asymptomatic, decided to follow up without surgery. It is not uncommon to find incidental 68 Ga-DOTA-peptide avid benign or secondary malignant lesion in 68 Ga-DOTApeptide PET CT scans [6, 7]. 68 Ga-DOTATATE PET CT helped early detection of papillary thyroid cancer avoiding
4 300 Annals of Nuclear Medicine (2018) 32: Fig. 5 A 54-year-old woman with right adrenal mass underwent 68 Ga-DOTATATE PET CT scan. Axial fusion (b) and maximumintensity-projection image (e) of Ga68-DOTATATE PET CT scan showed intense uptake (SUV max 35.9) in right adrenal mass with central necrosis, diagnosed pheochromocytoma by biopsy. In addition, two unknown bone lesions were detected in left iliac crest (axial fusion, c) and 7th thoracic vertebrae (axial fusion, d) showed intense uptake and evaluated pheochromocytoma metastasis with histological confirmation of one lesion. Finally an incidental left carotid body lesion (axial fusion, a) with intense of Ga68-DOTATATE uptake was detected and confirmed CBP histopathologically. Patient received peptide receptor radionuclide therapy for metastatic disease Table 1 The characteristics of patients and 68 Ga-DOTATATE PET CT findings Patient number Sex Age Indication Lesion localization Tumor type 68 Ga-DOTA- TATE uptake (SUV max ) Size (cm) Treatment 1 F 28 Staging Right carotid body Paraganglioma Surgery 2 F 37 Staging Right carotid body Paraganglioma Surgery 3 M 40 Staging Right carotid body Paraganglioma Surgery 4 F 73 Staging Left carotid body Right frontal cerebrum Right thyroid lobe 5 F 54 Metabolic characterization Left carotid body Right adrenal gland Left iliac crest 7th thoracic vertebrae Paraganglioma Meningioma Papillary thyroid cancer Paraganglioma metastasis metastasis Surgery Follow-up Surgery possible metastatic disease and provided curative therapy chance. The most common type of CBPs are sporadic forms, but familial cases can also seen more in than 10% of patients [3, 8]. Lee et al. reported that sporadic PGLs are multifocal in only 10 20%; however, in familial cases, up to 80% are multifocal [9]. Familial cases of PGL have been shown to be caused by germline mutations in three of the four succinate dehydrogenase (SDH) subunit genes, SDHB, SDHC, and SDHD [10, 11]. SDHD mutations are thought to predispose to mostly benign HNPs while SDHB mutations may account for abdominal paragangliomas and phaeochromocytomas [12, 13]. According to our 68 Ga-DOTATATE PET CT results, one patient was diagnosed incidental asymptomatic CBP in addition to adrenal pheochromocytoma and unknown bone metastases which changed the management of disease. It was recommended to search for SDH mutation, but was not accepted by the patient. Depending on the theranostic information of 68 Ga- DOTATATE PET CT, the patient received peptide receptor radionuclide therapy (PRRT) for metastatic disease due to the intense 68 Ga-DOTATATE uptake of tumors. These present findings showed that 68 Ga-DOTATATE PET CT is not only useful for detection of CBPs and metastases, but also demonstrate the expression of SSTRs, providing the proper patient selection for PRRT.
5 There are limited data in literature about diagnoses of CBPs with 68 Ga-DOTA-peptide PET CT. Naswa et al. reported 68 Ga-DOTANOC PET CT results of five patients with CBP and demonstrated two patients had unknown metastases, four patients had bilateral CBPs with intense 68 Ga-DOTANOC uptake [14]. Sharma et al. published a retrospective study of 26 patients with HNPs that 68 Ga- DOTANOC PET CT is superior to 131 I-MIBG scintigraphy and conventional imaging (CT/MR imaging) for baseline evaluation of HNPs including CBP patients who had intense 68 Ga-DOTANOC avidity [15]. Our findings support the previous results confirming high 68 Ga-DOTATATE uptake of all CBP lesions and unknown SSTR(+) lesions with higher sensitivity. Our main limitation was limited number of patients depending on rare occurrence of these tumors. The study was retrospective and only five patients with CBP were included. It seemed that a larger patient population could be enrolled with multicenter studies. Conclusion Our findings showed that 68 Ga-DOTATATE PET CT is a valuable diagnostic tool for staging of CBPs, detecting unknown lesions and changing the management of patients. It is also useful in demonstrating expression of SSTRs for PRRT opportunity. Compliance with ethical standards Conflict of interest The authors have no financial or personal relationships with other people or organizations that could inappropriately influence this work. References 1. Wasserman PG, Savargaonkar P. Paragangliomas: classification, pathology, and differential diagnosis. Otolaryngol Clin North Am. 2001;34(5): Pacheco-Ojeda L. Malignant carotid body tumors: report of three cases. Ann Otol Rhinol Laryngol. 2001;110(1): Sajid M, Hamilton G, Baker D. A multicenter review of carotid body tumour management. Eur J Vasc Endovasc Surg. 2007;34(2): Ambrosini V, Campana D, Bodei L, Nanni C, Castellucci P, Allegri V, et al. 68 Ga-DOTANOC PET/CT clinical impact in patients with neuroendocrine tumors. J Nucl Med. 2010;51(5): Mojtahedi A, Thamake S, Tworowska I, Ranganathan D, Delpassand ES. The value of 68 Ga-DOTATATE PET/CT in diagnosis and management of neuroendocrine tumors compared to current FDA approved imaging modalities: a review of literature. Am J Nucl Med Mol Imaging. 2014;4(5): Kuyumcu S, Özkan ZG, Sanli Y, Yilmaz E, Mudun A, Adalet I, et al. Physiological and tumoral uptake of 68 Ga-DOTATATE: standardized uptake values and challenges in interpretation. Ann Nucl Med. 2013;27(6): Hofman MS, Lau WE, Hicks RJ. Somatostatin receptor imaging with 68 Ga DOTATATE PET/CT: clinical utility, normal patterns, pearls, and pitfalls in interpretation. Radiographics. 2015;35(2): Yao L, Schiavi F, Cascon A, Qin Y, Inglada-Pérez L, King EE, et al. Spectrum and prevalence of FP/TMEM127 gene mutations in pheochromocytomas and paragangliomas. JAMA. 2010;304(23): Lee JH, Barich F, Karnell LH, Robinson RA, Zhen WK, Gantz BJ, et al. National Cancer Data Base report on malignant paragangliomas of the head and neck. Cancer. 2002;94(3): Astuti D, Latif F, Dallol A, Dahia PL, Douglas F, George E, et al. Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am J Hum Genet. 2001;69(1): Niemann S, Müller U. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat Genet. 2000;26(3): Baysal B. Hereditary paraganglioma targets diverse paraganglia. J Med Genet. 2002;39(9): Benn DE, Croxson MS, Tucker K, Bambach CP, Richardson AL, Delbridge L, et al. Novel succinate dehydrogenase subunit B (SDHB) mutations in familial phaeochromocytomas and paragangliomas, but an absence of somatic SDHB mutations in sporadic phaeochromocytomas. Oncogene. 2003;22(9): Naswa N, Kumar A, Sharma P, Bal C, Malhotra A, Kumar R. Imaging carotid body chemodectomas with 68 Ga-DOTA-NOC PET-CT. Br J Radiol. 2012;85(1016): Sharma P, Thakar A, KC SS, Dhull VS, Singh H, Naswa N, et al. 68 Ga-DOTANOC PET/CT for baseline evaluation of patients with head and neck paraganglioma. J Nucl Med. 2013;54(6):841 7.
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