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Kong G, Noe G, Chiang C, Herrmann K, Hope TA, Michael M. Assessment of response to PRRT including anatomical and molecular imaging as well as novel biomarkers. J Neuroendocrinol 2024:e13461. [PMID: 39520276 DOI: 10.1111/jne.13461] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/30/2024] [Revised: 09/05/2024] [Accepted: 10/24/2024] [Indexed: 11/16/2024]
Abstract
Peptide receptor radionuclide therapy (PRRT) is an effective treatment for both oncological and hormone control and is a widely accepted standard of care treatment for patients with neuroendocrine neoplasms (NEN). Its use is anticipated to increase significantly, and this demands accurate tools and paradigms to assess treatment response post PRRT. This article outlines the current role and future developments of anatomical, molecular imaging and biomarkers for response assessment to PRRT, highlighting the challenges and provides perspectives for the need to focus on a multimodality, multidisciplinary and individualised approach for patients with this complex heterogeneous disease.
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Affiliation(s)
- Grace Kong
- Department of Molecular Imaging and Therapeutic Nuclear Medicine, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia
- Sir Peter MacCallum Department of Oncology, University of Melbourne, Melbourne, Victoria, Australia
| | - Geertje Noe
- Department of Cancer Imaging, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia
| | - Cherie Chiang
- Department of Internal Medicine, Peter MacCallum Cancer Centre, Parkville, Victoria, Australia
- Department of Diabetes and Endocrinology, Melbourne Health, University of Melbourne, Parkville, Victoria, Australia
| | - Ken Herrmann
- Department of Nuclear Medicine, University of Duisburg-Essen and German Cancer Consortium (DKTK)-University Hospital Essen, Essen, Germany
| | - Thomas A Hope
- Department of Radiology, San Francisco VA Medical Center, San Francisco, California, USA
- Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, California, USA
| | - Michael Michael
- Sir Peter MacCallum Department of Oncology, University of Melbourne, Melbourne, Victoria, Australia
- Department of Medical Oncology, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia
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Berger F, Ingenerf M, Auernhammer CJ, Cyran C, Ebner R, Zacherl M, Ricke J, Schmid-Tannwald C. [Imaging of pancreatic neuroendocrine tumors]. RADIOLOGIE (HEIDELBERG, GERMANY) 2024; 64:559-567. [PMID: 38789854 DOI: 10.1007/s00117-024-01316-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Accepted: 04/24/2024] [Indexed: 05/26/2024]
Abstract
BACKGROUND Neuroendocrine tumors of the pancreas have a broad biological spectrum. The treatment decision is based on an optimal diagnosis with regard to the local findings and possible locoregional and distant metastases. In addition to purely morphologic imaging procedures, functional parameters are playing an increasingly important role in imaging. OBJECTIVES Prerequisites for optimal imaging of the pancreas, technical principles are provided, and the advantages and disadvantages of common cross-sectional imaging techniques as well as clinical indications for these special imaging methods are discussed. MATERIALS AND METHODS Guidelines, basic and review papers will be analyzed. RESULTS Neuroendocrine tumors of the pancreas have a broad imaging spectrum. Therefore, there is a need for multimodality imaging in which morphologic and functional techniques support each other. While positron emission tomography/computed tomography (PET/CT) can determine the presence of one or more lesions and its/their functional status of the tumor, magnetic resonance imaging (MRI) efficiently identifies the location, relationship to the main duct and the presence of liver metastases. CT allows a better vascular evaluation, even in the presence of anatomical variants as well as sensitive detection of lung metastases. CONCLUSIONS Knowledge of the optimal combination of imaging modalities including clinical and histopathologic results and dedicated imaging techniques is essential to achieve an accurate diagnosis to optimize treatment decision-making and to assess therapy response.
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Affiliation(s)
- Frank Berger
- Klinik und Poliklinik für Radiologie, Klinikum der Universität München, LMU München, München, Deutschland
| | - Maria Ingenerf
- Klinik und Poliklinik für Radiologie, Klinikum der Universität München, LMU München, München, Deutschland
| | - Christoph J Auernhammer
- Medizinische Klinik und Poliklinik 4, Klinikum der Universität München, LMU München, München, Deutschland
- Interdiziplinäres Zentrum für Neuroendokrine Tumoren des GastroEnteroPankreatischen Systems GEPNET-KUM (ENETS certified CoE), München, Deutschland
| | - Clemens Cyran
- Klinik und Poliklinik für Radiologie, Klinikum der Universität München, LMU München, München, Deutschland
- Interdiziplinäres Zentrum für Neuroendokrine Tumoren des GastroEnteroPankreatischen Systems GEPNET-KUM (ENETS certified CoE), München, Deutschland
| | - Ricarda Ebner
- Klinik und Poliklinik für Radiologie, Klinikum der Universität München, LMU München, München, Deutschland
| | - Mathias Zacherl
- Klinik für Nuklearmedizin, Klinikum der Universität München, LMU München, München, Deutschland
- Interdiziplinäres Zentrum für Neuroendokrine Tumoren des GastroEnteroPankreatischen Systems GEPNET-KUM (ENETS certified CoE), München, Deutschland
| | - Jens Ricke
- Klinik und Poliklinik für Radiologie, Klinikum der Universität München, LMU München, München, Deutschland
- Interdiziplinäres Zentrum für Neuroendokrine Tumoren des GastroEnteroPankreatischen Systems GEPNET-KUM (ENETS certified CoE), München, Deutschland
| | - Christine Schmid-Tannwald
- Klinik und Poliklinik für Radiologie, Klinikum der Universität München, LMU München, München, Deutschland.
- Interdiziplinäres Zentrum für Neuroendokrine Tumoren des GastroEnteroPankreatischen Systems GEPNET-KUM (ENETS certified CoE), München, Deutschland.
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Liu YL, Zhu HB, Chen ML, Sun W, Li XT, Sun YS. Prediction of the lymphatic, microvascular, and perineural invasion of pancreatic neuroendocrine tumors using preoperative magnetic resonance imaging. World J Gastrointest Surg 2023; 15:2809-2819. [PMID: 38222000 PMCID: PMC10784819 DOI: 10.4240/wjgs.v15.i12.2809] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/07/2023] [Revised: 11/06/2023] [Accepted: 12/06/2023] [Indexed: 12/27/2023] Open
Abstract
BACKGROUND Significant correlation between lymphatic, microvascular, and perineural invasion (LMPI) and the prognosis of pancreatic neuroendocrine tumors (PENTs) was confirmed by previous studies. There was no previous study reported the relationship between magnetic resonance imaging (MRI) parameters and LMPI. AIM To determine the feasibility of using preoperative MRI of the pancreas to predict LMPI in patients with non-functioning PENTs (NFPNETs). METHODS A total of 61 patients with NFPNETs who underwent MRI scans and lymphadenectomy from May 2011 to June 2018 were included in this retrospective study. The patients were divided into group 1 (n = 34, LMPI negative) and group 2 (n = 27, LMPI positive). The clinical characteristics and qualitative MRI features were collected. In order to predict LMPI status in NF-PNETs, a multivariate logistic regression model was constructed. Diagnostic performance was evaluated by calculating the receiver operator characteristic (ROC) curve with area under ROC, sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV) and accuracy. RESULTS There were significant differences in the lymph node metastasis stage, tumor grade, neuron-specific enolase levels, tumor margin, main pancreatic ductal dilatation, common bile duct dilatation, enhancement pattern, vascular and adjacent tissue involvement, synchronous liver metastases, the long axis of the largest lymph node, the short axis of the largest lymph node, number of the lymph nodes with short axis > 5 or 10 mm, and tumor volume between two groups (P < 0.05). Multivariate analysis showed that tumor margin (odds ratio = 11.523, P < 0.001) was a predictive factor for LMPI of NF-PNETs. The area under the receiver value for the predictive performance of combined predictive factors was 0.855. The sensitivity, specificity, PPV, NPV and accuracy of the model were 48.1% (14/27), 97.1% (33/34), 97.1% (13/14), 70.2% (33/47) and 0.754, respectively. CONCLUSION Using preoperative MRI, ill-defined tumor margins can effectively predict LMPI in patients with NF-PNETs.
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Affiliation(s)
- Yu-Liang Liu
- Department of Radiology, Peking University Cancer Hospital and Institute, Beijing 100142, China
| | - Hai-Bin Zhu
- Department of Radiology, Peking University Cancer Hospital and Institute, Beijing 100142, China
| | - Mai-Lin Chen
- Department of Radiology, Peking University Cancer Hospital and Institute, Beijing 100142, China
| | - Wei Sun
- Department of Pathology, Peking University Cancer Hospital and Institute, Beijing 100142, China
| | - Xiao-Ting Li
- Department of Radiology, Peking University Cancer Hospital and Institute, Beijing 100142, China
| | - Ying-Shi Sun
- Department of Radiology, Peking University Cancer Hospital and Institute, Beijing 100142, China
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Koffas A, Giakoustidis A, Papaefthymiou A, Bangeas P, Giakoustidis D, Papadopoulos VN, Toumpanakis C. Diagnostic work-up and advancement in the diagnosis of gastroenteropancreatic neuroendocrine neoplasms. Front Surg 2023; 10:1064145. [PMID: 36950054 PMCID: PMC10025557 DOI: 10.3389/fsurg.2023.1064145] [Citation(s) in RCA: 10] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/07/2022] [Accepted: 02/07/2023] [Indexed: 03/08/2023] Open
Abstract
Neuroendocrine neoplasms (NENs) are a heterogeneous group of neoplasms ranging from well-differentiated, slowly growing tumors to poorly differentiated carcinomas. These tumors are generally characterized by indolent course and quite often absence of specific symptoms, thus eluding diagnosis until at an advanced stage. This underscores the importance of establishing a prompt and accurate diagnosis. The gold-standard remains histopathology. This should contain neuroendocrine-specific markers, such as chromogranin A; and also, an estimate of the proliferation by Ki-67 (or MIB-1), which is pivotal for treatment selection and prognostication. Initial work-up involves assessment of serum Chromogranin A and in selected patients gut peptide hormones. More recently, the measurement of multiple NEN-related transcripts, or the detection of circulating tumor cells enhanced our current diagnostic armamentarium and appears to supersede historical serum markers, such as Chromogranin A. Standard imaging procedures include cross-sectional imaging, either computed tomography or magnetic resonance, and are combined with somatostatin receptor scintigraphy. In particular, the advent of 111In-DTPA-octreotide and more recently PET/CT and 68Ga-DOTA-Octreotate scans revolutionized the diagnostic landscape of NENs. Likewise, FDG PET represents an invaluable asset in the management of high-grade neuroendocrine carcinomas. Lastly, endoscopy, either conventional, or more advanced modalities such as endoscopic ultrasound, capsule endoscopy and enteroscopy, are essential for the diagnosis and staging of gastroenteropancreatic neuroendocrine neoplasms and are routinely integrated in clinical practice. The complexity and variability of NENs necessitate the deep understanding of the current diagnostic strategies, which in turn assists in offering optimal patient-tailored treatment. The current review article presents the diagnostic work-up of GEP-NENs and all the recent advances in the field.
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Affiliation(s)
- Apostolos Koffas
- Centre for Immunobiology, Blizard Institute, Barts and the London School of Medicine and Dentistry, Queen Mary University of London, London, United Kingdom
- Correspondence: Apostolos Koffas
| | - Alexandros Giakoustidis
- 1st Department of Surgery, General Hospital Papageorgiou, School of Medicine, Faculty of Medical Sciences, Aristotle University Thessaloniki, Thessaloniki, Greece
| | - Apostolis Papaefthymiou
- Pancreaticobiliary Medicine Unit, University College London Hospitals (UCLH), London, United Kingdom
| | - Petros Bangeas
- 1st Department of Surgery, General Hospital Papageorgiou, School of Medicine, Faculty of Medical Sciences, Aristotle University Thessaloniki, Thessaloniki, Greece
| | - Dimitrios Giakoustidis
- 1st Department of Surgery, General Hospital Papageorgiou, School of Medicine, Faculty of Medical Sciences, Aristotle University Thessaloniki, Thessaloniki, Greece
| | - Vasileios N Papadopoulos
- 1st Department of Surgery, General Hospital Papageorgiou, School of Medicine, Faculty of Medical Sciences, Aristotle University Thessaloniki, Thessaloniki, Greece
| | - Christos Toumpanakis
- Centre for Gastroenterology, Neuroendocrine Tumour Unit, ENETS Centre of Excellence, Royal Free Hospital, London, United Kingdom
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Galgano SJ, Morani AC, Gopireddy DR, Sharbidre K, Bates DDB, Goenka AH, Arif-Tiwari H, Itani M, Iravani A, Javadi S, Faria S, Lall C, Bergsland E, Verma S, Francis IR, Halperin DM, Chatterjee D, Bhosale P, Yano M. Pancreatic neuroendocrine neoplasms: a 2022 update for radiologists. ABDOMINAL RADIOLOGY (NEW YORK) 2022; 47:3962-3970. [PMID: 35244755 DOI: 10.1007/s00261-022-03466-9] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 01/25/2022] [Revised: 02/17/2022] [Accepted: 02/18/2022] [Indexed: 01/18/2023]
Abstract
Pancreatic neuroendocrine neoplasms (PaNENs) are a unique group of pancreatic neoplasms with a wide range of clinical presentations and behaviors. Given their heterogeneous appearance and increasing detection on cross-sectional imaging, it is essential that radiologists understand the variable presentation and distinctions PaNENs display compared to other pancreatic neoplasms. Additionally, some of these neoplasms may be hormonally functional, and it is imperative that radiologists be aware of the common clinical presentations of hormonally active PaNENs. Knowledge of PaNEN pathology and treatments may influence which imaging modality is optimal for each patient. Each imaging modality used for PaNENs has distinct advantages and disadvantages, particularly in different treatment settings. Thus, the focus of this manuscript is to provide an update for the radiologist on PaNEN pathology, imaging, and treatments.
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Affiliation(s)
- Samuel J Galgano
- Department of Radiology, University of Alabama at Birmingham, Birmingham, AL, USA.
| | | | - Dheeraj R Gopireddy
- Department of Radiology, University of Florida-Jacksonville, Jacksonville, FL, USA
| | - Kedar Sharbidre
- Department of Radiology, University of Alabama at Birmingham, Birmingham, AL, USA
| | - David D B Bates
- Department of Radiology, Memorial Sloan Kettering Cancer Center, New York, NY, USA
| | - Ajit H Goenka
- Department of Radiology, Mayo Clinic, Rochester, MN, USA
| | - Hina Arif-Tiwari
- Department of Radiology, University of Arizona-Tuscon, Tuscon, AZ, USA
| | - Malak Itani
- Mallinckrodt Institute of Radiology, Washington University in St. Louis, St. Louis, MO, USA
| | - Amir Iravani
- Mallinckrodt Institute of Radiology, Washington University in St. Louis, St. Louis, MO, USA
| | - Sanaz Javadi
- Department of Radiology, M.D. Anderson Cancer Center, Houston, TX, USA
| | - Silvana Faria
- Department of Radiology, M.D. Anderson Cancer Center, Houston, TX, USA
| | - Chandana Lall
- Department of Radiology, University of Florida-Jacksonville, Jacksonville, FL, USA
| | - Emily Bergsland
- Department of Medicine, University of California San Francisco, San Francisco, CA, USA
| | - Sadhna Verma
- Department of Radiology, University of Cincinnati, Cincinnati, OH, USA
| | - Isaac R Francis
- Department of Radiology, Michigan Medicine, Ann Arbor, MI, USA
| | - Daniel M Halperin
- Department of Gastrointestinal Medical Oncology, M.D. Anderson Cancer Center, Houston, TX, USA
| | - Deyali Chatterjee
- Department of Pathology, M.D. Anderson Cancer Center, Houston, TX, USA
| | - Priya Bhosale
- Department of Radiology, M.D. Anderson Cancer Center, Houston, TX, USA
| | - Motoyo Yano
- Department of Radiology, Mayo Clinic Arizona, Scottsdale, AZ, USA
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Chiapponi C, Bruns CJ. [Modern molecular and imaging diagnostics in pancreatic neuroendocrine neoplasms]. CHIRURGIE (HEIDELBERG, GERMANY) 2022; 93:731-738. [PMID: 35913626 DOI: 10.1007/s00104-022-01645-4] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Accepted: 04/20/2022] [Indexed: 06/15/2023]
Abstract
BACKGROUND AND OBJECTIVE New molecular diagnostic and radiologic imaging techniques can be used to assess the extent, risk of recurrence, prognosis and response to treatment of pancreatic neuroendocrine neoplasms (pNENs). They therefore represent a decisive help in setting the indications for surgical treatment, especially in advanced stages. METHODS This article presents a narrative assessment of the options and evidence for modern molecular and radiologic imaging diagnostics of pNENs based on the current literature. RESULTS While circulating DNA, circulating tumor cells and microRNAs have not yet become established in everyday clinical practice, the current literature suggests a promising role for the so-called NETest. Recent studies demonstrated its possible importance for the surgical management of pNENs. Besides [68Ga]Ga-DOTA-SSA-PET and [18]FDG-PET, which remain the gold standards for imaging NENs, radiomics represent an exciting alternative to biopsies and will possibly play an increasingly important role in the future. DISCUSSION There are new promising alternatives to chromogranin A, which has been clinically widespread since the 1970s despite several drawbacks, to map the extent, risk of recurrence, prognosis and response to treatment of pancreatic pNENs. In terms of personalized medicine, modern molecular and radiological diagnostics should play an increasing role for indicating and planning surgical treatment and for follow-up in the future.
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Affiliation(s)
- Costanza Chiapponi
- Klinik für Allgemein‑, Viszeral‑, Tumor- und Transplantationschirurgie, Uniklinik Köln, Kerpenerstr. 62, 50937, Köln, Deutschland.
| | - Christiane J Bruns
- Klinik für Allgemein‑, Viszeral‑, Tumor- und Transplantationschirurgie, Uniklinik Köln, Kerpenerstr. 62, 50937, Köln, Deutschland
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Liu F, Li J, Fang X, Meng Y, Zhang H, Yu J, Feng X, Wang L, Jiang H, Lu J, Bian Y, Shao C. Differentiation of Solid Pseudopapillary Tumor and Non-Functional Neuroendocrine Tumors of the Pancreas Based on CT Delayed Imaging: A Propensity Score Analysis. Acad Radiol 2022; 29:350-357. [PMID: 33731286 DOI: 10.1016/j.acra.2021.02.020] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/01/2021] [Revised: 02/15/2021] [Accepted: 02/21/2021] [Indexed: 11/01/2022]
Abstract
PURPOSE To evaluate the diagnostic performance of the delayed-phase difference between tumor and pancreas for differentiating solid pseudopapillary tumors (SPTs) from non-functional neuroendocrine tumors (NF-NETs) of the pancreas. METHODS This retrospective review included 148 consecutive patients with SPT and 98 consecutive patients with NF-NET confirmed by pathology. Patients with SPT and NF-NET were matched via propensity score matching (PSM). All patients underwent multidetector computed tomography (MDCT). For each patient, the delayed-phase difference between the tumor and pancreas was measured, and the performance of this variable was assessed based on its discriminative ability and clinical utility. RESULTS After PSM, 27 patients with SPT and 27 patients with NF-NET were included in the matched analysis. There were no statistically significant differences in clinical and CT characteristics between the resulting two groups (p > 0.05). The delayed-phase difference values between the tumor and pancreas were significantly lower in patients with SPT (median: -0.45; range: -2.05 to 0.73) than in patients with NF-NET (median: 0.71; range: -1.39 to 2.38). The delayed-phase difference between tumor and pancreas had a high diagnostic accuracy (area under the curve=0.88). The best cutoff point based on maximizing the sum of the sensitivity and specificity was -0.23 (sensitivity = 88.89%; specificity = 88.89%; accuracy = 0.89). CONCLUSIONS The delayed-phase difference between tumor and pancreas can accurately and noninvasively differentiate SPT from NF-NET.
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Segaran N, Devine C, Wang M, Ganeshan D. Current update on imaging for pancreatic neuroendocrine neoplasms. World J Clin Oncol 2021; 12:897-911. [PMID: 34733612 PMCID: PMC8546658 DOI: 10.5306/wjco.v12.i10.897] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/31/2021] [Revised: 06/21/2021] [Accepted: 08/27/2021] [Indexed: 02/06/2023] Open
Abstract
Pancreatic neuroendocrine neoplasms (panNEN) are a heterogeneous group of tumors with differing pathological, genetic, and clinical features. Based on clinical findings, they may be categorized into functioning and nonfunctioning tumors. Adoption of the 2017 World Health Organization classification system, particularly its differentiation between grade 3, well-differentiated pancreatic neuroendocrine tumors (panNET) and grade 3, poorly-differentiated pancreatic neuroendocrine carcinomas (panNEC) has emphasized the role imaging plays in characterizing these lesions. Endoscopic ultrasound can help obtain biopsy specimen and assess tumor margins and local spread. Enhancement patterns on computed tomography (CT) and magnetic resonance imaging (MRI) may be used to classify panNEN. Contrast enhanced MRI and diffusion-weighted imaging have been reported to be useful for characterization of panNEN and quantifying metastatic burden. Current and emerging radiotracers have broadened the utility of functional imaging in evaluating panNEN. Fluorine-18 fluorodeoxyglucose positron emission tomography (PET)/CT and somatostatin receptor imaging such as Gallium-68 1,4,7,10-tetraazacyclododecane-1,4,7,10-tetraacetic acid–octreotate PET/CT may be useful for improved identification of panNEN in comparison to anatomic modalities. These new techniques can also play a direct role in optimizing the selection of treatment for individuals and predicting tumor response based on somatostatin receptor expression. In addition, emerging methods of radiomics such as texture analysis may be a potential tool for staging and outcome prediction in panNEN, however further investigation is required before clinical implementation.
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Affiliation(s)
- Nicole Segaran
- Department of Radiology, Mayo Clinic Arizona, Phoenix, AZ 85259, United States
| | - Catherine Devine
- Department of Diagnostic Radiology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, United States
| | - Mindy Wang
- Department of Diagnostic Radiology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, United States
| | - Dhakshinamoorthy Ganeshan
- Department of Diagnostic Radiology, Abdominal Imaging, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, United States
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Półtorak-Szymczak G, Budlewski T, Furmanek MI, Wierzba W, Sklinda K, Walecki J, Mruk B. Radiological Imaging of Gastro-Entero-Pancreatic Neuroendocrine Tumors. The Review of Current Literature Emphasizing the Diagnostic Value of Chosen Imaging Methods. Front Oncol 2021; 11:670233. [PMID: 34211845 PMCID: PMC8239281 DOI: 10.3389/fonc.2021.670233] [Citation(s) in RCA: 9] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/20/2021] [Accepted: 04/14/2021] [Indexed: 02/03/2023] Open
Abstract
Despite development of radiologic imaging, detection and follow-up of neuroendocrine neoplasms (NENs) still pose a diagnostic challenge, due to the heterogeneity of NEN, their relatively long-term growth, and small size of primary tumor. A set of information obtained by using different radiological imaging tools simplifies a choice of the most appropriate treatment method. Moreover, radiological imaging plays an important role in the assessment of metastatic lesions, especially in the liver, as well as, tumor response to treatment. This article reviews the current, broadly in use imaging modalities which are applied to the diagnosis of GEP-NETs, (the most common type of NENs) and put emphasis on the strengths and limitations of each modality.
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Affiliation(s)
- Gabriela Półtorak-Szymczak
- Department of Radiology, Centre of Postgraduate Medical Education, Warsaw, Poland.,Central Clinical Hospital of the Ministry of the Interior and Administration in Warsaw, Warsaw, Poland
| | - Tadeusz Budlewski
- Central Clinical Hospital of the Ministry of the Interior and Administration in Warsaw, Warsaw, Poland.,Department of Nuclear Medicine, Central Clinical Hospital of the Ministry of the Interior and Administration in Warsaw, Warsaw, Poland
| | - Mariusz Ireneusz Furmanek
- Department of Radiology, Centre of Postgraduate Medical Education, Warsaw, Poland.,Central Clinical Hospital of the Ministry of the Interior and Administration in Warsaw, Warsaw, Poland
| | - Waldemar Wierzba
- Central Clinical Hospital of the Ministry of the Interior and Administration in Warsaw, Warsaw, Poland.,University of Humanities and Economics, Lodz, Poland
| | - Katarzyna Sklinda
- Department of Radiology, Centre of Postgraduate Medical Education, Warsaw, Poland.,Central Clinical Hospital of the Ministry of the Interior and Administration in Warsaw, Warsaw, Poland
| | - Jerzy Walecki
- Department of Radiology, Centre of Postgraduate Medical Education, Warsaw, Poland.,Central Clinical Hospital of the Ministry of the Interior and Administration in Warsaw, Warsaw, Poland
| | - Bartosz Mruk
- Department of Radiology, Centre of Postgraduate Medical Education, Warsaw, Poland.,Central Clinical Hospital of the Ministry of the Interior and Administration in Warsaw, Warsaw, Poland
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10
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Song T, Zhang QW, Duan SF, Bian Y, Hao Q, Xing PY, Wang TG, Chen LG, Ma C, Lu JP. MRI-based radiomics approach for differentiation of hypovascular non-functional pancreatic neuroendocrine tumors and solid pseudopapillary neoplasms of the pancreas. BMC Med Imaging 2021; 21:36. [PMID: 33622277 PMCID: PMC7901077 DOI: 10.1186/s12880-021-00563-x] [Citation(s) in RCA: 16] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/30/2020] [Accepted: 02/02/2021] [Indexed: 11/10/2022] Open
Abstract
BACKGROUND This study aims to investigate the value of radiomics parameters derived from contrast enhanced (CE) MRI in differentiation of hypovascular non-functional pancreatic neuroendocrine tumors (hypo-NF-pNETs) and solid pseudopapillary neoplasms of the pancreas (SPNs). METHODS Fifty-seven SPN patients and twenty-two hypo-NF-pNET patients were enrolled. Radiomics features were extracted from T1WI, arterial, portal and delayed phase of MR images. The enrolled patients were divided into training cohort and validation cohort with the 7:3 ratio. We built four radiomics signatures for the four phases respectively and ROC analysis were used to select the best phase to discriminate SPNs from hypo-NF-pNETs. The chosen radiomics signature and clinical independent risk factors were integrated to construct a clinic-radiomics nomogram. RESULTS SPNs occurred in younger age groups than hypo-NF-pNETs (P < 0.0001) and showed a clear preponderance in females (P = 0.0185). Age was a significant independent factor for the differentiation of SPNs and hypo-NF-pNETs revealed by logistic regression analysis. With AUC values above 0.900 in both training and validation cohort (0.978 [95% CI, 0.942-1.000] in the training set, 0.907 [95% CI, 0.765-1.000] in the validation set), the radiomics signature of the arterial phase was picked to build a clinic-radiomics nomogram. The nomogram, composed by age and radiomics signature of the arterial phase, showed sufficient performance for discriminating SPNs and hypo-NF-pNETs with AUC values of 0.965 (95% CI, 0.923-1.000) and 0.920 (95% CI, 0.796-1.000) in the training and validation cohorts, respectively. Delong Test did not demonstrate statistical significance between the AUC of the clinic-radiomics nomogram and radiomics signature of arterial phase. CONCLUSION CE-MRI-based radiomics approach demonstrated great potential in the differentiation of hypo-NF-pNETs and SPNs.
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Affiliation(s)
- Tao Song
- Department of Radiology, Changhai Hospital, The Navy Medical University (Second Military Medical University), 168 Changhai Road, Shanghai, 200433, China
| | - Qian-Wen Zhang
- Department of Radiology, Changhai Hospital, The Navy Medical University (Second Military Medical University), 168 Changhai Road, Shanghai, 200433, China
| | - Shao-Feng Duan
- GE Healthcare China, Pudong New Town, No.1 Huatuo Road, Shanghai, 210000, China
| | - Yun Bian
- Department of Radiology, Changhai Hospital, The Navy Medical University (Second Military Medical University), 168 Changhai Road, Shanghai, 200433, China
| | - Qiang Hao
- Department of Radiology, Changhai Hospital, The Navy Medical University (Second Military Medical University), 168 Changhai Road, Shanghai, 200433, China
| | - Peng-Yi Xing
- Department of Radiology, Changhai Hospital, The Navy Medical University (Second Military Medical University), 168 Changhai Road, Shanghai, 200433, China
| | - Tie-Gong Wang
- Department of Radiology, Changhai Hospital, The Navy Medical University (Second Military Medical University), 168 Changhai Road, Shanghai, 200433, China
| | - Lu-Guang Chen
- Department of Radiology, Changhai Hospital, The Navy Medical University (Second Military Medical University), 168 Changhai Road, Shanghai, 200433, China
| | - Chao Ma
- Department of Radiology, Changhai Hospital, The Navy Medical University (Second Military Medical University), 168 Changhai Road, Shanghai, 200433, China
| | - Jian-Ping Lu
- Department of Radiology, Changhai Hospital, The Navy Medical University (Second Military Medical University), 168 Changhai Road, Shanghai, 200433, China.
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11
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Verde F, Galatola R, Romeo V, Perillo T, Liuzzi R, Camera L, Klain M, Modica R, Faggiano A, Napolitano V, Colao A, Brunetti A, Maurea S. Pancreatic Neuroendocrine Tumors in Patients with Multiple Endocrine Neoplasia Type 1: Diagnostic Value of Different MRI Sequences. Neuroendocrinology 2021; 111:696-704. [PMID: 32580192 DOI: 10.1159/000509647] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/22/2020] [Accepted: 06/23/2020] [Indexed: 11/19/2022]
Abstract
BACKGROUND MRI is a useful imaging modality to assess the presence of pancreatic neuroendocrine tumors (PNETs), allowing repeat monitoring examinations in multiple endocrine neoplasia type 1 (MEN-1) patients. OBJECTIVES We aimed to compare the diagnostic accuracy of conventional MRI sequences to identify which sequence better depicts the presence of PNETs in MEN-1 patients. METHOD We performed a retrospective analysis of consecutive MEN-1 patients who underwent a conventional MRI protocol to monitor previously proven PNETs. MRI sequences T1-w chemical shift (CS), T2-w HASTE, fat-suppressed (FS) T2-w HASTE, diffusion-weighted imaging (DWI), and pre- and post-contrast FS T1-w sequences were independently analyzed by 2 experienced radiologists using a 3-grade score (no lesion, uncertain lesion, and certain lesion); lesion size and signal intensity were recorded. A Friedman ANOVA and a Wilcoxon pairwise test for the post hoc analysis were used. The sensitivity of each sequence was measured, and the results were analyzed with the χ2 test. RESULTS We included 21 patients with a total of 45 PNETs proven by histology, endoscopic ultrasonography-guided fine-needle aspiration, CT, and nuclear medicine studies. A statistically significant (p < 0.01) difference was observed in the detection performance of each MRI sequence, particularly between DWI (91%) and T2-w FS (85%) sequences in comparison to the others (T1-w CS, T2-w, and pre- and post-contrast FS T1-w, ≤56% for all); no significant (p = 0.5) difference was found between the detection performance of DWI and T2-w FS sequences. No correlation was observed between the qualitative score of each sequence and lesion tumor size. CONCLUSIONS DWI and T2-w FS sequences proved to be the most accurate in the detection of PNETs, thus suggesting a role for an abbreviated MRI protocol without contrast medium administration for monitoring MEN-1 patients.
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Affiliation(s)
- Francesco Verde
- Department of Advanced Biomedical Sciences, University of Naples "Federico II,", Naples, Italy
| | - Roberta Galatola
- Department of Advanced Biomedical Sciences, University of Naples "Federico II,", Naples, Italy
| | - Valeria Romeo
- Department of Advanced Biomedical Sciences, University of Naples "Federico II,", Naples, Italy,
| | - Teresa Perillo
- Department of Advanced Biomedical Sciences, University of Naples "Federico II,", Naples, Italy
| | - Raffaele Liuzzi
- Institute of Biostructures and Bioimaging of the National Council of Research (CNR), Naples, Italy
| | - Luigi Camera
- Department of Advanced Biomedical Sciences, University of Naples "Federico II,", Naples, Italy
| | - Michele Klain
- Department of Advanced Biomedical Sciences, University of Naples "Federico II,", Naples, Italy
| | - Roberta Modica
- Department of Clinical Medicine and Surgery, University of Naples "Federico II,", Naples, Italy
| | - Antongiulio Faggiano
- Department of Clinical Medicine and Surgery, University of Naples "Federico II,", Naples, Italy
| | - Vincenzo Napolitano
- Department of Translational Medical Sciences, University of Campania "L. Vanvitelli,", Naples, Italy
| | - Annamaria Colao
- Department of Clinical Medicine and Surgery, University of Naples "Federico II,", Naples, Italy
| | - Arturo Brunetti
- Department of Advanced Biomedical Sciences, University of Naples "Federico II,", Naples, Italy
| | - Simone Maurea
- Department of Advanced Biomedical Sciences, University of Naples "Federico II,", Naples, Italy
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12
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Shi YJ, Zhu HT, Liu YL, Wei YY, Qin XB, Zhang XY, Li XT, Sun YS. Radiomics Analysis Based on Diffusion Kurtosis Imaging and T2 Weighted Imaging for Differentiation of Pancreatic Neuroendocrine Tumors From Solid Pseudopapillary Tumors. Front Oncol 2020; 10:1624. [PMID: 32974201 PMCID: PMC7473210 DOI: 10.3389/fonc.2020.01624] [Citation(s) in RCA: 19] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/09/2020] [Accepted: 07/27/2020] [Indexed: 12/31/2022] Open
Abstract
Objective To develop and validate a radiomics model of diffusion kurtosis imaging (DKI) and T2 weighted imaging for discriminating pancreatic neuroendocrine tumors (PNETs) from solid pseudopapillary tumors (SPTs). Materials and Methods Sixty-six patients with histopathological confirmed PNETs (n = 31) and SPTs (n = 35) were enrolled in this study. ROIs of tumors were manually drawn on each slice at T2WI and DWI (b = 1,500 s/mm2) from 3T MRI. Intraclass correlation coefficients were used to evaluate the interobserver agreement. Mean diffusivity (MD) and mean kurtosis (MK) were derived from DKI. The least absolute shrinkage and selection operator regression were used for feature selection. Results MD and MK had a moderate diagnostic performancewith the area under curve (AUC) of 0.71 and 0.65, respectively. A radiomics model, which incorporated sex and age of patients and radiomics signature of the tumor, showed excellent discrimination performance with AUC of 0.97 and 0.86 in the primary and validation cohort. Moreover, the new model had better diagnostic performance than that of MD (P = 0.023) and MK (P = 0.004), and showed excellent differentiation with a sensitivity of 95.00% and specificity of 91.67% in primary cohort, and the sensitivity of 90.91% and specificity of 81.82% in the validation cohort. The accuracy of radiomics analysis, radiologist 1, and radiologist 2 for diagnosing SPTs and PNETs were 92.42, 77.27, and 78.79%, respectively. The accuracy of radiomics analysis was significantly higher than that of subjective diagnosis (P < 0.05). Conclusions Radiomics model could improve the diagnostic accuracy of SPTs and PNETs and contribute to determining an appropriate treatment strategy for pancreatic tumors.
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Affiliation(s)
- Yan-Jie Shi
- Department of Radiology, Key Laboratory of Carcinogenesis and Translational Research, Peking University Cancer Hospital, Beijing, China
| | - Hai-Tao Zhu
- Department of Radiology, Key Laboratory of Carcinogenesis and Translational Research, Peking University Cancer Hospital, Beijing, China
| | - Yu-Liang Liu
- Department of Radiology, Key Laboratory of Carcinogenesis and Translational Research, Peking University Cancer Hospital, Beijing, China
| | - Yi-Yuan Wei
- Department of Radiology, Key Laboratory of Carcinogenesis and Translational Research, Peking University Cancer Hospital, Beijing, China
| | - Xiu-Bo Qin
- Department of Radiology, Key Laboratory of Carcinogenesis and Translational Research, Peking University Cancer Hospital, Beijing, China
| | - Xiao-Yan Zhang
- Department of Radiology, Key Laboratory of Carcinogenesis and Translational Research, Peking University Cancer Hospital, Beijing, China
| | - Xiao-Ting Li
- Department of Radiology, Key Laboratory of Carcinogenesis and Translational Research, Peking University Cancer Hospital, Beijing, China
| | - Ying-Shi Sun
- Department of Radiology, Key Laboratory of Carcinogenesis and Translational Research, Peking University Cancer Hospital, Beijing, China
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13
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Khanna L, Prasad SR, Sunnapwar A, Kondapaneni S, Dasyam A, Tammisetti VS, Salman U, Nazarullah A, Katabathina VS. Pancreatic Neuroendocrine Neoplasms: 2020 Update on Pathologic and Imaging Findings and Classification. Radiographics 2020; 40:1240-1262. [PMID: 32795239 DOI: 10.1148/rg.2020200025] [Citation(s) in RCA: 67] [Impact Index Per Article: 13.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
Pancreatic neuroendocrine neoplasms (panNENs) are heterogeneous neoplasms with neuroendocrine differentiation that show characteristic clinical, histomorphologic, and prognostic features; genetic alterations; and biologic behavior. Up to 10% of panNENs develop in patients with syndromes that predispose them to cancer, such as multiple endocrine neoplasia type 1, von Hippel-Lindau disease, tuberous sclerosis complex, neurofibromatosis type 1, and glucagon cell adenomatosis. PanNENs are classified as either functioning tumors, which manifest early because of clinical symptoms related to increased hormone production, or nonfunctioning tumors, which often manifest late because of mass effect. PanNENs are histopathologically classified as well-differentiated pancreatic neuroendocrine tumors (panNETs) or poorly differentiated pancreatic neuroendocrine carcinomas (panNECs) according to the 2010 World Health Organization (WHO) classification system. Recent advances in cytogenetics and molecular biology have shown substantial heterogeneity in panNECs, and a new tumor subtype, well-differentiated, high-grade panNET, has been introduced. High-grade panNETs and panNECs are two distinct entities with different pathogenesis, clinical features, imaging findings, treatment options, and prognoses. The 2017 WHO classification system and the eighth edition of the American Joint Committee on Cancer staging system include substantial changes. Multidetector CT, MRI, and endoscopic US help in anatomic localization of the primary tumor, local-regional spread, and metastases. Somatostatin receptor scintigraphy and fluorine 18-fluorodeoxyglucose PET/CT are helpful for functional and metabolic assessment. Knowledge of recent updates in the pathogenesis, classification, and staging of panNENs and familiarity with their imaging findings allow optimal patient treatment. ©RSNA, 2020.
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Affiliation(s)
- Lokesh Khanna
- From the Departments of Radiology (L.K., A.S., U.S., V.S.K.) and Pathology (V.S.T.), University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, San Antonio, TX 78229; Department of Radiology, University of Texas M. D. Anderson Cancer Center, Houston, Tex (S.R.P.); Department of Molecular Biosciences, University of Texas at Austin, Austin, Tex (S.K.); Department of Radiology, University of Pittsburgh Medical Center, Pittsburgh, Pa (A.D.); and Department of Radiology, University of Texas Health Science Center at Houston, Houston, Tex (A.N.)
| | - Srinivasa R Prasad
- From the Departments of Radiology (L.K., A.S., U.S., V.S.K.) and Pathology (V.S.T.), University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, San Antonio, TX 78229; Department of Radiology, University of Texas M. D. Anderson Cancer Center, Houston, Tex (S.R.P.); Department of Molecular Biosciences, University of Texas at Austin, Austin, Tex (S.K.); Department of Radiology, University of Pittsburgh Medical Center, Pittsburgh, Pa (A.D.); and Department of Radiology, University of Texas Health Science Center at Houston, Houston, Tex (A.N.)
| | - Abhijit Sunnapwar
- From the Departments of Radiology (L.K., A.S., U.S., V.S.K.) and Pathology (V.S.T.), University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, San Antonio, TX 78229; Department of Radiology, University of Texas M. D. Anderson Cancer Center, Houston, Tex (S.R.P.); Department of Molecular Biosciences, University of Texas at Austin, Austin, Tex (S.K.); Department of Radiology, University of Pittsburgh Medical Center, Pittsburgh, Pa (A.D.); and Department of Radiology, University of Texas Health Science Center at Houston, Houston, Tex (A.N.)
| | - Sainath Kondapaneni
- From the Departments of Radiology (L.K., A.S., U.S., V.S.K.) and Pathology (V.S.T.), University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, San Antonio, TX 78229; Department of Radiology, University of Texas M. D. Anderson Cancer Center, Houston, Tex (S.R.P.); Department of Molecular Biosciences, University of Texas at Austin, Austin, Tex (S.K.); Department of Radiology, University of Pittsburgh Medical Center, Pittsburgh, Pa (A.D.); and Department of Radiology, University of Texas Health Science Center at Houston, Houston, Tex (A.N.)
| | - Anil Dasyam
- From the Departments of Radiology (L.K., A.S., U.S., V.S.K.) and Pathology (V.S.T.), University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, San Antonio, TX 78229; Department of Radiology, University of Texas M. D. Anderson Cancer Center, Houston, Tex (S.R.P.); Department of Molecular Biosciences, University of Texas at Austin, Austin, Tex (S.K.); Department of Radiology, University of Pittsburgh Medical Center, Pittsburgh, Pa (A.D.); and Department of Radiology, University of Texas Health Science Center at Houston, Houston, Tex (A.N.)
| | - Varaha S Tammisetti
- From the Departments of Radiology (L.K., A.S., U.S., V.S.K.) and Pathology (V.S.T.), University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, San Antonio, TX 78229; Department of Radiology, University of Texas M. D. Anderson Cancer Center, Houston, Tex (S.R.P.); Department of Molecular Biosciences, University of Texas at Austin, Austin, Tex (S.K.); Department of Radiology, University of Pittsburgh Medical Center, Pittsburgh, Pa (A.D.); and Department of Radiology, University of Texas Health Science Center at Houston, Houston, Tex (A.N.)
| | - Umber Salman
- From the Departments of Radiology (L.K., A.S., U.S., V.S.K.) and Pathology (V.S.T.), University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, San Antonio, TX 78229; Department of Radiology, University of Texas M. D. Anderson Cancer Center, Houston, Tex (S.R.P.); Department of Molecular Biosciences, University of Texas at Austin, Austin, Tex (S.K.); Department of Radiology, University of Pittsburgh Medical Center, Pittsburgh, Pa (A.D.); and Department of Radiology, University of Texas Health Science Center at Houston, Houston, Tex (A.N.)
| | - Alia Nazarullah
- From the Departments of Radiology (L.K., A.S., U.S., V.S.K.) and Pathology (V.S.T.), University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, San Antonio, TX 78229; Department of Radiology, University of Texas M. D. Anderson Cancer Center, Houston, Tex (S.R.P.); Department of Molecular Biosciences, University of Texas at Austin, Austin, Tex (S.K.); Department of Radiology, University of Pittsburgh Medical Center, Pittsburgh, Pa (A.D.); and Department of Radiology, University of Texas Health Science Center at Houston, Houston, Tex (A.N.)
| | - Venkata S Katabathina
- From the Departments of Radiology (L.K., A.S., U.S., V.S.K.) and Pathology (V.S.T.), University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, San Antonio, TX 78229; Department of Radiology, University of Texas M. D. Anderson Cancer Center, Houston, Tex (S.R.P.); Department of Molecular Biosciences, University of Texas at Austin, Austin, Tex (S.K.); Department of Radiology, University of Pittsburgh Medical Center, Pittsburgh, Pa (A.D.); and Department of Radiology, University of Texas Health Science Center at Houston, Houston, Tex (A.N.)
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14
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Rozenblum L, Mokrane FZ, Yeh R, Sinigaglia M, Besson F, Seban RD, Chougnet CN, Revel-Mouroz P, Zhao B, Otal P, Schwartz LH, Dercle L. The role of multimodal imaging in guiding resectability and cytoreduction in pancreatic neuroendocrine tumors: focus on PET and MRI. Abdom Radiol (NY) 2019; 44:2474-2493. [PMID: 30980115 DOI: 10.1007/s00261-019-01994-5] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/17/2022]
Abstract
Pancreatic neuroendocrine tumors (pNETs) are rare neoplasms that secrete peptides and neuro-amines. pNETs can be sporadic or hereditary, syndromic or non-syndromic with different clinical presentations and prognoses. The role of medical imaging includes locating the tumor, assessing its extent, and evaluating the feasibility of curative surgery or cytoreduction. Pancreatic NETs have very distinctive phenotypes on CT, MRI, and PET. PET have been demonstrated to be very sensitive to detect either well-differentiated pNETs using 68Gallium somatostatin receptor (SSTR) radiotracers, or more aggressive undifferentiated pNETS using 18F-FDG. A comprehensive interpretation of multimodal imaging guides resectability and cytoreduction in pNETs. The imaging phenotype provides information on the differentiation and proliferation of pNETs, as well as the spatial and temporal heterogeneity of tumors with prognostic and therapeutic implications. This review provides a structured approach for standardized reading and reporting of medical imaging studies with a focus on PET and MR techniques. It explains which imaging approach should be used for different subtypes of pNET and what a radiologist should be looking for and reporting when interpreting these studies.
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Affiliation(s)
- Laura Rozenblum
- Sorbonne Université, Service de Médecine Nucléaire, AP-HP, Hôpital La Pitié-Salpêtrière, 75013, Paris, France
| | - Fatima-Zohra Mokrane
- Radiology Department, Toulouse University Hospital, 1 Avenue du Professeur Jean Poulhes, 31059, Toulouse, France
- Department of Radiology, New York Presbyterian Hospital, Columbia University, New York, NY, USA
| | - Randy Yeh
- Memorial Sloan Kettering Cancer Center, Molecular Imaging and Therapy Service, New York, NY, USA
| | - Mathieu Sinigaglia
- Department of Imaging and Nuclear Medicine, Institut Claudius Regaud - Institut Universitaire du Cancer de Toulouse - Oncopole, Toulouse, France
| | - Florent Besson
- Paris Sud University, Kremlin Bicêtre Hospital, Paris, France
| | - Romain-David Seban
- Department of Nuclear Medicine, Institut Curie-René Huguenin, Saint-Cloud, France
| | - Cecile N Chougnet
- Department of Endocrine Oncology, Hôpital Saint Louis, Paris, France
| | - Paul Revel-Mouroz
- Radiology Department, Toulouse University Hospital, 1 Avenue du Professeur Jean Poulhes, 31059, Toulouse, France
| | - Binsheng Zhao
- Department of Radiology, New York Presbyterian Hospital, Columbia University, New York, NY, USA
| | - Philippe Otal
- Radiology Department, Toulouse University Hospital, 1 Avenue du Professeur Jean Poulhes, 31059, Toulouse, France
| | - Lawrence H Schwartz
- Department of Radiology, New York Presbyterian Hospital, Columbia University, New York, NY, USA
| | - Laurent Dercle
- Department of Radiology, New York Presbyterian Hospital, Columbia University, New York, NY, USA.
- UMR 1015, Gustave Roussy Institute, Université Paris-Saclay, Villejuif, 94805, France.
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