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Neuroendocrine Tumors: Clinical Challenges

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A special issue of Journal of Clinical Medicine (ISSN 2077-0383). This special issue belongs to the section "Oncology".

Deadline for manuscript submissions: closed (30 September 2020) | Viewed by 52756

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Prof. Dr. Francesco Panzuto

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Digestive and Lilver Disease Unit, Sant’Andrea University Hospital, ENETS Center of Excellence, Rome, Italy
Interests: neuroendocrine tumors; digestive oncology; pancreatic diseases; gut hormones
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Although increasing in incidence and prevalence, neuroendocrine tumors (NETs) remain rare and complex diseases with heterogeneous biology and clinical behavior, requiring multidisciplinary team management. Knowledge of these diseases has significantly increased in recent decades, thanks to improvements in the diagnostic accuracy of cross-sectional imaging procedures; the evolution of nuclear medicine tecniques; and the development of promising therapeutic approaches that have been shown to positively impact disease clinical outcome and patients’ quality of life. The present Special Issue aims at investigating the “gray areas” that still remain in the clinical management of NETs, focusing on the unmet need that physicians dealing with these diseases may face during diagnostic work-up and therapeutic strategy setting up.

Dr. Francesco Panzuto
Guest Editor

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Keywords

Neuroendocrine tumors
Carcinoid syndrome
Pancreatic endocrine tumors
Multidisciplinary team
Diagnosis
Prognostic factors
Therapeutic approach
Somatostatin analogs
Peptide receptor radionuclide therapy
Targeted therapies

Published Papers (13 papers)

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Editorial

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3 pages, 178 KiB

Open AccessEditorial

Clinical Challenges in the Management of Neuroendocrine Tumors

by Francesco Panzuto

J. Clin. Med. 2021, 10(2), 257; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm10020257 - 12 Jan 2021

Cited by 1 | Viewed by 1322

Abstract

Neuroendocrine tumors (NET) are rare and heterogeneous diseases, whose prognosis is affected by several factors including the primary tumor site, grading, somatostatin receptor expression, and disease staging [...] Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

Research

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10 pages, 1119 KiB

Open AccessArticle

Professional Assessment of the Impact of COVID-19 on Handling NET Patients

by Sebastian Krug, Jakob Garbe, Senta König, Hanna Ungewiss, Patrick Michl, Anja Rinke and Jörg Schrader

J. Clin. Med. 2020, 9(11), 3633; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm9113633 - 11 Nov 2020

Cited by 8 | Viewed by 2132

Abstract

The treatment and monitoring of patients with neuroendocrine tumors (NET) has been a major challenge during the COVID-19 pandemic. In a survey, we investigated the influence of COVID-19 on the care of NET patients in the German speaking countries Germany, Austria and Switzerland. The multidisciplinarity of all treating physicians in the outpatient and inpatient sector was reflected in our survey. Furthermore, we were able to present findings pertaining to the university and non-university medical care. Overall, only a minority of appointments were cancelled, mostly as a result of medical prioritization and less for fear of infection by patients. In the university sector, longer delays for diagnostic measures were observed in comparison to non-university care. During the COVID-19 crisis, NET patients rarely changed their current therapy, but the pandemic impacted the assessment of the different treatment modalities at risk of developing severe COVID-19 disease. This survey provides the first real-world data on the treatment of NET patients from the physicians’ perspective during the COVID-19 crisis. Despite delays in diagnostic procedures and outpatient appointments, only a minority of physicians foresee a major impact of COVID-19 on NET patient care. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

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9 pages, 1988 KiB

Open AccessArticle

Analysis of miR-29 Serum Levels in Patients with Neuroendocrine Tumors—Results from an Exploratory Study

by Burcin Özdirik, Anna K. Stueven, Raphael Mohr, Lukas Geisler, Alexander Wree, Jana Knorr, Münevver Demir, Mihael Vucur, Sven H. Loosen, Fabian Benz, Markus Reiss, Bertram Wiedenmann, Frank Tacke, Henning Jann, Teresa Hellberg and Christoph Roderburg

J. Clin. Med. 2020, 9(9), 2881; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm9092881 - 06 Sep 2020

Cited by 8 | Viewed by 1805

Abstract

Background and aims: Due to its involvement in tumor biology as well as tumor-associated stroma cell responses, recent data suggested a potential role of miR-29 as a biomarker for different malignancies. However, its role in neuroendocrine tumors (NETs) is only poorly understood. Methods: We measured circulating levels of miR-29b in 45 patients with NET and compared them to 19 healthy controls. Results were correlated with clinical records. Results: In our cohort of NET patients treated between 2010 and 2019 at our department, miR-29b serum levels were significantly downregulated when compared to healthy control samples. Further, a significant correlation between chromogranin A (CgA) and relative miR-29b levels was noted. However, serum levels of miR-29b were independent of tumor-related factors such as proliferation activity according to Ki-67 index, tumor grading, the TMN stage of malignant tumors, somatostatin receptor expression or clinical features such as functional or non-functional disease and presence of tumor relapse. Finally, in contrast to previous results from other malignancies, miR-29b serum levels were not a significant predictor of overall survival in NET patients. Conclusion: Our data suggest a role for miR-29b serum levels as a previously unrecognized biomarker for diagnosis of NET. However, miR-29 does not allow for predicting tumor stage or patients’ outcome. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

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13 pages, 600 KiB

Open AccessArticle

Outcomes of Patients with Clinical Stage I-IIIA Large-Cell Neuroendocrine Lung Cancer Treated with Resection

by Anna Lowczak, Agnieszka Kolasinska-Cwikla, Jarosław B Ćwikła, Karolina Osowiecka, Jakub Palucki, Robert Rzepko, Lidka Glinka and Anna Doboszyńska

J. Clin. Med. 2020, 9(5), 1370; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm9051370 - 07 May 2020

Cited by 7 | Viewed by 2313

Abstract

Large-cell neuroendocrine carcinoma (LCNEC) is a rare malignancy with poor prognosis. The rationale of the study was to determine the survival of LCNEC patients in I–IIIA clinical stages who underwent resection. A total of 53 LCNEC (89%) and combined LCNEC (11%) patients in stages I–IIIA who underwent surgery with radical intent between 2002–2018 were included in the current study. Overall survival (OS) and time to recurrence (TTR) were estimated. Uni- and multivariable analyses were conducted using Cox-regression model. Patients were treated with surgery alone (51%), surgery with radiochemotherapy (4%), with radiotherapy (2%), with adjuvant chemotherapy (41%), or with neoadjuvant chemotherapy (2%). The median (95% Confidence Interval (CI)) OS and TTR was 52 months (20.1–102.1 months) and 20 months (7.0–75.6 months), respectively. Patients treated in clinical stage I showed better OS than patients in stages II–IIIA (p = 0.008). Patients with R0 resection margin (negative margin, no tumor at the margin) and without lymph node metastasis had significantly better TTR. In the multivariate analysis, age was an independent factor influencing OS. Recurrence within 1 year was noted in more than half cases of LCNEC. R0 resection margin and N0 status (no lymph node metastasis) were factors improving TTR. Age >64 years was observed as a main independent factor influencing OS. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

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11 pages, 1398 KiB

Open AccessArticle

Perioperative Chemotherapy in Poorly Differentiated Neuroendocrine Neoplasia of the Bladder: A Multicenter Analysis

by Giuseppe Lamberti, Maria Pia Brizzi, Sara Pusceddu, Fabio Gelsomino, Giovanni Di Meglio, Francesco Massari, Giuseppe Badalamenti, Ferdinando Riccardi, Toni Ibrahim, Chiara Ciccarese, Sebastiano Buti, Carlo Carnaghi, Natalie Prinzi, Francesco Panzuto and Davide Campana

J. Clin. Med. 2020, 9(5), 1351; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm9051351 - 05 May 2020

Cited by 5 | Viewed by 2167

Abstract

There is scant evidence about optimal management of poorly differentiated neuroendocrine carcinoma of the bladder (BNEC). We performed a multicenter retrospective study on BNEC patients from 13 Italian neuroendocrine-dedicated centers to analyze strategies associated with better outcomes. Mixed adeno-neuroendocrine carcinomas (MANEC) were included. We analyzed overall survival (OS) in the overall cohort, relapse-free survival (RFS) in radically operated patients and progression-free survival (PFS) in patients who received chemotherapy for metastatic disease. Fifty-one BNEC patients were included (male: 46, median age: 70 years). Overall, median OS was 16.0 months, radical tumor resection was performed in 37 patients (72.5%) and 11 of these (29.7%) also received peri-operative platinum-etoposide chemotherapy. Median OS was longer in patients with better performance status (PS) and in those with stage I–III disease at diagnosis compared to stage IV. Among patients who underwent radical tumor resection (N = 37), RFS was longer in patients with better PS and showed a trend towards a longer RFS in those treated with peri-operative chemotherapy than with surgery alone (11 vs. 6 months; p = 0.078). Among 28 patients receiving chemotherapy for metastatic disease, PFS was 5.0 months and there was a trend towards improved PFS in patients receiving carboplatin-etoposide chemotherapy compared to other regimens. A multivariate model unmasked a significant association between carboplatin-etoposide chemotherapy and risk for disease progression or death (HR: 0.39 (95%CI: 0.16–0.96) p = 0.040). Performance status might be associated with improved RFS in radically operated patients, while type of chemotherapy might affect PFS in patients receiving chemotherapy for metastatic BNEC. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

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Review

Jump to: Editorial, Research

18 pages, 353 KiB

Open AccessReview

Large Cell Neuroendocrine Carcinoma of the Lung: Current Understanding and Challenges

by Elisa Andrini, Paola Valeria Marchese, Dario De Biase, Cristina Mosconi, Giambattista Siepe, Francesco Panzuto, Andrea Ardizzoni, Davide Campana and Giuseppe Lamberti

J. Clin. Med. 2022, 11(5), 1461; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm11051461 - 07 Mar 2022

Cited by 20 | Viewed by 6282

Abstract

Large cell neuroendocrine carcinoma of the lung (LCNEC) is a rare and highly aggressive type of lung cancer, with a complex biology that shares similarities with both small-cell lung cancer (SCLC) and non-small-cell lung cancer (NSCLC). The prognosis of LCNEC is poor, with a median overall survival of 8–12 months. The diagnosis of LCNEC requires the identification of neuroendocrine morphology and the expression of at least one of the neuroendocrine markers (chromogranin A, synaptophysin or CD56). In the last few years, the introduction of next-generation sequencing allowed the identification of molecular subtypes of LCNEC, with prognostic and potential therapeutic implications: one subtype is similar to SCLC (SCLC-like), while the other is similar to NSCLC (NSCLC-like). Because of LCNEC rarity, most evidence comes from small retrospective studies and treatment strategies that are extrapolated from those adopted in patients with SCLC and NSCLC. Nevertheless, limited but promising data about targeted therapies and immune checkpoint inhibitors in patients with LCNEC are emerging. LCNEC clinical management is still controversial and standardized treatment strategies are currently lacking. The aim of this manuscript is to review clinical and molecular data about LCNEC to better understand the optimal management and the potential prognostic and therapeutic implications of molecular subtypes. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

13 pages, 604 KiB

Open AccessReview

Emerging Treatment Options for Gastroenteropancreatic Neuroendocrine Tumors

by Mauro Cives, Eleonora Pelle’ and Jonathan Strosberg

J. Clin. Med. 2020, 9(11), 3655; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm9113655 - 13 Nov 2020

Cited by 23 | Viewed by 3572

Abstract

Treatment options for neuroendocrine tumors (NETs) and carcinomas (NECs) are expanding. Early-phase studies have shown preliminary evidence of the antitumor activity of alpha-emitting peptide receptor radionuclide therapy (PRRT), and novel radiopeptides incorporating somatostatin receptor antagonists (rather than agonists) have been developed. Several tyrosine kinase inhibitors (TKIs) with antiangiogenic potential have been evaluated in patients with NETs, including lenvatinib, axitinib, cabozantinib and pazopanib. Recently, two phase 3 clinical trials have demonstrated the efficacy and safety of surufatinib, an inhibitor of vascular endothelial growth factor receptor (VEGFR)-1, -2, -3, fibroblast growth factor receptor (FGFR)-1 and colony stimulating factor-1 receptor (CSF-1R), in patients with pancreatic and extra-pancreatic NETs. Multiple clinical trials of combination immunotherapy have been recently completed, but interpretation of the results is hampered by small samples sizes and discordant outcomes. This review summarizes recent data on emerging treatments for neuroendocrine neoplasms. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

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15 pages, 300 KiB

Open AccessReview

Advances in the Management of Medullary Thyroid Carcinoma: Focus on Peptide Receptor Radionuclide Therapy

by Erika Grossrubatscher, Giuseppe Fanciulli, Luca Pes, Franz Sesti, Carlotta Dolci, Federica de Cicco, Annamaria Colao, Antongiulio Faggiano and NIKE Group

J. Clin. Med. 2020, 9(11), 3507; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm9113507 - 29 Oct 2020

Cited by 21 | Viewed by 2608

Abstract

Effective treatment options in advanced/progressive/metastatic medullary thyroid carcinoma (MTC) are currently limited. As in other neuroendocrine neoplasms (NENs), peptide receptor radionuclide therapy (PRRT) has been used as a therapeutic option in MTC. To date, however, there are no published reviews dealing with PRRT approaches. We performed an in-depth narrative review on the studies published in this field and collected information on registered clinical trials related to this topic. We identified 19 published studies, collectively involving more than 200 patients with MTC, and four registered clinical trials. Most cases of MTC were treated with PRRT with somatostatin analogues (SSAs) radiolabelled with 90 yttrium (90Y) and 177 lutetium (177Lu). These radiopharmaceuticals show efficacy in the treatment of patients with MTC, with a favourable radiological response (stable disease, partial response or complete response) in more than 60% of cases, coupled with low toxicity. As MTC specifically also expresses cholecystokinin receptors (CCK2Rs), PRRT with this target has also been tried, and some randomised trials are ongoing. Overall, PRRT seems to have an effective role and might be considered in the therapeutic strategy of advanced/progressive/metastatic MTC. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

14 pages, 2736 KiB

Open AccessReview

Essentials of Insulinoma Localization with Selective Arterial Calcium Stimulation and Hepatic Venous Sampling

by Ken Zhao, Nihal Patel, Kopal Kulkarni, Jonathan S. Gross and Bedros Taslakian

J. Clin. Med. 2020, 9(10), 3091; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm9103091 - 25 Sep 2020

Cited by 10 | Viewed by 4754

Abstract

Insulinomas are the most common functional pancreatic neuroendocrine tumor. Most insulinomas can be localized non-invasively with cross-sectional and nuclear imaging. Selective arterial calcium stimulation and hepatic venous sampling is an effective and safe minimally-invasive procedure for insulinoma localization that may be utilized when non-invasive techniques are inconclusive. The procedure’s technical success and proper interpretation of its results is dependent on the interventional radiologist’s knowledge of normal and variant pancreatic arterial perfusion. Accurate pre-operative localization aids in successful surgical resection. Technical and anatomic considerations of insulinoma localization with selective arterial calcium stimulation and hepatic venous sampling are reviewed. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

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19 pages, 829 KiB

Open AccessReview

Differential Diagnosis and Management of Diarrhea in Patients with Neuroendocrine Tumors

by Sara Pusceddu, Roberta Elisa Rossi, Martina Torchio, Natalie Prinzi, Monica Niger, Jorgelina Coppa, Luca Giacomelli, Rodolfo Sacco, Antonio Facciorusso, Francesca Corti, Alessandra Raimondi, Michele Prisciandaro, Elena Colombo, Teresa Beninato, Marta Del Vecchio, Massimo Milione, Maria Di Bartolomeo and Filippo de Braud

J. Clin. Med. 2020, 9(8), 2468; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm9082468 - 01 Aug 2020

Cited by 12 | Viewed by 6739

Abstract

Diarrhea is a recurrent symptom in patients with neuroendocrine tumors (NETs) and can represent different etiologies; thus, differential diagnosis is challenging. This paper distinguishes the different causes of chronic diarrhea in patients with gastroenteropancreatic NETs, with the aim to identify the most appropriate therapeutic approach. Underlying causes of diarrhea can be multifactorial, including not only diarrhea that is related to specific hormonal hypersecretory syndromes, but also diarrhea that is secondary to the following: extensive surgery which can cause pancreatic exocrine insufficiency or short bowel syndrome, treatment with somatostatin analogs or other antineoplastic agents, and bile acid malabsorption. After initial management of diarrhea with general treatments (dietary modification, use of antidiarrheals), a proper differential diagnosis is necessary to treat patients with specific etiology-driven therapeutic approaches, such as somatostatin analogs, pancreatic enzyme replacement therapy, and tryptophan hydroxylase inhibitors. In conclusion, NETs should be considered in the differential diagnosis of patients suffering from chronic diarrhea, after the exclusion of more common etiologies. Furthermore, physicians should keep in mind that several different etiologies might be responsible for diarrhea occurrence in NET patients. A prompt diagnosis of the actual cause of diarrhea is necessary to guide the treatment and a multidisciplinary approach is mandatory. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

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16 pages, 12280 KiB

Open AccessReview

Prevention and Management of Hormonal Crisis during Theragnosis with LU-DOTA-TATE in Neuroendocrine Tumors. A Systematic Review and Approach Proposal

by Maria Isabel del Olmo-García, Maria Angustias Muros, Martín López-de-la-Torre, Marc Agudelo, Pilar Bello, Jose M. Soriano and Juan-Francisco Merino-Torres

J. Clin. Med. 2020, 9(7), 2203; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm9072203 - 12 Jul 2020

Cited by 17 | Viewed by 4274

Abstract

Neuroendocrine tumors (NETs) frequently overexpress somatostatin receptors (SSTR) on their cell surface. The first-line pharmacological treatment for inoperable metastatic functioning well-differentiated NETs are somatostatin analogs. On second line, Lu-DOTA-TATE (¹⁷⁷Lu-DOTA⁰ Tyr ³ octreotate) has shown stabilization of the disease and an increase in progression free survival, as well as effectiveness in controlling symptoms and increasing quality of life. The management of functional NETs before and during LU-DOTA-TATE treatment is specially challenging, as several complications such as severe carcinoid and catecholamine crisis have been described. The aim of this review is to establish practical guidance for the management and prevention of the most common hormonal crises during radionuclide treatment with Lu-DOTA-TATE: carcinoid syndrome (CS) and catecholamine hypersecretion, as well as to provide a brief commentary on other infrequent metabolic complications. To establish a practical approach, a systematic review was performed. This systematic review was developed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement and conducted using MEDLINE (accessed from PubMed), Google Scholar and ClinicalTrials.gov. Literature searches found 449 citations, and finally nine were considered for this systematic review. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

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21 pages, 1799 KiB

Open AccessReview

Pathogenesis and Clinical Management of Mesenteric Fibrosis in Small Intestinal Neuroendocine Neoplasms: A Systematic Review

by Anna Koumarianou, Krystallenia I. Alexandraki, Göran Wallin, Gregory Kaltsas and Kosmas Daskalakis

J. Clin. Med. 2020, 9(6), 1777; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm9061777 - 08 Jun 2020

Cited by 17 | Viewed by 3319

Abstract

Mesenteric fibrosis (MF) constitutes an underrecognized sequela in patients with small intestinal neuroendocrine neoplasms (SI-NENs), often complicating the disease clinical course. The aim of the present systematic review, carried out by Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) methodology, is to provide an update in evolving aspects of MF pathogenesis and its clinical management in SI-NENs. Complex and dynamic interactions are present in the microenvironment of tumor deposits in the mesentery. Serotonin, as well as the signaling pathways of certain growth factors play a pivotal, yet not fully elucidated role in the pathogenesis of MF. Clinically, MF often results in significant morbidity by causing either acute complications, such as intestinal obstruction and/or acute ischemia or more chronic conditions involving abdominal pain, venous stasis, malabsorption and malnutrition. Surgical resection in patients with locoregional disease only or symptomatic distant stage disease, as well as palliative minimally invasive interventions in advanced inoperable cases seem clinically meaningful, whereas currently available systemic and/or targeted treatments do not unequivocally affect the development of MF in SI-NENs. Increased awareness and improved understanding of the molecular pathogenesis of MF in SI-NENs may provide better diagnostic and predictive tools for its timely recognition and intervention and also facilitates the development of agents targeting MF. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

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20 pages, 2546 KiB

Open AccessReview

Neuroendocrine Cancer of the Breast: A Rare Entity

by Azzurra Irelli, Maria Maddalena Sirufo, Luca Morelli, Carlo D’Ugo, Lia Ginaldi and Massimo De Martinis

J. Clin. Med. 2020, 9(5), 1452; https://0-doi-org.brum.beds.ac.uk/10.3390/jcm9051452 - 13 May 2020

Cited by 21 | Viewed by 10513

Abstract

Neuroendocrine breast cancer (NEBC) is a rare histotype of breast carcinoma that presents, in most cases, positive hormone receptors and negative HER2. Indeed, the analysis of gene expression profiles revealed that NEBC belongs mainly to the luminal subtype. Cases of HER2-positive and triple-negative NEBC are rare. The cardinal treatment of early NEBC is surgery, similar to the treatment of invasive non-special histological type carcinoma. The use of radiotherapy follows the criteria applied in infiltrating breast cancer of non-special histotype. In the post-operative phase, therefore after the surgical treatment of mammary quadrantectomy, or mastectomy associated with homolateral sentinel lymph node removal ± axillary dissection, based on the histopathological characteristics of the tumor, the use of chemotherapy (anthracycline + taxane) and/or hormone therapy, whether or not associated with anti-HER2 therapy (trastuzumab) is the rule. Literature data report the use of cisplatin and etoposide, as in small cell lung cancers. Most of the information currently available derive from single case reports or a series of clinical cases; it follows the difficulty of formulating definite recommendations on the correct management of this histological type of breast cancer. This review describes available knowledge on this rare entity to improve the diagnostic and therapeutic strategies and offer insights to stimulate exploration of the many aspects still unknown. Full article

(This article belongs to the Special Issue Neuroendocrine Tumors: Clinical Challenges)

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