Evaluation of therapeutic agent selection based on comprehensive genomic profiling in gastroenteropancreatic neuroendocrine neoplasms
Comprehensive genomic profiling (CGP) is increasingly being integrated into standard clinical practice as a strategy to guide subsequent treatment decisions by identifying novel therapeutic options based on tumor-specific mutations. However, its clinical utility in neuroendocrine neoplasms (NENs) re...
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| Published in | PloS one Vol. 20; no. 8; p. e0325727 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
06.08.2025
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1932-6203 1932-6203 |
| DOI | 10.1371/journal.pone.0325727 |
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| Abstract | Comprehensive genomic profiling (CGP) is increasingly being integrated into standard clinical practice as a strategy to guide subsequent treatment decisions by identifying novel therapeutic options based on tumor-specific mutations. However, its clinical utility in neuroendocrine neoplasms (NENs) remains to be determined. We conducted a cross-sectional analysis of genomic alterations, including tumor mutational burden (TMB) and microsatellite instability (MSI), in gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs), comparing neuroendocrine tumors (NETs) and neuroendocrine carcinomas (NECs).
CGP was performed on 50 patients with advanced GEP-NENs between August 2017 and October 2023. Of these, 38 were diagnosed with NETs and 12 with NECs. Primary tumor sites included the pancreas (n = 24), gastrointestinal tract (n = 25), and one case of unknown origin. In our study, CGP analysis comparing NETs and NECs documented different genetic profiles. In addition, median TMB was significantly higher in NECs (5.0 vs. 1.9 mutations/megabase; p = 0.0101). High TMB was identified in 4 of 12 NECs (33.3%) and in only 1 of 38 NETs (2.6%) (p = 0.0093). NECs also harbored a significantly greater number of mutations per case than NETs (5.5 vs. 2.0; p = 0.0014). Actionable mutations were identified in 18 of 50 patients, and 7 patients received mutation-guided therapy: 2 with NETs and 5 with NECs. The frequency of treatment initiation based on CGP findings was significantly higher in patients with NECs (p = 0.0059).
NECs are genetically distinct from NETs, with a higher prevalence of actionable mutations and greater therapeutic relevance of CGP findings. These results suggest that CGP may be particularly valuable in NECs, where therapeutic options are limited, supporting its proactive implementation in this subgroup. |
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| AbstractList | IntroductionComprehensive genomic profiling (CGP) is increasingly being integrated into standard clinical practice as a strategy to guide subsequent treatment decisions by identifying novel therapeutic options based on tumor-specific mutations. However, its clinical utility in neuroendocrine neoplasms (NENs) remains to be determined. We conducted a cross-sectional analysis of genomic alterations, including tumor mutational burden (TMB) and microsatellite instability (MSI), in gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs), comparing neuroendocrine tumors (NETs) and neuroendocrine carcinomas (NECs).ResultsCGP was performed on 50 patients with advanced GEP-NENs between August 2017 and October 2023. Of these, 38 were diagnosed with NETs and 12 with NECs. Primary tumor sites included the pancreas (n = 24), gastrointestinal tract (n = 25), and one case of unknown origin. In our study, CGP analysis comparing NETs and NECs documented different genetic profiles. In addition, median TMB was significantly higher in NECs (5.0 vs. 1.9 mutations/megabase; p = 0.0101). High TMB was identified in 4 of 12 NECs (33.3%) and in only 1 of 38 NETs (2.6%) (p = 0.0093). NECs also harbored a significantly greater number of mutations per case than NETs (5.5 vs. 2.0; p = 0.0014). Actionable mutations were identified in 18 of 50 patients, and 7 patients received mutation-guided therapy: 2 with NETs and 5 with NECs. The frequency of treatment initiation based on CGP findings was significantly higher in patients with NECs (p = 0.0059).ConclusionsNECs are genetically distinct from NETs, with a higher prevalence of actionable mutations and greater therapeutic relevance of CGP findings. These results suggest that CGP may be particularly valuable in NECs, where therapeutic options are limited, supporting its proactive implementation in this subgroup. Comprehensive genomic profiling (CGP) is increasingly being integrated into standard clinical practice as a strategy to guide subsequent treatment decisions by identifying novel therapeutic options based on tumor-specific mutations. However, its clinical utility in neuroendocrine neoplasms (NENs) remains to be determined. We conducted a cross-sectional analysis of genomic alterations, including tumor mutational burden (TMB) and microsatellite instability (MSI), in gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs), comparing neuroendocrine tumors (NETs) and neuroendocrine carcinomas (NECs). CGP was performed on 50 patients with advanced GEP-NENs between August 2017 and October 2023. Of these, 38 were diagnosed with NETs and 12 with NECs. Primary tumor sites included the pancreas (n = 24), gastrointestinal tract (n = 25), and one case of unknown origin. In our study, CGP analysis comparing NETs and NECs documented different genetic profiles. In addition, median TMB was significantly higher in NECs (5.0 vs. 1.9 mutations/megabase; p = 0.0101). High TMB was identified in 4 of 12 NECs (33.3%) and in only 1 of 38 NETs (2.6%) (p = 0.0093). NECs also harbored a significantly greater number of mutations per case than NETs (5.5 vs. 2.0; p = 0.0014). Actionable mutations were identified in 18 of 50 patients, and 7 patients received mutation-guided therapy: 2 with NETs and 5 with NECs. The frequency of treatment initiation based on CGP findings was significantly higher in patients with NECs (p = 0.0059). NECs are genetically distinct from NETs, with a higher prevalence of actionable mutations and greater therapeutic relevance of CGP findings. These results suggest that CGP may be particularly valuable in NECs, where therapeutic options are limited, supporting its proactive implementation in this subgroup. Introduction Comprehensive genomic profiling (CGP) is increasingly being integrated into standard clinical practice as a strategy to guide subsequent treatment decisions by identifying novel therapeutic options based on tumor-specific mutations. However, its clinical utility in neuroendocrine neoplasms (NENs) remains to be determined. We conducted a cross-sectional analysis of genomic alterations, including tumor mutational burden (TMB) and microsatellite instability (MSI), in gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs), comparing neuroendocrine tumors (NETs) and neuroendocrine carcinomas (NECs). Results CGP was performed on 50 patients with advanced GEP-NENs between August 2017 and October 2023. Of these, 38 were diagnosed with NETs and 12 with NECs. Primary tumor sites included the pancreas (n = 24), gastrointestinal tract (n = 25), and one case of unknown origin. In our study, CGP analysis comparing NETs and NECs documented different genetic profiles. In addition, median TMB was significantly higher in NECs (5.0 vs. 1.9 mutations/megabase; p = 0.0101). High TMB was identified in 4 of 12 NECs (33.3%) and in only 1 of 38 NETs (2.6%) ( p = 0.0093). NECs also harbored a significantly greater number of mutations per case than NETs (5.5 vs. 2.0; p = 0.0014). Actionable mutations were identified in 18 of 50 patients, and 7 patients received mutation-guided therapy: 2 with NETs and 5 with NECs. The frequency of treatment initiation based on CGP findings was significantly higher in patients with NECs ( p = 0.0059). Conclusions NECs are genetically distinct from NETs, with a higher prevalence of actionable mutations and greater therapeutic relevance of CGP findings. These results suggest that CGP may be particularly valuable in NECs, where therapeutic options are limited, supporting its proactive implementation in this subgroup. Introduction Comprehensive genomic profiling (CGP) is increasingly being integrated into standard clinical practice as a strategy to guide subsequent treatment decisions by identifying novel therapeutic options based on tumor-specific mutations. However, its clinical utility in neuroendocrine neoplasms (NENs) remains to be determined. We conducted a cross-sectional analysis of genomic alterations, including tumor mutational burden (TMB) and microsatellite instability (MSI), in gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs), comparing neuroendocrine tumors (NETs) and neuroendocrine carcinomas (NECs). Results CGP was performed on 50 patients with advanced GEP-NENs between August 2017 and October 2023. Of these, 38 were diagnosed with NETs and 12 with NECs. Primary tumor sites included the pancreas (n = 24), gastrointestinal tract (n = 25), and one case of unknown origin. In our study, CGP analysis comparing NETs and NECs documented different genetic profiles. In addition, median TMB was significantly higher in NECs (5.0 vs. 1.9 mutations/megabase; p = 0.0101). High TMB was identified in 4 of 12 NECs (33.3%) and in only 1 of 38 NETs (2.6%) (p = 0.0093). NECs also harbored a significantly greater number of mutations per case than NETs (5.5 vs. 2.0; p = 0.0014). Actionable mutations were identified in 18 of 50 patients, and 7 patients received mutation-guided therapy: 2 with NETs and 5 with NECs. The frequency of treatment initiation based on CGP findings was significantly higher in patients with NECs (p = 0.0059). Conclusions NECs are genetically distinct from NETs, with a higher prevalence of actionable mutations and greater therapeutic relevance of CGP findings. These results suggest that CGP may be particularly valuable in NECs, where therapeutic options are limited, supporting its proactive implementation in this subgroup. Comprehensive genomic profiling (CGP) is increasingly being integrated into standard clinical practice as a strategy to guide subsequent treatment decisions by identifying novel therapeutic options based on tumor-specific mutations. However, its clinical utility in neuroendocrine neoplasms (NENs) remains to be determined. We conducted a cross-sectional analysis of genomic alterations, including tumor mutational burden (TMB) and microsatellite instability (MSI), in gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs), comparing neuroendocrine tumors (NETs) and neuroendocrine carcinomas (NECs).INTRODUCTIONComprehensive genomic profiling (CGP) is increasingly being integrated into standard clinical practice as a strategy to guide subsequent treatment decisions by identifying novel therapeutic options based on tumor-specific mutations. However, its clinical utility in neuroendocrine neoplasms (NENs) remains to be determined. We conducted a cross-sectional analysis of genomic alterations, including tumor mutational burden (TMB) and microsatellite instability (MSI), in gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs), comparing neuroendocrine tumors (NETs) and neuroendocrine carcinomas (NECs).CGP was performed on 50 patients with advanced GEP-NENs between August 2017 and October 2023. Of these, 38 were diagnosed with NETs and 12 with NECs. Primary tumor sites included the pancreas (n = 24), gastrointestinal tract (n = 25), and one case of unknown origin. In our study, CGP analysis comparing NETs and NECs documented different genetic profiles. In addition, median TMB was significantly higher in NECs (5.0 vs. 1.9 mutations/megabase; p = 0.0101). High TMB was identified in 4 of 12 NECs (33.3%) and in only 1 of 38 NETs (2.6%) (p = 0.0093). NECs also harbored a significantly greater number of mutations per case than NETs (5.5 vs. 2.0; p = 0.0014). Actionable mutations were identified in 18 of 50 patients, and 7 patients received mutation-guided therapy: 2 with NETs and 5 with NECs. The frequency of treatment initiation based on CGP findings was significantly higher in patients with NECs (p = 0.0059).RESULTSCGP was performed on 50 patients with advanced GEP-NENs between August 2017 and October 2023. Of these, 38 were diagnosed with NETs and 12 with NECs. Primary tumor sites included the pancreas (n = 24), gastrointestinal tract (n = 25), and one case of unknown origin. In our study, CGP analysis comparing NETs and NECs documented different genetic profiles. In addition, median TMB was significantly higher in NECs (5.0 vs. 1.9 mutations/megabase; p = 0.0101). High TMB was identified in 4 of 12 NECs (33.3%) and in only 1 of 38 NETs (2.6%) (p = 0.0093). NECs also harbored a significantly greater number of mutations per case than NETs (5.5 vs. 2.0; p = 0.0014). Actionable mutations were identified in 18 of 50 patients, and 7 patients received mutation-guided therapy: 2 with NETs and 5 with NECs. The frequency of treatment initiation based on CGP findings was significantly higher in patients with NECs (p = 0.0059).NECs are genetically distinct from NETs, with a higher prevalence of actionable mutations and greater therapeutic relevance of CGP findings. These results suggest that CGP may be particularly valuable in NECs, where therapeutic options are limited, supporting its proactive implementation in this subgroup.CONCLUSIONSNECs are genetically distinct from NETs, with a higher prevalence of actionable mutations and greater therapeutic relevance of CGP findings. These results suggest that CGP may be particularly valuable in NECs, where therapeutic options are limited, supporting its proactive implementation in this subgroup. Comprehensive genomic profiling (CGP) is increasingly being integrated into standard clinical practice as a strategy to guide subsequent treatment decisions by identifying novel therapeutic options based on tumor-specific mutations. However, its clinical utility in neuroendocrine neoplasms (NENs) remains to be determined. We conducted a cross-sectional analysis of genomic alterations, including tumor mutational burden (TMB) and microsatellite instability (MSI), in gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs), comparing neuroendocrine tumors (NETs) and neuroendocrine carcinomas (NECs). CGP was performed on 50 patients with advanced GEP-NENs between August 2017 and October 2023. Of these, 38 were diagnosed with NETs and 12 with NECs. Primary tumor sites included the pancreas (n = 24), gastrointestinal tract (n = 25), and one case of unknown origin. In our study, CGP analysis comparing NETs and NECs documented different genetic profiles. In addition, median TMB was significantly higher in NECs (5.0 vs. 1.9 mutations/megabase; p = 0.0101). High TMB was identified in 4 of 12 NECs (33.3%) and in only 1 of 38 NETs (2.6%) (p = 0.0093). NECs also harbored a significantly greater number of mutations per case than NETs (5.5 vs. 2.0; p = 0.0014). Actionable mutations were identified in 18 of 50 patients, and 7 patients received mutation-guided therapy: 2 with NETs and 5 with NECs. The frequency of treatment initiation based on CGP findings was significantly higher in patients with NECs (p = 0.0059). NECs are genetically distinct from NETs, with a higher prevalence of actionable mutations and greater therapeutic relevance of CGP findings. These results suggest that CGP may be particularly valuable in NECs, where therapeutic options are limited, supporting its proactive implementation in this subgroup. |
| Audience | Academic |
| Author | Ishibashi, Naoya Ono, Hiroaki Yamashita, Hironari Ikeda, Sadakatsu Miyazawa, Suguru Ueda, Hiroki Watanabe, Shuichi Aoyama, Satoru Tanabe, Minoru Asano, Daisuke Akahoshi, Keiichi Ishikawa, Yoshiya |
| AuthorAffiliation | 2 Department of Precision Cancer Medicine, Center for Innovative Cancer Treatment, Institute of Science Tokyo, Tokyo, Japan 1 Department of Hepatobiliary and Pancreatic Surgery, Graduate School of Medicine, Institute of Science Tokyo, Tokyo, Japan University of Split Faculty of Medicine: Sveuciliste u Splitu Medicinski fakultet, CROATIA |
| AuthorAffiliation_xml | – name: University of Split Faculty of Medicine: Sveuciliste u Splitu Medicinski fakultet, CROATIA – name: 1 Department of Hepatobiliary and Pancreatic Surgery, Graduate School of Medicine, Institute of Science Tokyo, Tokyo, Japan – name: 2 Department of Precision Cancer Medicine, Center for Innovative Cancer Treatment, Institute of Science Tokyo, Tokyo, Japan |
| Author_xml | – sequence: 1 givenname: Suguru surname: Miyazawa fullname: Miyazawa, Suguru – sequence: 2 givenname: Hiroaki orcidid: 0000-0001-9230-5714 surname: Ono fullname: Ono, Hiroaki – sequence: 3 givenname: Hironari surname: Yamashita fullname: Yamashita, Hironari – sequence: 4 givenname: Daisuke surname: Asano fullname: Asano, Daisuke – sequence: 5 givenname: Yoshiya surname: Ishikawa fullname: Ishikawa, Yoshiya – sequence: 6 givenname: Shuichi surname: Watanabe fullname: Watanabe, Shuichi – sequence: 7 givenname: Hiroki surname: Ueda fullname: Ueda, Hiroki – sequence: 8 givenname: Satoru surname: Aoyama fullname: Aoyama, Satoru – sequence: 9 givenname: Naoya surname: Ishibashi fullname: Ishibashi, Naoya – sequence: 10 givenname: Keiichi surname: Akahoshi fullname: Akahoshi, Keiichi – sequence: 11 givenname: Sadakatsu orcidid: 0000-0003-1629-7171 surname: Ikeda fullname: Ikeda, Sadakatsu – sequence: 12 givenname: Minoru surname: Tanabe fullname: Tanabe, Minoru |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/40768514$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright: © 2025 Miyazawa et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. COPYRIGHT 2025 Public Library of Science 2025 Miyazawa et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2025 Miyazawa et al 2025 Miyazawa et al 2025 Miyazawa et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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| SubjectTerms | Adult Aged Aged, 80 and over Analysis Bile ducts Biology and Life Sciences Biomarkers, Tumor - genetics Biopsy Cancer Cancer therapies Carcinoma, Neuroendocrine - drug therapy Carcinoma, Neuroendocrine - genetics Carcinoma, Neuroendocrine - pathology Care and treatment Clinical outcomes Cross-Sectional Studies Female Gastrointestinal system Gastrointestinal tract Genes Genetic counseling Genetic markers Genomes Genomic analysis Genomics Health aspects Hospitals Humans Intestinal Neoplasms - drug therapy Intestinal Neoplasms - genetics Intestinal Neoplasms - pathology Liver Lymphatic system Male Medicine and Health Sciences Metastasis Microsatellite Instability Middle Aged Mutation Neoplasms Neuroendocrine tumors Neuroendocrine Tumors - drug therapy Neuroendocrine Tumors - genetics Neuroendocrine Tumors - pathology Pancreatic Neoplasms - drug therapy Pancreatic Neoplasms - genetics Pancreatic Neoplasms - pathology Patients Pharmacology Small intestine Stomach Neoplasms - drug therapy Stomach Neoplasms - genetics Stomach Neoplasms - pathology Subgroups Tumors |
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| Title | Evaluation of therapeutic agent selection based on comprehensive genomic profiling in gastroenteropancreatic neuroendocrine neoplasms |
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