Targeted Genetic Sequencing Analysis of 223 Cases of Pseudomyxoma Peritonei Treated by Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy Shows Survival Related to GNAS and KRAS Status

ABSTRACT Background and Aim Pseudomyxoma peritonei (PMP) is an unusual condition with unique behaviour caused by a mucinous neoplasm, usually arising from the appendix. The aim of this study was to evaluate the prevalence of genomic alterations in clinical specimens of PMP using a targeted assay and...

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Main Authors: Jane Gibson, Reuben J. Pengelly, Amatta Mirandari, Konstantinos Boukas, Sophia Stanford, Thomas Desmond Cecil, Faheez Mohamed, Sanjeev Paul Dayal, Alexios Tzivanakis, Brendan John Moran, Alex Mirnezami, Norman John Carr, Sarah Ennis
Format: Article
Language:English
Published: Wiley 2024-10-01
Series:Cancer Medicine
Online Access:https://doi.org/10.1002/cam4.70340
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author Jane Gibson
Reuben J. Pengelly
Amatta Mirandari
Konstantinos Boukas
Sophia Stanford
Thomas Desmond Cecil
Faheez Mohamed
Sanjeev Paul Dayal
Alexios Tzivanakis
Brendan John Moran
Alex Mirnezami
Norman John Carr
Sarah Ennis
author_facet Jane Gibson
Reuben J. Pengelly
Amatta Mirandari
Konstantinos Boukas
Sophia Stanford
Thomas Desmond Cecil
Faheez Mohamed
Sanjeev Paul Dayal
Alexios Tzivanakis
Brendan John Moran
Alex Mirnezami
Norman John Carr
Sarah Ennis
author_sort Jane Gibson
collection DOAJ
description ABSTRACT Background and Aim Pseudomyxoma peritonei (PMP) is an unusual condition with unique behaviour caused by a mucinous neoplasm, usually arising from the appendix. The aim of this study was to evaluate the prevalence of genomic alterations in clinical specimens of PMP using a targeted assay and correlate the findings with clinical, pathological and outcome data. Sequencing data from 223 patients were analysed. Results The median follow‐up interval was 48 months. The primary neoplasm was appendiceal in 216 patients, ovarian in 4, urachal in 2 and renal in one. We confirmed common mutations in GNAS and KRAS (42% each) with significant co‐occurrence of variants in these genes. TP53 mutations were found in 8%. Other mutations were rare but included novel mutations in BAP1 and ERBB4. Of 17 patients with acellular peritoneal mucin, 6 (35%) were positive for DNA mutations. The non‐appendiceal cases generally showed a similar mutational landscape to the appendiceal lesions with GNAS and KRAS commonly mutated, although one urachal lesion showed multi‐hit TP53 mutation without variants in either GNAS or KRAS. Survival was significantly associated with the grade of the primary neoplasm, the grade of the peritoneal disease, the completeness of cytoreduction score and with mutation in either GNAS, KRAS or both. The hazard ratio (HR) associated with mutation in GNAS and/or KRAS was 1.87 (p = 0.004). Conclusions Survival outcome was more closely associated with the grade of the peritoneal disease than with the grade of the primary neoplasm. Our findings support the developing concept that mutational analysis may provide prognostic information in patients with PMP.
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spelling doaj-art-a576fc9c5d5f4fe6b861a0b303a2fb742025-08-20T02:17:59ZengWileyCancer Medicine2045-76342024-10-011320n/an/a10.1002/cam4.70340Targeted Genetic Sequencing Analysis of 223 Cases of Pseudomyxoma Peritonei Treated by Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy Shows Survival Related to GNAS and KRAS StatusJane Gibson0Reuben J. Pengelly1Amatta Mirandari2Konstantinos Boukas3Sophia Stanford4Thomas Desmond Cecil5Faheez Mohamed6Sanjeev Paul Dayal7Alexios Tzivanakis8Brendan John Moran9Alex Mirnezami10Norman John Carr11Sarah Ennis12Cancer Sciences, Faculty of Medicine University of Southampton Southampton UKHuman Development and Health, Faculty of Medicine University of Southampton Southampton UKCancer Sciences, Faculty of Medicine University of Southampton Southampton UKWessex Investigational Sciences Hub, Cancer Sciences, Faculty of Medicine University of Southampton, Southampton General Hospital Southampton UKPeritoneal Malignancy Institute Basingstoke and North Hampshire Hospital Basingstoke UKPeritoneal Malignancy Institute Basingstoke and North Hampshire Hospital Basingstoke UKPeritoneal Malignancy Institute Basingstoke and North Hampshire Hospital Basingstoke UKPeritoneal Malignancy Institute Basingstoke and North Hampshire Hospital Basingstoke UKPeritoneal Malignancy Institute Basingstoke and North Hampshire Hospital Basingstoke UKPeritoneal Malignancy Institute Basingstoke and North Hampshire Hospital Basingstoke UKCancer Sciences, Faculty of Medicine University of Southampton Southampton UKHuman Development and Health, Faculty of Medicine University of Southampton Southampton UKHuman Development and Health, Faculty of Medicine University of Southampton Southampton UKABSTRACT Background and Aim Pseudomyxoma peritonei (PMP) is an unusual condition with unique behaviour caused by a mucinous neoplasm, usually arising from the appendix. The aim of this study was to evaluate the prevalence of genomic alterations in clinical specimens of PMP using a targeted assay and correlate the findings with clinical, pathological and outcome data. Sequencing data from 223 patients were analysed. Results The median follow‐up interval was 48 months. The primary neoplasm was appendiceal in 216 patients, ovarian in 4, urachal in 2 and renal in one. We confirmed common mutations in GNAS and KRAS (42% each) with significant co‐occurrence of variants in these genes. TP53 mutations were found in 8%. Other mutations were rare but included novel mutations in BAP1 and ERBB4. Of 17 patients with acellular peritoneal mucin, 6 (35%) were positive for DNA mutations. The non‐appendiceal cases generally showed a similar mutational landscape to the appendiceal lesions with GNAS and KRAS commonly mutated, although one urachal lesion showed multi‐hit TP53 mutation without variants in either GNAS or KRAS. Survival was significantly associated with the grade of the primary neoplasm, the grade of the peritoneal disease, the completeness of cytoreduction score and with mutation in either GNAS, KRAS or both. The hazard ratio (HR) associated with mutation in GNAS and/or KRAS was 1.87 (p = 0.004). Conclusions Survival outcome was more closely associated with the grade of the peritoneal disease than with the grade of the primary neoplasm. Our findings support the developing concept that mutational analysis may provide prognostic information in patients with PMP.https://doi.org/10.1002/cam4.70340
spellingShingle Jane Gibson
Reuben J. Pengelly
Amatta Mirandari
Konstantinos Boukas
Sophia Stanford
Thomas Desmond Cecil
Faheez Mohamed
Sanjeev Paul Dayal
Alexios Tzivanakis
Brendan John Moran
Alex Mirnezami
Norman John Carr
Sarah Ennis
Targeted Genetic Sequencing Analysis of 223 Cases of Pseudomyxoma Peritonei Treated by Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy Shows Survival Related to GNAS and KRAS Status
Cancer Medicine
title Targeted Genetic Sequencing Analysis of 223 Cases of Pseudomyxoma Peritonei Treated by Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy Shows Survival Related to GNAS and KRAS Status
title_full Targeted Genetic Sequencing Analysis of 223 Cases of Pseudomyxoma Peritonei Treated by Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy Shows Survival Related to GNAS and KRAS Status
title_fullStr Targeted Genetic Sequencing Analysis of 223 Cases of Pseudomyxoma Peritonei Treated by Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy Shows Survival Related to GNAS and KRAS Status
title_full_unstemmed Targeted Genetic Sequencing Analysis of 223 Cases of Pseudomyxoma Peritonei Treated by Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy Shows Survival Related to GNAS and KRAS Status
title_short Targeted Genetic Sequencing Analysis of 223 Cases of Pseudomyxoma Peritonei Treated by Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy Shows Survival Related to GNAS and KRAS Status
title_sort targeted genetic sequencing analysis of 223 cases of pseudomyxoma peritonei treated by cytoreductive surgery and hyperthermic intraperitoneal chemotherapy shows survival related to gnas and kras status
url https://doi.org/10.1002/cam4.70340
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