Clinical outcomes and safety of immune checkpoint inhibitors in patients with solid tumors and paraneoplastic syndromes

Background Patients with paraneoplastic syndromes (PNS) are excluded from clinical trials involving immune checkpoint inhibitors (ICIs) due to safety concerns. Moreover, real-world data on efficacy and safety is scarce.Methods In this retrospective study, data were collected on patients with PNS and...

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Main Authors: Lucia Kwak, So Yeon Kim, Guru Sonpavde, Elad Sharon, Abdul Rafeh Naqash, Alessio Cortellini, Rana R McKay, Toni K Choueiri, Thomas Marron, Amin H Nassar, Jeffrey A Sparks, Kaushal Parikh, Frank Aboubakar Nana, Jenny Linnoila, Shruti Gupta, Nicole R LeBoeuf, Elio Adib, Ahmad Al-Hader, Edward El-Am, Dory Freeman, Ahmed Bilal Khalid, Marita Salame, Elias Bou Farhat, Arjun Ravishankar, Bachar Ahmad, David Kaldas, Andrea Malgeri, Ole-Petter R Hamnvik, Thomas Dilling, Elie Najem, Talal El Zarif, Serena Rahme, Caiwei Zhong, Tarek H Mouhieddine
Format: Article
Language:English
Published: BMJ Publishing Group 2024-03-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/12/3/e008724.full
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author Lucia Kwak
So Yeon Kim
Guru Sonpavde
Elad Sharon
Abdul Rafeh Naqash
Alessio Cortellini
Rana R McKay
Toni K Choueiri
Thomas Marron
Amin H Nassar
Jeffrey A Sparks
Kaushal Parikh
Frank Aboubakar Nana
Jenny Linnoila
Shruti Gupta
Nicole R LeBoeuf
Elio Adib
Ahmad Al-Hader
Edward El-Am
Dory Freeman
Ahmed Bilal Khalid
Marita Salame
Elias Bou Farhat
Arjun Ravishankar
Bachar Ahmad
David Kaldas
Andrea Malgeri
Ole-Petter R Hamnvik
Thomas Dilling
Elie Najem
Talal El Zarif
Serena Rahme
Caiwei Zhong
Tarek H Mouhieddine
author_facet Lucia Kwak
So Yeon Kim
Guru Sonpavde
Elad Sharon
Abdul Rafeh Naqash
Alessio Cortellini
Rana R McKay
Toni K Choueiri
Thomas Marron
Amin H Nassar
Jeffrey A Sparks
Kaushal Parikh
Frank Aboubakar Nana
Jenny Linnoila
Shruti Gupta
Nicole R LeBoeuf
Elio Adib
Ahmad Al-Hader
Edward El-Am
Dory Freeman
Ahmed Bilal Khalid
Marita Salame
Elias Bou Farhat
Arjun Ravishankar
Bachar Ahmad
David Kaldas
Andrea Malgeri
Ole-Petter R Hamnvik
Thomas Dilling
Elie Najem
Talal El Zarif
Serena Rahme
Caiwei Zhong
Tarek H Mouhieddine
author_sort Lucia Kwak
collection DOAJ
description Background Patients with paraneoplastic syndromes (PNS) are excluded from clinical trials involving immune checkpoint inhibitors (ICIs) due to safety concerns. Moreover, real-world data on efficacy and safety is scarce.Methods In this retrospective study, data were collected on patients with PNS and solid tumors receiving ICI between 2015 and 2022 at nine institutions. Patients were classified into: Cohort 1 (pre-existing PNS before ICI initiation), cohort 2 (PNS during ICI treatment), and cohort 3 (PNS after ICI discontinuation). Patients with metastatic non-small cell lung cancer (NSCLC) (mNSCLC) from cohort 1 were matched to patients who were PNS-free at each institution up to a 1:3 ratio for age, sex, type of ICI, use of concurrent chemotherapy, and number of lines of systemic therapy prior to ICI initiation. Kaplan-Meier method was used to assess overall survival (OS) and time-to-next treatment (TTNT).Results Among 109 patients with PNS treated with ICIs, median age at ICI initiation was 67 years (IQR: 58–74). The most represented cancer type was NSCLC (n=39, 36%). In cohort 1 (n=55), PNS exacerbations occurred in 16 (29%) patients with median time to exacerbation after ICI of 1.1 months (IQR: 0.7–3.3). Exacerbation or de novo PNS prompted temporary/permanent interruption of ICIs in 14 (13%) patients. For cohort 2 (n=16), median time between ICI initiation and de novo PNS was 1.2 months (IQR: 0.4–3.5). Treatment-related adverse events (trAEs) occurred in 43 (39%) patients. Grade ≥3 trAEs occurred in 18 (17%) patients. PNS-directed immunosuppressive therapy was required in 55 (50%) patients. We matched 18 patients with mNSCLC and PNS (cohort 1) to 40 without PNS, treated with ICIs. There was no significant difference in OS or TTNT between patients with mNSCLC with and without PNS, although a trend was seen towards worse outcomes in patients with PNS. TrAEs occurred in 6/18 (33%) and 14/40 (35%), respectively. Grade ≥3 trAEs occurred in 4 (22%) patients with PNS and 7 (18%) patients without PNS.Conclusions Exacerbations of pre-existing PNS occurred in 29% of patients treated with ICIs and both exacerbations and de novo PNS occur early in the ICI course. TrAE from ICIs were similar between patients with and without PNS. Our data suggest that pre-existing PNS should not preclude consideration of ICI therapy although patients may not derive the same clinical benefit compared with patients without PNS.
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spelling doaj-art-e3a36a44dc60429b90c5ae6bfb3606602025-08-20T01:58:00ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262024-03-0112310.1136/jitc-2023-008724Clinical outcomes and safety of immune checkpoint inhibitors in patients with solid tumors and paraneoplastic syndromesLucia Kwak0So Yeon Kim1Guru Sonpavde2Elad Sharon3Abdul Rafeh Naqash4Alessio Cortellini5Rana R McKay6Toni K Choueiri7Thomas Marron8Amin H Nassar9Jeffrey A Sparks10Kaushal Parikh11Frank Aboubakar Nana12Jenny Linnoila13Shruti Gupta14Nicole R LeBoeuf15Elio Adib16Ahmad Al-Hader17Edward El-Am18Dory Freeman19Ahmed Bilal Khalid20Marita Salame21Elias Bou Farhat22Arjun Ravishankar23Bachar Ahmad24David Kaldas25Andrea Malgeri26Ole-Petter R Hamnvik27Thomas Dilling28Elie Najem29Talal El Zarif30Serena Rahme31Caiwei Zhong32Tarek H Mouhieddine33Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USAYale University, New Haven, Connecticut, USAAdventHealth Cancer Institute, Orlando, Florida, USADFCI, Boston, Massachusetts, USAMedical Oncology/TSET Phase 1 Program, The University of Oklahoma Stephenson Cancer Center, Oklahoma City, Oklahoma, USADepartment of Medicine and Surgery, Università Campus Bio-Medico di Roma, Roma, ItalyDivision of Medical Oncology, University of California San Diego, La Jolla, California, USA1 Harvard Medical School, Boston, Massachussetts, USAOncology, Icahn School of Medicine at Mount Sinai, New York, New York, USADepartment of Hematology/Oncology, Yale New Haven Hospital, New Haven, Connecticut, USA2 Division of Rheumatology, Immunology and Allergy, Department of Medicine, Brigham and Women`s Hospital, Boston, Massachusetts, USAMayo Clinic, Rochester, Minnesota, USADivision of Pneumology, CHU UCL Namur, Yvoir, Namur, BelgiumMassachusetts General Hospital, Boston, Massachusetts, USAassistant professor3 Harvard Medical School, Boston, Massachusetts, USAHarvard Medical School, Boston, Massachusetts, USAIndiana Melvin and Bren Simon Comprehensive Cancer Center, Indianapolis, Indiana, USAMayo Clinic, Rochester, Minnesota, USADepartment of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USAIndiana Melvin and Bren Simon Comprehensive Cancer Center, Indianapolis, Indiana, USAMayo Clinic, Rochester, Minnesota, USADepartment of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USAYale University, New Haven, Connecticut, USAYale University, New Haven, Connecticut, USADepartment of Internal Medicine, University of South Florida, Tampa, Florida, USAMedical Oncology, Fondazione Policlinico Universitario Campus Bio-Medico, Rome, ItalyHarvard Medical School, Boston, Massachusetts, USADepartment of Internal Medicine, University of South Florida, Tampa, Florida, USADepartment of Radiology, Harvard Medical School, Boston, Massachusetts, USAYale University, New Haven, Connecticut, USADepartment of Cardiovascular Medicine, Mayo Clinic, Rochester, New York, USADepartment of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts, USAIcahn School of Medicine at Mount Sinai, New York, New York, USABackground Patients with paraneoplastic syndromes (PNS) are excluded from clinical trials involving immune checkpoint inhibitors (ICIs) due to safety concerns. Moreover, real-world data on efficacy and safety is scarce.Methods In this retrospective study, data were collected on patients with PNS and solid tumors receiving ICI between 2015 and 2022 at nine institutions. Patients were classified into: Cohort 1 (pre-existing PNS before ICI initiation), cohort 2 (PNS during ICI treatment), and cohort 3 (PNS after ICI discontinuation). Patients with metastatic non-small cell lung cancer (NSCLC) (mNSCLC) from cohort 1 were matched to patients who were PNS-free at each institution up to a 1:3 ratio for age, sex, type of ICI, use of concurrent chemotherapy, and number of lines of systemic therapy prior to ICI initiation. Kaplan-Meier method was used to assess overall survival (OS) and time-to-next treatment (TTNT).Results Among 109 patients with PNS treated with ICIs, median age at ICI initiation was 67 years (IQR: 58–74). The most represented cancer type was NSCLC (n=39, 36%). In cohort 1 (n=55), PNS exacerbations occurred in 16 (29%) patients with median time to exacerbation after ICI of 1.1 months (IQR: 0.7–3.3). Exacerbation or de novo PNS prompted temporary/permanent interruption of ICIs in 14 (13%) patients. For cohort 2 (n=16), median time between ICI initiation and de novo PNS was 1.2 months (IQR: 0.4–3.5). Treatment-related adverse events (trAEs) occurred in 43 (39%) patients. Grade ≥3 trAEs occurred in 18 (17%) patients. PNS-directed immunosuppressive therapy was required in 55 (50%) patients. We matched 18 patients with mNSCLC and PNS (cohort 1) to 40 without PNS, treated with ICIs. There was no significant difference in OS or TTNT between patients with mNSCLC with and without PNS, although a trend was seen towards worse outcomes in patients with PNS. TrAEs occurred in 6/18 (33%) and 14/40 (35%), respectively. Grade ≥3 trAEs occurred in 4 (22%) patients with PNS and 7 (18%) patients without PNS.Conclusions Exacerbations of pre-existing PNS occurred in 29% of patients treated with ICIs and both exacerbations and de novo PNS occur early in the ICI course. TrAE from ICIs were similar between patients with and without PNS. Our data suggest that pre-existing PNS should not preclude consideration of ICI therapy although patients may not derive the same clinical benefit compared with patients without PNS.https://jitc.bmj.com/content/12/3/e008724.full
spellingShingle Lucia Kwak
So Yeon Kim
Guru Sonpavde
Elad Sharon
Abdul Rafeh Naqash
Alessio Cortellini
Rana R McKay
Toni K Choueiri
Thomas Marron
Amin H Nassar
Jeffrey A Sparks
Kaushal Parikh
Frank Aboubakar Nana
Jenny Linnoila
Shruti Gupta
Nicole R LeBoeuf
Elio Adib
Ahmad Al-Hader
Edward El-Am
Dory Freeman
Ahmed Bilal Khalid
Marita Salame
Elias Bou Farhat
Arjun Ravishankar
Bachar Ahmad
David Kaldas
Andrea Malgeri
Ole-Petter R Hamnvik
Thomas Dilling
Elie Najem
Talal El Zarif
Serena Rahme
Caiwei Zhong
Tarek H Mouhieddine
Clinical outcomes and safety of immune checkpoint inhibitors in patients with solid tumors and paraneoplastic syndromes
Journal for ImmunoTherapy of Cancer
title Clinical outcomes and safety of immune checkpoint inhibitors in patients with solid tumors and paraneoplastic syndromes
title_full Clinical outcomes and safety of immune checkpoint inhibitors in patients with solid tumors and paraneoplastic syndromes
title_fullStr Clinical outcomes and safety of immune checkpoint inhibitors in patients with solid tumors and paraneoplastic syndromes
title_full_unstemmed Clinical outcomes and safety of immune checkpoint inhibitors in patients with solid tumors and paraneoplastic syndromes
title_short Clinical outcomes and safety of immune checkpoint inhibitors in patients with solid tumors and paraneoplastic syndromes
title_sort clinical outcomes and safety of immune checkpoint inhibitors in patients with solid tumors and paraneoplastic syndromes
url https://jitc.bmj.com/content/12/3/e008724.full
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