Cited by 277Cancer Immunotherapy and BiomarkersLung Cancer Research StudiesLung Cancer Treatments and Mutations

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Sex-Based Heterogeneity in Response to Lung Cancer Immunotherapy: A Systematic Review and Meta-Analysis

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Conforti, Fabio, Pala, Laura, Bagnardi, Vincenzo, Viale, Giuseppe, De Pas, Tommaso, Pagan, Eleonora, Pennacchioli, Elisabetta, Cocorocchio, Emilia, Ferrucci, Pier Francesco, De Marinis, Filippo, Gelber, Richard D, Goldhirsch, Aron·2019·JNCI: Journal of the National Cancer Institute

DOI 10.1093/jnci/djz094PMC PMC6695312

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Abstract

Background: We previously showed that therapy with anti–checkpoints T-lymphocyte-associated protein 4 (anti–CTLA-4) or antiprogrammed cell death protein 1 (anti–PD-1) agents was more effective for men as compared with women. However, because the sex-dimorphism of the immune system is complex, involving multiple elements of immune responses, it is possible that women could derive larger benefit than men from strategies other than therapy with immune checkpoint inhibitors (ICIs) alone. Here we investigated whether women could derive larger benefit than men from the combination of chemotherapy and anti-PD-1 or anti-PD-L1. Methods: We performed two meta-analyses. The first included all randomized controlled trials (RCTs) testing anti-PD1 and anti–PD-L1 plus chemotherapy vs chemotherapy to assess different efficacy between men and women. The second included all RCTs of first-line systemic treatment in advanced non-small cell lung cancer testing anti–PD-1/PD-L1 given either alone or combined with chemotherapy to assess the different efficacy of these two immunotherapeutic strategies according to patients’ sex. For each RCT included in the two meta-analyses, first, a trial-specific ratio of hazard ratios (HRs) was calculated from the ratio of the reported hazard ratios in men and in women; second, these trial-specific ratios of hazard ratios were combined across trials using a random-effects model to obtain a pooled hazard ratios ratio. A pooled HRs ratio estimate lower than 1 indicates a greater treatment effect in men, and higher than 1 a greater effect in women. Results: Eight RCTs were included in the first meta-analysis. The pooled overall survival hazard ratios (OS-HRs) comparing anti–PD-1/PD-L1 plus chemotherapy vs chemotherapy was 0.76 (95% confidence interval [CI] = 0.66 to 0.87) for men and 0.48 (95% CI = 0.35 to 0.67) for women. The pooled ratio of the overall survival hazard ratios reported in men vs women was 1.56 (95% CI = 1.21 to 2.01), indicating a statistically significant greater effect for women. Six RCTs were included in the second meta-analysis: three tested an anti-PD-1 alone, whereas three RCTs tested anti-PD-1/PD-L1 plus chemotherapy. The pooled overall survival hazard ratios were 0.78 (95% CI = 0.60 to 1.00) in men and 0.97 (95% CI = 0.79 to 1.19) in women for anti–PD-1 alone, compared with 0.76 (95% CI = 0.64 to 0.91) in men and 0.44 (95% CI = 0.25 to 0.76) in women for anti–PD-1/PD-L1 plus chemotherapy. The pooled ratio of overall survival hazard ratios was 0.83 (95% CI = 0.65 to 1.06) for anti–PD-1 alone, indicating a greater effect in men, and 1.70 (95% CI = 1.16 to 2.49) for anti–PD-1/PD-L1 plus chemotherapy, indicating a greater effect in women. Conclusion: Women with advanced lung cancer derived a statistically significantly larger benefit from the addition of chemotherapy to anti–PD-1/PD-L1 as compared with men.

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Additional file 3 of Sex-biased molecular differences in lung adenocarcinoma are ethnic and smoking specific
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Additional file 15 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 4 of Gene regulatory networks reveal sex difference in lung adenocarcinoma
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Additional file 1 of Gene regulatory networks reveal sex difference in lung adenocarcinoma
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Additional file 1 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 5 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 9 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 6 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 5 of Gene regulatory networks reveal sex difference in lung adenocarcinoma
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Additional file 6 of The association of sex-biased ATRX mutation in female gastric cancer patients with enhanced immunotherapy-related anticancer immunity
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Additional file 1 of The association of sex-biased ATRX mutation in female gastric cancer patients with enhanced immunotherapy-related anticancer immunity
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Additional file 12 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 14 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 3 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 13 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 6 of Gene regulatory networks reveal sex difference in lung adenocarcinoma
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Additional file 7 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
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Additional file 1 of Sex-biased molecular differences in lung adenocarcinoma are ethnic and smoking specific
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Additional file 5 of The association of sex-biased ATRX mutation in female gastric cancer patients with enhanced immunotherapy-related anticancer immunity
Ge, Y., Wei, F., Du, G., Fei, G., Li, W., Li, X., Chu, J., & Wei, P. (2021) · Figshare · doi:10.6084/m9.figshare.14177153
Additional file 8 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693865
Additional file 3 of Gene regulatory networks reveal sex difference in lung adenocarcinoma
Saha, E., Guebila, M. B., Fanfani, V., Fischer, J., Shutta, K. H., Mandros, P., DeMeo, D. L., Quackenbush, J. F., & Lopes‐Ramos, C. M. (2024) · Figshare · doi:10.6084/m9.figshare.26758201
Additional file 2 of Sex-related differences in serum biomarker levels predict the activity and efficacy of immune checkpoint inhibitors in advanced melanoma and non-small cell lung cancer patients
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Additional file 3 of The association of sex-biased ATRX mutation in female gastric cancer patients with enhanced immunotherapy-related anticancer immunity
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Additional file 2 of Gene regulatory networks reveal sex difference in lung adenocarcinoma
Saha, E., Guebila, M. B., Fanfani, V., Fischer, J., Shutta, K. H., Mandros, P., DeMeo, D. L., Quackenbush, J. F., & Lopes‐Ramos, C. M. (2024) · Figshare · doi:10.6084/m9.figshare.26758198
Additional file 4 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693853
Additional file 2 of Sex disparities revealed by single-cell and bulk sequencing and their impacts on the efficacy of immunotherapy in esophageal cancer
Yan, H., Huang, J., Li, Y., & Zhao, B. (2024) · Figshare · doi:10.6084/m9.figshare.26693847
Additional file 4 of The association of sex-biased ATRX mutation in female gastric cancer patients with enhanced immunotherapy-related anticancer immunity
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Additional file 7 of Gene regulatory networks reveal sex difference in lung adenocarcinoma
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Authors: Conforti, F., Pala, L., Bagnardi, V., Viale, G., De Pas, T., Pagan, E., Pennacchioli, E., Cocorocchio, E., Ferrucci, P. F., De Marinis, F., Gelber, R. D., & Goldhirsch, A.
Affiliations: See the Notes section for the full list of authors’ affiliations
Corresponding author: Conforti, Fabio
ORCID: Conforti, Fabio
Pala, Laura
Bagnardi, Vincenzo
Viale, Giuseppe
Pagan, Eleonora
Pennacchioli, Elisabetta
Cocorocchio, Emilia
Ferrucci, Pier Francesco
Gelber, Richard D
Venue: JNCI: Journal of the National Cancer Institute
Publisher: Oxford University Press (OUP)
Published: 2019-05-20
Volume: 111
Issue: 8
Pages: 772-781
ISSN: 0027-8874 (ISSN-L)
1460-2105
DOI: 10.1093/jnci/djz094
PMC: PMC6695312
OpenAlex: W2946644285
Cited by: 262
References: 34
Citations by year: 2026: 23 · 2025: 39 · 2024: 56 · 2023: 36 · 2022: 36 · 2021: 39 · 2020: 28 · 2019: 4
FWCI: 2.55
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations: JNCI Journal of the National Cancer Institute (publishedVersion)
PubMed (publishedVersion)
PubMed Central (publishedVersion)
BOA (University of Milano-Bicocca) (submittedVersion)
Topics: Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Health Sciences › Medicine › Oncology › Lung Cancer Research Studies
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Treatments and Mutations
Keywords: sex differences, lung cancer immunotherapy, immune checkpoint inhibitors, anti-PD-1, PD-L1 inhibitors, anti-CTLA-4, non-small cell lung cancer, combination chemotherapy, overall survival, first-line systemic treatment
MeSH terms: Female, Humans, Immunotherapy, Lung Neoplasms, Male, Sex Characteristics, Disease-Free Survival, B7-H1 Antigen, CTLA-4 Antigen, Programmed Cell Death 1 Receptor

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Sex-Based Heterogeneity in Response to Lung Cancer Immunotherapy: A Systematic Review and Meta-Analysis

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