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      Sex and survival in non-small cell lung cancer: A nationwide cohort study

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          Abstract

          Aim

          To in detail delineate sex differences in non-small cell lung cancer outcome and investigate possible underlying drivers.

          Methods

          We performed a nationwide, population-based cohort study using data on all incident cases of lung squamous cell carcinoma (n = 10,325) and adenocarcinoma (n = 23,465) recorded in the Swedish Lung Cancer Register in 2002–2016. Flexible parametric models were applied to compute adjusted female-to-male hazard ratios (aHRs) and standardized survival proportions over follow-up including age, calendar year, education, marital status, birth country, health care region, performance status, smoking history, comorbidities, and tumor location in the final model.

          Results

          Women presented with better performance status, were younger, and more often never-smokers. Women with adenocarcinoma also had lower comorbidity burden, less advanced stage, and were more often EGFR positive. Men with adenocarcinoma had a consistently poorer lung cancer-specific survival across stage; HR 0.69; 95% CI 0.63–0.76 (stage IA-IIB) to 0.94; 95% CI 0.88–0.99 (stage IIIB-IV), remaining largely unchanged after adjustments; aHR 0.74; 95% CI 0.66–0.82 to 0.84; 95% CI 0.81–0.87. The same pattern was observed in squamous cell carcinoma, except in stage IIIA disease, where we found no sex differences in survival.

          Conclusions

          Men with non-small cell lung cancer have a consistently poorer prognosis, even after careful adjustments for a wide range of prognostic factors. While the pattern was similar in both squamous cell and adenocarcinoma, it was larger and more consistent in the latter.

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          Most cited references30

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          Comorbidity measures for use with administrative data.

          A Elixhauser, C. Steiner, D Harris … (1998)
          This study attempts to develop a comprehensive set of comorbidity measures for use with large administrative inpatient datasets. The study involved clinical and empirical review of comorbidity measures, development of a framework that attempts to segregate comorbidities from other aspects of the patient's condition, development of a comorbidity algorithm, and testing on heterogeneous and homogeneous patient groups. Data were drawn from all adult, nonmaternal inpatients from 438 acute care hospitals in California in 1992 (n = 1,779,167). Outcome measures were those commonly available in administrative data: length of stay, hospital charges, and in-hospital death. A comprehensive set of 30 comorbidity measures was developed. The comorbidities were associated with substantial increases in length of stay, hospital charges, and mortality both for heterogeneous and homogeneous disease groups. Several comorbidities are described that are important predictors of outcomes, yet commonly are not measured. These include mental disorders, drug and alcohol abuse, obesity, coagulopathy, weight loss, and fluid and electrolyte disorders. The comorbidities had independent effects on outcomes and probably should not be simplified as an index because they affect outcomes differently among different patient groups. The present method addresses some of the limitations of previous measures. It is based on a comprehensive approach to identifying comorbidities and separates them from the primary reason for hospitalization, resulting in an expanded set of comorbidities that easily is applied without further refinement to administrative data for a wide range of diseases.
          Article 0 comments Cited 1237 times – based on 0 reviews     Review now
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            The International Association for the Study of Lung Cancer Staging Project: prognostic factors and pathologic TNM stage in surgically managed non-small cell lung cancer.

            Kari Chansky, Jean-Paul Sculier, John Crowley … (2009)
            To assess the impact of cell type, age, and gender in addition to pathologic tumor, node, metastasis (TNM) stage in surgically managed stage I-IIIA non-small cell lung cancer (NSCLC) cases from the international staging database of the International Association for the Study of Lung Cancer. From the 67,725 cases of NSCLC submitted to the staging database, 9137 surgically managed cases were selected for which all the following variables were available: pathologic stage, age, gender, and specific histologic cell type. Performance status and smoking history were examined in subsets. Methods used were Cox proportional hazards regression and recursive partitioning and amalgamation (RPA) analyses. Pathologic TNM stage, age, and gender were all independently prognostic for survival. The bronchioloalveolar carcinoma (BAC) subtype had superior survival over other cell types despite the potential for heterogeneity in this group. Adjusted comparisons revealed a small survival advantage for squamous cell carcinomas over non-BAC adenocarcinoma histology and also over large cell, though the effect appeared to be limited to the male patients. RPA revealed the importance of TNM stage primarily, and age was prognostic within stage groups. Cell type was not found to add prognostic value in the RPA analysis. Prognostic groups were formed based on the RPA output, and the prognostic value of these groupings was validated using the North American Surveillance, Epidemiology, and End Results Registries. Performance status and smoking history were prognostic in the subsets where data were available. Effects of other variable were not influenced by the inclusion of smoking status in regression models. Age and gender are confirmed as important prognostic factors in surgically resected NSCLC. Cell type is less important, although the small population of cases classified as BAC have a survival advantage over other histologies, and there may be a small survival advantage for squamous cell carcinomas over non-BAC adenocarcinomas. Imbalances between stage, gender, and cell type at presentation may lead to a misleading result with respect to cell type in unadjusted analyses. Pathologic TNM category is the most important prognostic factor in this analysis.
            Article 0 comments Cited 143 times – based on 0 reviews     Review now
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              Survival determinants in extensive-stage non-small-cell lung cancer: the Southwest Oncology Group experience.

              M. LeBlanc, Thomas Crowley, Robert B. Livingston … (1991)
              We analyzed the 2,531-patient Southwest Oncology Group extensive-stage non-small-cell lung cancer (ENSCLC) data base from 1974 to 1988 to (1) assess the interactions of host- or tumor-related prognostic factors and therapy using Cox modeling and recursive partitioning and amalgamation (RPA) to determine whether each independently predicts outcome, and (2) use RPA to define prognostic subsets with different survival potentials. Good performance status (PS), female sex, and age greater than or equal to 70 years were significant independent predictors in a Cox model applied to the entire population. In a second Cox model for patients with good PS enrolled on recent studies, hemoglobin level greater than or equal to 11.0 g/dL, normal lactate dehydrogenase (LDH), normal calcium, and a single metastatic site were significant favorable factors. The use of cisplatin was an additional independent predictor of improved outcome in both Cox models after adjustments for year of accrual and all prognostic variables. The favorable effect of cisplatin was observed in each of six RPA-derived subgroups from the entire population. A second RPA of 904 patients from recent trials (nearly all received cisplatin-based therapy) resulted in three distinct prognostic subsets based on PS, age, hemoglobin, and LDH; greater than or equal to 1-year survivals were 27%, 16%, and 6% (P less than .0001). The best survival occurred for patients with a good PS who had a hemoglobin level greater than or equal to 11 g/dL and who were older than 47 years. This analysis suggests that although several factors were independent variables in the Cox models, three important prognostic subgroups were easily defined through RPA. Together with other analyses, our results suggest the need to modify the stage IV category in NSCLC.
              Article 0 comments Cited 101 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Cecilia Radkiewicz:
                ORCID: http://orcid.org/0000-0003-0683-1537
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Paul William Dickman: Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Anna Louise Viktoria Johansson: Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Gunnar Wagenius: Role: ConceptualizationRole: Data curationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Gustaf Edgren: Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Mats Lambe: Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Eric J. Duell: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 27 June 2019
                Publication date Collection: 2019
                Volume: 14
                Issue: 6
                Electronic Location Identifier: e0219206
                Affiliations
                [1 ] Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden
                [2 ] Department of Oncology, Södersjukhuset, Stockholm, Sweden
                [3 ] Cancer Registry of Norway, Oslo, Norway
                [4 ] Cancer Theme, Karolinska University Hospital, Stockholm, Sweden
                [5 ] Department of Medicine Solna, Clinical Epidemiology Division T2, Karolinska Institutet, Stockholm, Sweden
                [6 ] Department of Cardiology, Södersjukhuset, Stockholm, Sweden
                [7 ] Regional Cancer Center Uppsala-Örebro, Uppsala, Sweden
                Catalan Institute of Oncology - Bellvitage Biomedical Research Institute (ICO-IDIBELL), SPAIN
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-0683-1537
                Article
                Publisher ID: PONE-D-19-10489
                DOI: 10.1371/journal.pone.0219206
                PMC ID: 6597110
                PubMed ID: 31247015
                SO-VID: 48bf53d8-e138-4ba1-9065-9787a7bbb783
                Copyright © © 2019 Radkiewicz et al
                License:

                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.

                History
                Date received : 12 April 2019
                Date accepted : 18 June 2019
                Page count
                Figures: 2, Tables: 3, Pages: 14
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100006636, Forskningsrådet om Hälsa, Arbetsliv och Välfärd;
                Award ID: FORTE 2013-0138
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004359, Vetenskapsrådet;
                Award ID: 2017-01954
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004348, Stockholms Läns Landsting;
                Award Recipient :
                This work was supported by grants from FORTE - The Swedish Research Council for Health, Working Life and Welfare (2012-03047 to ML); the Swedish research council (2017-01954 to GE); and Stockholm County Council (clinical research appointment to GE). The funding bodies had no role in the data collection and analysis and was not involved in the interpretation of results, writing, revision, or approval of the manuscript.
                Categories
                Subject: Research Article
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Cancer Detection and Diagnosis
                Subject: Medicine and Health Sciences
                Subject: Oncology
                Subject: Cancer Detection and Diagnosis
                Subject: Medicine and Health Sciences
                Subject: Oncology
                Subject: Cancers and Neoplasms
                Subject: Lung and Intrathoracic Tumors
                Subject: Non-Small Cell Lung Cancer
                Subject: Medicine and Health Sciences
                Subject: Oncology
                Subject: Cancers and Neoplasms
                Subject: Carcinomas
                Subject: Adenocarcinomas
                Subject: Medicine and Health Sciences
                Subject: Oncology
                Subject: Cancers and Neoplasms
                Subject: Carcinomas
                Subject: Adenocarcinomas
                Subject: Adenocarcinoma of the Lung
                Subject: Medicine and Health Sciences
                Subject: Oncology
                Subject: Cancers and Neoplasms
                Subject: Lung and Intrathoracic Tumors
                Subject: Adenocarcinoma of the Lung
                Subject: Medicine and Health Sciences
                Subject: Oncology
                Subject: Cancers and Neoplasms
                Subject: Lung and Intrathoracic Tumors
                Subject: Squamous Cell Lung Carcinoma
                Subject: Medicine and Health Sciences
                Subject: Oncology
                Subject: Cancers and Neoplasms
                Subject: Carcinomas
                Subject: Squamous Cell Carcinomas
                Subject: Squamous Cell Lung Carcinoma
                Subject: Medicine and Health Sciences
                Subject: Oncology
                Subject: Cancers and Neoplasms
                Subject: Lung and Intrathoracic Tumors
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Histology
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Histology
                Subject: Medicine and Health Sciences
                Subject: Oncology
                Subject: Cancers and Neoplasms
                Subject: Carcinomas
                Subject: Squamous Cell Carcinomas
                Custom metadata
                Data Availability The Lung Cancer DataBase Sweden (LcBaSE) is a research database containing detailed clinical and socioeconomic individual-level data from several nationwide registers. Even though LcBaSE is anonymized, single individuals could potentially be identified and their privacy violated. Furthermore, this type of information is labelled sensitive personal data that is confidential and fall under rigorous, legal secrecy restrictions in Sweden. Data cannot be shared publicly without violating the Swedish law. Anyone wishing to access data is prompted to apply for ethical permission through the Swedish Ethical Review Authority (contact details at https://etikprovningsmyndigheten.se), which includes motivating the use of sensitive personal data, specifying the underlying research objective as well as safety aspects concerning data storage and management. Results can only be presented at an aggregated level. Researchers who meet the criteria to access confidential data can in an initial step contact the primary owner of the Lung Cancer Register, the Chief Legal Officer in Region Uppsala in Central Sweden Johan Ahlgren (e-mail: johan.ahlgren@ 123456rccuppsalaorebro.se ).

                ScienceOpen disciplines: Uncategorized
                Data availability:
                ScienceOpen disciplines: Uncategorized

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