Advertisement

Sex differences in cancer risk and survival: A Swedish cohort study

Published:August 10, 2017DOI:https://doi.org/10.1016/j.ejca.2017.07.013

      Highlights

      • Male sex is associated with increased risk for most cancers sites.
      • The male excess risk ratio has decreased, but remains significant over time.
      • The fraction of cancer explained by factors related to male sex is considerable.
      • Men experience poorer survival in most cancer sites.

      Abstract

      Aim

      The aim of this study is to firmly delineate temporal and age trends regarding sex discrepancies in cancer risk and survival as well as quantifying the potential gain achieved by eliminating this inequality.

      Methods

      We performed a population-based cohort study using data on all adult incident cancer cases (n = 872,397) recorded in the Swedish Cancer Register in 1970–2014. To assess the associations between sex and cancer risk and sex and survival, male-to-female incidence rate ratios (IRRs) and excess mortality ratios (EMRs) adjusted for age and year of diagnosis were estimated using Poisson regression.

      Results

      Men were at increased risk for 34 of 39 and had poorer prognosis for 27 of 39 cancers. Women were at increased risk for 5 of 39 and had significantly poorer survival for 2 of 39 cancers. IRRs among male predominant sites ranged from 1.05; 95% confidence interval (CI), 1.03–-1.1 (lung adenocarcinoma) to 8.0; 95% CI, 7.5–8.5 (larynx). EMRs among sites with male survival disadvantage ranged from 1.1; 95% CI, 1.03–1.1 (colon) to 2.1; 95% CI, 1.5–-2.8 (well-differentiated thyroid).

      Conclusion

      Male sex is associated with increased risk and poorer survival for most cancer sites. Identifying and eliminating factors driving the observed sex differences may reduce the global cancer burden.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to European Journal of Cancer
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Legato M.J.
        • Johnson P.A.
        • Manson J.E.
        Consideration of sex differences in medicine to improve health care and patient outcomes.
        JAMA. 2016; 316: 1865-1866
        • Cook M.B.
        • Dawsey S.M.
        • Freedman N.D.
        • Inskip P.D.
        • Wichner S.M.
        • Quraishi S.M.
        • et al.
        Sex disparities in cancer incidence by period and age.
        Cancer Epidemiol Biomarkers Prev. 2009; 18: 1174-1182
        • Edgren G.
        • Liang L.
        • Adami H.O.
        • Chang E.T.
        Enigmatic sex disparities in cancer incidence.
        Eur J Epidemiol. 2012; 27: 187-196
        • Scelo G.
        • Li P.
        • Chanudet E.
        • Muller D.C.
        Variability of sex disparities in cancer incidence over 30 years: the striking case of kidney cancer.
        Eur Urol Focus. 2017; https://doi.org/10.1016/j.euf.2017.01.006
        • Cook M.B.
        • McGlynn K.A.
        • Devesa S.S.
        • Freedman N.D.
        • Anderson W.F.
        Sex disparities in cancer mortality and survival.
        Cancer Epidemiol Biomarkers Prev. 2011; 20: 1629-1637
        • Innos K.
        • Padrik P.
        • Valvere V.
        • Aareleid T.
        Sex differences in cancer survival in Estonia: a population-based study.
        BMC Cancer. 2015; 15: 72
        • Jung K.W.
        • Park S.
        • Shin A.
        • Oh C.M.
        • Kong H.J.
        • Jun J.K.
        • et al.
        Do female cancer patients display better survival rates compared with males? Analysis of the Korean National Registry data, 2005–2009.
        PLoS One. 2012; 7: e52457
        • Lortet-Tieulent J.
        • Renteria E.
        • Sharp L.
        • Weiderpass E.
        • Comber H.
        • Baas P.
        • et al.
        Convergence of decreasing male and increasing female incidence rates in major tobacco-related cancers in Europe in 1988–2010.
        Eur J Cancer. 2015; 51: 1144-1163
        • McCartney G.
        • Mahmood L.
        • Leyland A.H.
        • Batty G.D.
        • Hunt K.
        Contribution of smoking-related and alcohol-related deaths to the gender gap in mortality: evidence from 30 European countries.
        Tob Control. 2011; 20: 166-168
        • Forsberg L.A.
        • Rasi C.
        • Malmqvist N.
        • Davies H.
        • Pasupulati S.
        • Pakalapati G.
        • et al.
        Mosaic loss of chromosome Y in peripheral blood is associated with shorter survival and higher risk of cancer.
        Nat Genet. 2014; 46: 624-628
        • Dunford A.
        • Weinstock D.M.
        • Savova V.
        • Schumacher S.E.
        • Cleary J.P.
        • Yoda A.
        • et al.
        Tumor-suppressor genes that escape from X-inactivation contribute to cancer sex bias.
        Nat Genet. 2017; 49: 10-16
        • Micheli A.
        • Ciampichini R.
        • Oberaigner W.
        • Ciccolallo L.
        • de Vries E.
        • Izarzugaza I.
        • et al.
        The advantage of women in cancer survival: an analysis of EUROCARE-4 data.
        Eur J Cancer. 2009; 45: 1017-1027
        • Joosse A.
        • Collette S.
        • Suciu S.
        • Nijsten T.
        • Patel P.M.
        • Keilholz U.
        • et al.
        Sex is an independent prognostic indicator for survival and relapse/progression-free survival in metastasized stage III to IV melanoma: a pooled analysis of five European organisation for research and treatment of cancer randomized controlled trials.
        J Clin Oncol. 2013; 31: 2337-2346
        • Austad S.N.
        Why women live longer than men: sex differences in longevity.
        Gend Med. 2006; 3: 79-92
        • Barlow L.
        • Westergren K.
        • Holmberg L.
        • Talback M.
        The completeness of the Swedish Cancer Register: a sample survey for year 1998.
        Acta Oncol. 2009; 48: 27-33
        • Ludvigsson J.F.
        • Almqvist C.
        • Bonamy A.K.
        • Ljung R.
        • Michaelsson K.
        • Neovius M.
        • et al.
        Registers of the Swedish total population and their use in medical research.
        Eur J Epidemiol. 2016; 31: 125-136
        • Organization WH
        Histological classification of Neoplasms.
        The Committee on Tumour Nomenclature and Statistics of the International Union Against Cancer, Paris1956
        • Organization WH
        Manual of the international statistical classification of diseases, injuries, and causes of death: based on the recommendations of the seventh revision Conference, 1955, and adopted by the ninth World Health Assembly under the WHO Nomenclature Regulations.
        World Health Organization, Geneva1957
        • Moriyama I.M.
        The eighth revision of the International Classification of Diseases.
        Am J Public Health Nations Health. 1966; 56: 1277-1280
        • Muir C.S.
        • Van Holten V.
        • Percy C.L.
        International Classification of Diseases for Oncology.
        World Health Organization, Geneva1990
        • Daly L.E.
        Confidence limits made easy: interval estimation using a substitution method.
        Am J Epidemiol. 1998; 147: 783-790
        • Dickman P.W.
        • Adami H.O.
        Interpreting trends in cancer patient survival.
        J Intern Med. 2006; 260: 103-117
        • Dickman P.W.
        • Coviello E.
        Estimating and modelling relative survival.
        Stata J. 2015; 15: 186-215
        • Corazziari I.
        • Quinn M.
        • Capocaccia R.
        Standard cancer patient population for age standardising survival ratios.
        Eur J Cancer. 2004; 40: 2307-2316
        • Lambert P.C.
        • Royston P.
        Further development of flexible parametric models for survival analysis.
        Stata J. 2009; 9: 265-290
        • Dickman P.W.
        • Sloggett A.
        • Hills M.
        • Hakulinen T.
        Regression models for relative survival.
        Stat Med. 2004; 23: 51-64
        • Planchard D.
        • Loriot Y.
        • Goubar A.
        • Commo F.
        • Soria J.C.
        Differential expression of biomarkers in men and women.
        Semin Oncol. 2009; 36: 553-565
        • Shahabi S.
        • He S.
        • Kopf M.
        • Mariani M.
        • Petrini J.
        • Scambia G.
        • et al.
        Free testosterone drives cancer aggressiveness: evidence from US population studies.
        PLoS One. 2013; 8: e61955
        • Adami H.O.
        • Holmberg L.
        • Persson I.
        Female sex hormones and cancer survival.
        Lancet. 1994; 344: 760-761
        • Dorak M.T.
        • Karpuzoglu E.
        Gender differences in cancer susceptibility: an inadequately addressed issue.
        Front Genet. 2012; 3: 268
        • Tomasetti C.
        • Vogelstein B.
        Variation in cancer risk among tissues can be explained by the number of stem cell divisions.
        Science. 2015; 347: 78-81
        • de Martel C.
        • Franceschi S.
        Infections and cancer: established associations and new hypotheses.
        Crit Rev Oncol Hematol. 2009; 70: 183-194
        • Vahter M.
        • Akesson A.
        • Liden C.
        • Ceccatelli S.
        • Berglund M.
        Gender differences in the disposition and toxicity of metals.
        Environ Res. 2007; 104: 85-95
        • Higdon J.V.
        • Frei B.
        Is there a gender difference in the effect of antioxidants on cancer risk?.
        Br J Nutr. 2005; 94: 139-140
        • Whiteman D.C.
        • Wilson L.F.
        The fractions of cancer attributable to modifiable factors: a global review.
        Cancer Epidemiol. 2016; 44: 203-221
      1. Living conditions, Report no 114: use of alcohol and tobacco: Statistics Sweden. 2007 (Report No.: 114)
        • Janssen-Heijnen M.L.
        • Houterman S.
        • Lemmens V.E.
        • Louwman M.W.
        • Maas H.A.
        • Coebergh J.W.
        Prognostic impact of increasing age and co-morbidity in cancer patients: a population-based approach.
        Crit Rev Oncol Hematol. 2005; 55: 231-240
        • Noren A.
        • Eriksson H.G.
        • Olsson L.I.
        Selection for surgery and survival of synchronous colorectal liver metastases; a nationwide study.
        Eur J Cancer. 2016; 53: 105-114
        • Smolina K.
        • Ball L.
        • Humphries K.H.
        • Khan N.
        • Morgan S.G.
        Sex disparities in post-acute myocardial infarction pharmacologic treatment initiation and adherence: problem for young women.
        Circ Cardiovasc Qual Outcomes. 2015; 8: 586-592
        • Wang Y.
        • Freemantle N.
        • Nazareth I.
        • Hunt K.
        Gender differences in survival and the use of primary care prior to diagnosis of three cancers: an analysis of routinely collected UK general practice data.
        PLoS One. 2014; 9: e101562