Differences in cancer survival by sex: a population-based study using cancer registry data

Abstract

Purpose

Few large-scale studies have investigated sex differences in cancer survival and little is known about their temporal and age-related patterns.

Methods

We used cancer registry data for first primary cancers diagnosed between 1982 and 2015 in Victoria, Australia. Cases were followed until the end of 2015 through linkage to death registries. Differences in survival were assessed for 25 cancers using the Pohar-Perme estimator of net survival and the excess mortality rate ratio (EMRR) adjusting for age and year of diagnosis.

Results

Five-year net survival for all cancers combined was lower for men (47.1%; 95% CI 46.9–47.4) than women (52.0%; 95% CI 51.7–52.3); EMRR 1.13 (95% CI 1.12–1.14; p < 0.001). A survival disadvantage for men was observed for 11 cancers: head and neck, esophagus, colorectum, pancreas, lung, bone, melanoma, mesothelioma, kidney, thyroid, and non-Hodgkin lymphoma. In contrast, women had lower survival from cancers of the bladder, renal pelvis, and ureter. For the majority of cancers with survival differences, the EMRR decreased with increasing age at diagnosis; for colorectal, esophageal, and kidney cancer, the EMRR increased with time since diagnosis.

Conclusion

Identifying the underlying reasons behind sex differences in cancer survival is necessary to address inequalities, which may improve outcomes for men and women.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Change history

  • 11 October 2018

    In the original publication of the article, the concluding paragraph of the Discussion section was inadvertently missed and is provided below.

References

  1. 1.

    Pardue ML (2001) Exploring the biological contributions to human health: does sex matter? J Women’s Health Gend Based Med 10(5):433–439

    Article  Google Scholar 

  2. 2.

    Legato MJ, Johnson PA, Manson JE (2016) Consideration of sex differences in medicine to improve health care and patient outcomes. JAMA 316(18):1865–1866. https://doi.org/10.1001/jama.2016.13995

    Article  PubMed  Google Scholar 

  3. 3.

    Dorak MT, Karpuzoglu E (2012) Gender differences in cancer susceptibility: an inadequately addressed issue. Front Genet 3:268. https://doi.org/10.3389/fgene.2012.00268

    Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Kinoshita FL, Ito Y, Morishima T, Miyashiro I, Nakayama T (2017) Sex differences in lung cancer survival: long-term trends using population-based cancer registry data in Osaka, Japan. Jpn J Clin Oncol 47(9):863–869. https://doi.org/10.1093/jjco/hyx094

    Article  PubMed  Google Scholar 

  5. 5.

    Sagerup CM, Småstuen M, Johannesen TB, Helland Å, Brustugun OT (2011) Sex-specific trends in lung cancer incidence and survival: a population study of 40,118 cases. Thorax 66(4):301–307

    Article  Google Scholar 

  6. 6.

    Ulas A, Tokluoglu S, Kos M, Silay K, Akinci S, Oksuzoglu B, Alkis N (2015) Lung cancer in women, a different disease: survival differences by sex in Turkey. Asian Pac J Cancer Prev 16(2):815–822

    Article  Google Scholar 

  7. 7.

    Salmerón D, Chirlaque MD, Isabel Izarzugaza M, Sánchez MJ, Marcos-Gragera R, Ardanaz E, Galceran J, Mateos A, Navarro C (2012) Lung cancer prognosis in Spain: the role of histology, age and sex. Respir Med 106:1301–1308. https://doi.org/10.1016/j.rmed.2012.06.006

    Article  PubMed  Google Scholar 

  8. 8.

    Wisnivesky JP, Halm EA (2007) Sex differences in lung cancer survival: do tumors behave differently in elderly women? J Clin Oncol 25(13):1705–1712

    Article  Google Scholar 

  9. 9.

    Kotake K, Asano M, Ozawa H, Kobayashi H, Sugihara K (2016) Gender differences in colorectal cancer survival in Japan. Int J Clin Oncol 21(1):194–203. https://doi.org/10.1007/s10147-015-0868-6

    Article  PubMed  Google Scholar 

  10. 10.

    Majek O, Gondos A, Jansen L, Emrich K, Holleczek B, Katalinic A, Nennecke A, Eberle A, Brenner H (2013) Sex differences in colorectal cancer survival: population-based analysis of 164,996 colorectal cancer patients in Germany. PLoS ONE 8(7):e68077–e68077. https://doi.org/10.1371/journal.pone.0068077

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Hendifar A, Yang D, Lenz F, Lurje G, Pohl A, Lenz C, Ning Y, Zhang W, Lenz H-J (2009) Gender disparities in metastatic colorectal cancer survival. Clin Cancer Res 15(20):6391–6397. https://doi.org/10.1158/1078-0432.ccr-09-0877

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Joosse A, Collette S, Suciu S, Nijsten T, Lejeune F, Kleeberg UR, Coebergh JWW, Eggermont AM, de Vries E (2012) Superior outcome of women with stage I/II cutaneous melanoma: pooled analysis of four European Organisation for Research and Treatment of Cancer phase III trials. J Clin Oncol 30(18):2240–2247

    Article  Google Scholar 

  13. 13.

    de Vries E, Nijsten TEC, Visser O, Bastiaannet E, van Hattem S, Janssen-Heijnen ML, Coebergh JWW (2008) Superior survival of females among 10,538 Dutch melanoma patients is independent of Breslow thickness, histologic type and tumor site. AnnOncol 19(3):583–589

    Google Scholar 

  14. 14.

    Scoggins CR, Ross MI, Reintgen DS, Noyes RD, Goydos JS, Beitsch PD, Urist MM, Ariyan S, Sussman JJ, Edwards MJ (2006) Gender-related differences in outcome for melanoma patients. Ann Surg 243(5):693

    Article  Google Scholar 

  15. 15.

    Patel MI, Bang A, Gillett D, Cheluvappa R, Smith DP (2015) Poor survival of females with bladder cancer is limited to those aged 70 years or over: a population-wide linkage study, New South Wales, Australia. Cancer Med 4:1145–1152. https://doi.org/10.1002/cam4.452

    Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Tracey E, Watt H, Currow D, Young J, Armstrong B (2014) Investigation of poorer bladder cancer survival in women in NSW, Australia: a data linkage study. BJU Int 113(3):437–448

    Article  Google Scholar 

  17. 17.

    Mungan NA, Aben KK, Schoenberg MP, Visser O, Coebergh JW, Witjes JA, Kiemeney LA (2000) Gender differences in stage-adjusted bladder cancer survival. Urology 55(6):876–880

    CAS  Article  Google Scholar 

  18. 18.

    Waldhoer T, Berger I, Haidinger G, Zielonke N, Madersbacher S (2015) Sex Differences of ≥ pT1 Bladder Cancer Survival in Austria: A descriptive, long-term, nation-wide analysis based on 27,773 Patients. Urol Int 94(4):383–389

    Article  Google Scholar 

  19. 19.

    Radkiewicz C, Johansson ALV, Dickman PW, Lambe M, Edgren G (2017) Sex differences in cancer risk and survival: A Swedish cohort study. Eur J Cancer 84:130–140. https://doi.org/10.1016/j.ejca.2017.07.013

    Article  PubMed  Google Scholar 

  20. 20.

    Ellison LF (2016) Differences in cancer survival in Canada by sex. Health Rep 27(4):19

    PubMed  Google Scholar 

  21. 21.

    Innos K, Padrik P, Valvere V, Aareleid T (2015) Sex differences in cancer survival in Estonia: a population-based study. BMC Cancer 15:72–72. https://doi.org/10.1186/s12885-015-1080-9

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Kyu-Won J, Sohee P, Aesun S, Chang-Mo O, Hyun-Joo K, Jae Kwan J, Young-Joo W (2012) Do female cancer patients display better survival rates compared with males? Analysis of the Korean National Registry Data, 2005–2009. PLoS ONE 7(12):1–6. https://doi.org/10.1371/journal.pone.0052457

    CAS  Article  Google Scholar 

  23. 23.

    Oberaigner W, Siebert U (2011) Do women with cancer have better survival as compared to men after adjusting for staging distribution? Eur J Pub Health 21(3):387–391

    Article  Google Scholar 

  24. 24.

    Cook MB, McGlynn KA, Devesa SS, Freedman ND, Anderson WF (2011) Sex disparities in cancer mortality and survival. Cancer Epidemiol Biomarkers Prev 20(8):1629–1637

    Article  Google Scholar 

  25. 25.

    Micheli A, Ciampichini R, Oberaigner W, Ciccolallo L, de Vries E, Izarzugaza I, Zambon P, Gatta G, De Angelis R (2009) The advantage of women in cancer survival: an analysis of EUROCARE-4 data. Eur J Cancer 45(6):1017–1027. https://doi.org/10.1016/j.ejca.2008.11.008

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Micheli A, Mariotto A, Giorgi Rossi A, Gatta G, Muti P (1998) The prognostic role of gender in survival of adult cancer patients. EUROCARE Working Group. Eur J Cancer 34(14 Spec No):2271–2278

    CAS  Article  Google Scholar 

  27. 27.

    Ellison L, Gibbons L (2001) Five-year relative survival from prostate, breast, colorectal and lung cancer. Health Rep 13(1):23–34

    CAS  PubMed  Google Scholar 

  28. 28.

    Australian Consortium for Classification Development. International Statistical Classification of Diseases and Related Health Problems, Tenth Revision, Australian Modification (ICD-10-AM/ACHI/ACS) Independent Hospital Pricing Authority, Darlinghurst, NSW

  29. 29.

    Harris NL, Jaffe ES, Diebold J, Flandrin G, Muller-Hermelink HK, Vardiman J, Lister TA, Bloomfield CD (1999) World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: report of the Clinical Advisory Committee meeting—Airlie House, Virginia, November 1997. J Clin Oncol 17(12):3835–3849

    CAS  Article  Google Scholar 

  30. 30.

    Australian Blood Cancer Registry (2008) Report of the third annual stakeholder meeting, Stamford Plaza Sydney Airport, October 2007. Sydney: ABCR

  31. 31.

    Egevad L, Heanue M, Berney D, Fleming K, Ferlay J (2007) Histological groups. In: Curado MP, Edwards B, Shin HR, Storm H, Ferlay J, Heanue M, Byle P (eds) Cancer incidence in five continents. IARC Scientific Publications, Lyon pp 61–66

    Google Scholar 

  32. 32.

    Perme MP, Stare J, Estève J (2012) On estimation in relative survival. Biometrics 68(1):113–120. https://doi.org/10.1111/j.1541-0420.2011.01640.x

    Article  PubMed  Google Scholar 

  33. 33.

    Coviello E, Dickman PW, Seppå K, Pokhrel A (2015) Estimating net survival using a life-table approach. The Stata Journal 15:173–185

    Google Scholar 

  34. 34.

    Ederer F, Heise H (1959) Instructions to IBM 650 programmers in processing survival computations. Methodol Note. https://doi.org/10.1371/journal.pone.0070680

    Article  Google Scholar 

  35. 35.

    Dickman PW, Coviello E (2015) Estimating and modeling relative survival. Stat J 15(1):186–215

    Google Scholar 

  36. 36.

    Brenner H, Hakulinen T (2007) Patients with previous cancer should not be excluded in international comparative cancer survival studies. Int J Cancer 121(10):2274–2278

    CAS  Article  Google Scholar 

  37. 37.

    Blakely T, Soeberg M, Carter K, Costilla R, Atkinson J, Sarfati D (2012) Bias in relative survival methods when using incorrect life-tables: lung and bladder cancer by smoking status and ethnicity in New Zealand. Int J Cancer 131(6):E974–E982. https://doi.org/10.1002/ijc.27531

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    eDorak MT, Ebru e (2012) Gender differences in cancer susceptibility: an inadequately addressed issue. Front Genet. https://doi.org/10.3389/fgene.2012.00268/full

    Article  Google Scholar 

  39. 39.

    Klein SL, Flanagan KL (2016) Sex differences in immune responses. Nat Rev Immunol 16(10):626. https://doi.org/10.1038/nri.2016.90

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Yingying W, Nick F, Irwin N, Kate H (2014) 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 9(7):e101562. https://doi.org/10.1371/journal.pone.0101562

    CAS  Article  Google Scholar 

  41. 41.

    Zaitsu M, Toyokawa S, Tonooka A, Nakamura F, Takeuchi T, Homma Y, Kobayashi Y (2015) Sex differences in bladder cancer pathology and survival: analysis of a population-based cancer registry. Cancer Med 4(3):363. https://doi.org/10.1002/cam4.379

    Article  PubMed  Google Scholar 

  42. 42.

    Tracey E, Roder D, Luke C, Bishop J (2009) Bladder cancer survivals in New South Wales, Australia: why do women have poorer survival than men? BJU Int 104(4):498–504. https://doi.org/10.1111/j.1464-410X.2009.08527.x

    Article  PubMed  Google Scholar 

  43. 43.

    Lucca I, Klatte T, Fajkovic H, de Martino M, Shariat SF (2015) Gender differences in incidence and outcomes of urothelial and kidney cancer. Nat Rev Urol 12(10):585. https://doi.org/10.1038/nrurol.2015.232

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Marks P, Soave A, Shariat SF, Fajkovic H, Fisch M, Rink M (2016) Female with bladder cancer: what and why is there a difference? Trans Androl Urol 5(5):668–682

    Article  Google Scholar 

  45. 45.

    Lyratzopoulos G, Abel GA, McPhail S, Neal RD, Rubin GP (2013) Gender inequalities in the promptness of diagnosis of bladder and renal cancer after symptomatic presentation: evidence from secondary analysis of an English primary care audit survey. BMJ Open 3(6):1

    Article  Google Scholar 

  46. 46.

    Henning A, Wehrberger M, Madersbacher S, Pycha A, Martini T, Comploj E, Jeschke K, Tripolt C, Rauchenwald M (2013) Do differences in clinical symptoms and referral patterns contribute to the gender gap in bladder cancer? BJU Int 112(1):68–73. https://doi.org/10.1111/j.1464-410X.2012.11661.x

    Article  PubMed  Google Scholar 

  47. 47.

    Burge F, Kockelbergh R (2016) Closing the gender gap: can we improve bladder cancer survival in women? A systematic review of diagnosis, treatment and outcomes. Urol Int 97(4):373–379. https://doi.org/10.1159/000449256

    Article  PubMed  Google Scholar 

  48. 48.

    Shahabi S, He S, Kopf M, Mariani M, Petrini J, Scambia G, Ferlini C (2013) Free testosterone drives cancer aggressiveness: evidence from US population studies. PLoS ONE 8(4):e61955

    CAS  Article  Google Scholar 

  49. 49.

    Vaccarella S, Franceschi S, Bray F, Wild CP, Plummer M, Dal Maso L (2016) Worldwide thyroid-cancer epidemic? The increasing impact of overdiagnosis. N Engl J Med 375(7):614–617

    Article  Google Scholar 

  50. 50.

    Dal Maso L, Tavilla A, Pacini F, Serraino D, van Dijk B, Chirlaque M, Capocaccia R, Larrañaga N, Colonna M, Agius D (2017) Survival of 86,690 patients with thyroid cancer: a population-based study in 29 European countries from EUROCARE-5. Eur J Cancer 77:140–152

    CAS  Article  Google Scholar 

  51. 51.

    Pandeya N, Wilson LF, Bain CJ, Martin KL, Webb PM, Whiteman DC (2015) Cancers in Australia in 2010 attributable to tobacco smoke. Aust N Z J Public Health 39(5):464–470

    Article  Google Scholar 

Download references

Acknowledgments

Nina Afshar is the recipient of an Australian Government Research Training Program Scholarship.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Nina Afshar.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethics approval

Ethical approval to conduct the analyses of these data was granted by the Cancer Council Victoria Human Research Ethics Committee. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

For this type of study formal consent is not required.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Afshar, N., English, D.R., Thursfield, V. et al. Differences in cancer survival by sex: a population-based study using cancer registry data. Cancer Causes Control 29, 1059–1069 (2018). https://doi.org/10.1007/s10552-018-1079-z

Download citation

Keywords

  • Sex differences
  • Inequalities
  • Cancer registries
  • Survival analysis
  • Cancer survival
  • Excess mortality