Skip to main content
Log in

Population-based risk assessment of second primary cancers following a first head and neck cancer: patterns of association and difficulties of its analysis

  • Research Article
  • Published:
Clinical and Translational Oncology Aims and scope Submit manuscript

Abstract

Purpose

The diagnosis of a second primary cancer (SPC) is a major concern in the follow-up of survivors of a primary head and neck cancer (HNC), but the anatomic subsites in the head and neck area are close, making it difficult to distinguish a SPC of a recurrence and therefore register it correctly.

Methods

We performed a retrospective cohort study using data from two population-based cancer registries in Catalonia, Spain: the Tarragona Cancer Registry and the Girona Cancer Registry. All patients diagnosed with HNC during the period 1994–2013 were registered and followed-up to collect cases of SPC. We analysed the standardized incidence ratio (SIR) and the excess absolute risk (EAR) to determine the risk of second malignancies following a prior HNC.

Results

923 SPC were found in a cohort of 5646 patients diagnosed of a first head and neck cancer. Men had an increased risk of a SPC with a SIR of 2.22 and an EAR of 216.76. Women also had an increased risk with a SIR of 2.02 and an EAR of 95.70. We show the risk for different tumour sites and discuss the difficulties of the analysis.

Conclusion

The risks of a SPC following a prior HNC in Tarragona and Girona are similar to those previously found in other similar cohorts. It would appear to be advisable to make a revision of the international rules of classification of multiple tumours, grouping the sites of head and neck area with new aetiological criteria to better determine and interpret the risks of SPC obtained in these studies.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Schou G, Storm HH, Jensen OM. Second cancer following cancers of the buccal cavity and pharynx in Denmark, 1943–80. Natl Cancer Inst Monogr. 1985;68:253–76.

    CAS  PubMed  Google Scholar 

  2. Wood ME, Vogel V, Ng A, Foxhall L, Goodwin P, Travis LB. Second malignant neoplasms: assessment and strategies for risk reduction. J Clin Oncol. 2012;30(30):3734–45.

    Article  Google Scholar 

  3. Slaughter M, Danely P, Harry W, et al. Field cancerization in oral stratified squamous epithelium clinical implications of multicentric origin. Cancer. 1953;6:963–8.

    Article  CAS  Google Scholar 

  4. Mohan M, Jagannathan N. Oral field cancerization: an update on current concepts. Oncology Rev. 2014;8:244–50.

    Google Scholar 

  5. Ha PK, Califano JA. The molecular biology of mucosal field cancerization of the head and neck. Crit Rev Oral Biol Med. 2003;14:363–9.

    Article  Google Scholar 

  6. Martel M, Alemany L, Taberna M, Mena M, Tous S, Bagué S, et al. The role of HPV on the risk of second primary neoplasia in patients with oropharyngeal carcinoma. Oral Oncol. 2017;64:37–433.

    Article  Google Scholar 

  7. Engeland A, Bjorge T, Haldorsen T, Tretli S. Use of multiple primary cancers to indicate associations between smoking and cancer incidence: an analysis of 500000 cancer cases diagnosed in Norway during 1953–93. Int J Cancer. 1997;70:401–4017.

    Article  CAS  Google Scholar 

  8. Shiels MS, Gibson T, Sampson J, Albanes D, Andreotti G, Freeman LB, Berrington de Gonzalez A, Caporaso N, Curtis RE, Elena J, Freedman ND, Robien K, Black A, Morton LM. Cigarette smoking prior to first cancer and risk of second smoking-associated cancers among survivors of bladder, kidney, head and neck, and stage I lung cancers. J Clin Oncol. 2014;32(35):3989–95.

    Article  Google Scholar 

  9. Berg JW. Morphologic classification of human cancer. In: Schottenfeld D & Fraumeni JF. Jr. Cancer epidemiology and prevention, 1982, Chapter 5, pp 74–89. Saunders Company

  10. (2005) Working Group of the International Association of Cancer Registries. International rules for multiple primary cancers (ICD-0 third edition). Eur J Cancer Prev. 14(4):307–308.

  11. (1992) International statistical classification of diseases and related health problems, tenth revision. World Health Organization, Geneva.

  12. Brown LM, McCarron P, Freedman M. Chapter 3: New malignancies following cancer of the buccal cavity and pharynx. In: Curtis RE, Freedman DM, Ron E, Ries LAG, Hacker DG, Edwards BK, Tucker MA, Fraumeni JF Jr. (eds). New malignancies among Cancer survivors: SEER Cancer Registries, 1973–2000. National Cancer Institute, NIH Publ. No. 05–5302. Bethesda, MD, 2006

  13. Castellsagué X, Alemany L, Quer M, Halec G, Quirós B, Tous S, et al. HPV involvement in head and neck cancers: comprehensive assessment of biomarkers in 3680 patients. J Natl Cancer Inst. 2016;108(6):djv403.

    Article  Google Scholar 

  14. Gillison ML, Koch WM, Capone RB, Spafford M, Westra WH, Wu L, et al. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst. 2000;92(9):709–20.

    Article  CAS  Google Scholar 

  15. Lubin JH, Purdue M, Kelsey K, Zhang ZF, Winn D, Wei Q, et al. Total exposure and exposure rate effects for alcohol and smoking and risk of head and neck cancer: a pooled analysis of case-control studies. Am J Epidemiol. 2009;170(8):937–47.

    Article  Google Scholar 

  16. Morris LG, Sikora AG, Hayes RB, Patel SG, Ganly I. Anatomic sites at elevated risk of second primary cancer after an index head and neck cancer. Cancer Causes Control. 2011;22(5):671–9.

    Article  Google Scholar 

  17. Bosetti C, Scelo G, Chuang SC, Tonita JM, Tamaro S, Jonasson JG, Kliewer EV, Hemminki K, Weiderpass E, Pukkala E, Tracey E, Olsen JH, Pompe-Kirn V, Brewster DH, Martos C, Chia KS, Brennan P, Hashibe M, Levi F, La Vecchia C, Boffetta P. High constant incidence rates of second primary cancers of the head and neck: a pooled analysis of 13 cancer registries. Int J Cancer. 2011;129(1):173–9.

    Article  CAS  Google Scholar 

  18. Coca-Palez A, Rodrigo JP, Suárez C, Nixon IJ, Mäkitie A, Sanabria A, et al. The risk of second primary tumours in head and neck cancer: a systematic review. Head Neck. 2020;42(3):456–66.

    Article  Google Scholar 

  19. Chaturvedi AK, Engels EA, Pfeiffer RM, et al. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol. 2011;29:4294–301.

    Article  Google Scholar 

  20. Morris LG, Sikora AG, Patel SG, Hayes RB, Ganly I. Second primary cancers after an index head and neck cancer: subsite-specific trends in the era of human papillomavirus-associated oropharyngeal cancer. J Clin Oncol. 2010;29:739–46.

    Article  Google Scholar 

  21. Neumann F, Jégu J, Mougin C, Prétet JL, Guizard AV, Lapôtre-Ledoux B, Bara S, Bouvier V, Colonna M, Troussard X, Trétarre B, Grosclaude P, Velten M, Woronoff AS. Risk of second primary cancer after a first potentially-human papillomavirus-related cancer: a population-based study. Prev Med. 2016;90:52–8.

    Article  Google Scholar 

  22. Suk R, Mahale P, Sonawane K, Sikora AG, Chhatwal J, Schmeler KM, Sigel K, Cantor SB, Chiao EY, Deshmukh A. Trends in risks for second primary cancers associated with index human papillomavirus-associated cancers. JAMA Network Open. 2018;1(5):e181999.

    Article  Google Scholar 

  23. Jégu J, Colonna M, Daubisse-Marliac L, Trétarre B, Ganry O, Guizard AV, Bara S, Troussard X, Bouvier V, Woronoff AS, Velten M. The effect of patient characteristics on second primary cancer risk in France. BMC Cancer. 2014;14:94–107.

    Article  Google Scholar 

  24. Curtis RE, Freedman DM, Ron E, Ries LAG, Hacker DG, Edwards BK, Tucker MA, Fraumeni JF. New malignancies among cancer survivors: SEER Cancer Registries, 1973–2000. National Cancer Institute, NIH Publ. No 05–5302. Bethesda, MD, 2006

  25. Buzzoni C, Crocetti E. AIRTUM working group. italian cancer figures report 2013: multiple tumours. Epidemiol Prev. 2013;37((4–5) suppl 1):1–152.

    Google Scholar 

  26. Weir HK, Johnson CJ, Ward KC, Coleman MP. The effect of multiple primary rules on cancer incidence rates and trends. Cancer Causes Control. 2016;3:377–90.

    Article  Google Scholar 

  27. Ye Y, Neil AL, Wills KE, Venn AJ. Temporal trends in the risk of developing multiple primary cancers: a systematic review. BMC Cancer. 2016;16(1):849–66.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Katie Linder for reviewing the English grammar of the manuscript.

Funding

This research did not receive any specific grants from public, commercial, or not-for-profit funding agencies.

Author information

Authors and Affiliations

Authors

Contributions

JRC, JGa, JM, AI, JB, MC, RMG and JGu contributed to study design and to the analysis and interpretation of the study results. JRC and JGa wrote the manuscript. MP was responsible for the databases in Girona Cancer Registry (GCR). LL were responsible for the databases in Tarragona Cancer Registry (TCR). AA performed the statistical analysis. JGa and MC are the coordinators of the TCR. RMG and AI are the coordinators of the GCR. All authors corrected and approved the final manuscript.

Corresponding author

Correspondence to J. Rubió-Casadevall.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This study uses anonymous data and complies with all the laws and rules of the National Health System that regulates the activity of population-based cancer registries.

Informed consent

For this type of study formal consent is not required.

Availability of data and material

This study was carried out using anonymized data from the Girona Cancer Registry (GCR) and Tarragona Cancer Registry (TCR) which comply with the legal regulations for data protection and management of clinical data in force in Spain. Both registries belong to and comply with the regulations of the International Association of Cancer Registries (IACR) and the International Agency for Research in Cancer (IARC). No intervention has been performed on human or animal subjects. All procedures have been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 39 kb)

Supplementary file2 (DOCX 28 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rubió-Casadevall, J., Galceran, J., Ameijide, A. et al. Population-based risk assessment of second primary cancers following a first head and neck cancer: patterns of association and difficulties of its analysis. Clin Transl Oncol 23, 788–798 (2021). https://doi.org/10.1007/s12094-020-02470-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12094-020-02470-z

Keywords

Navigation