Log in

Significant calendar period deviations in testicular germ cell tumors indicate that postnatal exposures are etiologically relevant

  • Original paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Purpose

The current working model of type II testicular germ cell tumor (TGCT) pathogenesis states that carcinoma in situ arises during embryogenesis, is a necessary precursor, and always progresses to cancer. An implicit condition of this model is that only in utero exposures affect the development of TGCT in later life. In an age-period-cohort analysis, this working model contends an absence of calendar period deviations. We tested this contention using data from the SEER registries of the United States.

Methods

We assessed age-period-cohort models of TGCTs, seminomas, and nonseminomas for the period 1973–2008. Analyses were restricted to whites diagnosed at ages 15–74 years. We tested whether calendar period deviations were significant in TGCT incidence trends adjusted for age deviations and cohort effects.

Results

This analysis included 32,250 TGCTs (18,475 seminomas and 13,775 nonseminomas). Seminoma incidence trends have increased with an average annual percentage change in log-linear rates (net drift) of 1.25 %, relative to just 0.14 % for nonseminoma. In more recent time periods, TGCT incidence trends have plateaued and then undergone a slight decrease. Calendar period deviations were highly statistically significant in models of TGCT (p = 1.24−9) and seminoma (p = 3.99−14), after adjustment for age deviations and cohort effects; results for nonseminoma (p = 0.02) indicated that the effects of calendar period were much more muted.

Conclusion

Calendar period deviations play a significant role in incidence trends of TGCT, which indicates that postnatal exposures are etiologically relevant.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. McGlynn KA, Cook MB (2009) Etiologic factors in testicular germ-cell tumors. Future Oncol 5(9):1389–1402. doi:10.2217/fon.09.116

    Article  PubMed  Google Scholar 

  2. Skakkebaek NE, Berthelsen JG, Muller J (1982) Carcinoma-in situ of the undescended testis. Urol Clin North Am 9(3):377–385

    PubMed  CAS  Google Scholar 

  3. Sonne SB, Almstrup K, Dalgaard M, Juncker AS, Edsgard D, Ruban L, Harrison NJ, Schwager C, Abdollahi A, Huber PE, Brunak S, Gjerdrum LM, Moore HD, Andrews PW, Skakkebaek NE, Rajpert-De Meyts E, Leffers H (2009) Analysis of gene expression profiles of microdissected cell populations indicates that testicular carcinoma in situ is an arrested gonocyte. Cancer Res 69(12):5241–5250. doi:10.1158/0008-5472.CAN-08-4554

    Article  PubMed  CAS  Google Scholar 

  4. Oosterhuis JW, Kersemaekers AM, Jacobsen GK, Timmer A, Steyerberg EW, Molier M, Van Weeren PC, Stoop H, Looijenga LH (2003) Morphology of testicular parenchyma adjacent to germ cell tumours. An interim report. APMIS 111(1):32–40 (discussion 41-32)

    Article  PubMed  CAS  Google Scholar 

  5. von der Maase H, Rorth M, Walbom-Jorgensen S, Sorensen BL, Christophersen IS, Hald T, Jacobsen GK, Berthelsen JG, Skakkebaek NE (1986) Carcinoma in situ of contralateral testis in patients with testicular germ cell cancer: study of 27 cases in 500 patients. Br Med J (Clin Res Ed) 293(6559):1398–1401

    Article  CAS  Google Scholar 

  6. Skakkebaek NE (1978) Carcinoma in situ of the testis: frequency and relationship to invasive germ cell tumours in infertile men. Histopathology 2(3):157–170

    Article  PubMed  CAS  Google Scholar 

  7. Giwercman A, Skakkebaek NE (1993) Carcinoma in situ of the testis: biology, screening and management. Eur Urol 23(Suppl 2):19–21

    PubMed  Google Scholar 

  8. Aalen OO, Tretli S (1999) Analyzing incidence of testis cancer by means of a frailty model. Cancer Causes Control 10(4):285–292

    Article  PubMed  CAS  Google Scholar 

  9. Bray F, Richiardi L, Ekbom A, Pukkala E, Cuninkova M, Moller H (2006) Trends in testicular cancer incidence and mortality in 22 European countries: continuing increases in incidence and declines in mortality. Int J Cancer 118(12):3099–3111

    Article  PubMed  CAS  Google Scholar 

  10. Moller H (1989) Decreased testicular cancer risk in men born in wartime. J Natl Cancer Inst 81(21):1668–1669

    Article  PubMed  CAS  Google Scholar 

  11. McGlynn KA, Devesa SS, Sigurdson AJ, Brown LM, Tsao L, Tarone RE (2003) Trends in the incidence of testicular germ cell tumors in the United States. Cancer 97(1):63–70

    Article  PubMed  Google Scholar 

  12. Baade P, Carriere P, Fritschi L (2008) Trends in testicular germ cell cancer incidence in Australia. Cancer Causes Control 19(10):1043–1049. doi:10.1007/s10552-008-9168-z

    Article  PubMed  Google Scholar 

  13. Bray F, Richiardi L, Ekbom A, Forman D, Pukkala E, Cuninkova M, Moller H (2006) Do testicular seminoma and nonseminoma share the same etiology? Evidence from an age-period-cohort analysis of incidence trends in eight European countries. Cancer Epidemiol Biomarkers Prev 15(4):652–658

    Article  PubMed  Google Scholar 

  14. Liu S, Wen SW, Mao Y, Mery L, Rouleau J (1999) Birth cohort effects underlying the increasing testicular cancer incidence in Canada. Can J Public Health 90(3):176–180

    PubMed  CAS  Google Scholar 

  15. Richiardi L, Bellocco R, Adami HO, Torrang A, Barlow L, Hakulinen T, Rahu M, Stengrevics A, Storm H, Tretli S, Kurtinaitis J, Tyczynski JE, Akre O (2004) Testicular cancer incidence in eight northern European countries: secular and recent trends. Cancer Epidemiol Biomarkers Prev 13(12):2157–2166

    PubMed  Google Scholar 

  16. Liu S, Semenciw R, Waters C, Wen SW, Mery LS, Mao Y (2000) Clues to the aetiological heterogeneity of testicular seminomas and non-seminomas: time trends and age-period-cohort effects. Int J Epidemiol 29(5):826–831

    Article  PubMed  CAS  Google Scholar 

  17. Zheng T, Holford TR, Ma Z, Ward BA, Flannery J, Boyle P (1996) Continuing increase in incidence of germ-cell testis cancer in young adults: experience from Connecticut, USA, 1935–1992. Int J Cancer 65(6):723–729. doi:10.1002/(SICI)1097-0215(19960315)65:6<723:AID-IJC2>3.0.CO;2-0

    Article  PubMed  CAS  Google Scholar 

  18. Moller H (2001) Trends in incidence of testicular cancer and prostate cancer in Denmark. Hum Reprod 16(5):1007–1011

    Article  PubMed  CAS  Google Scholar 

  19. Sincic N, Kulis T, Znaor A, Bray F (2012) Time trends in testicular cancer in Croatia 1983–2007: rapid increases in incidence, no declines in mortality. Cancer Epidemiol 36(1):11–15. doi:10.1016/j.canep.2011.09.010

    Article  PubMed  Google Scholar 

  20. Rosenberg PS, Anderson WF (2010) Proportional hazards models and age-period-cohort analysis of cancer rates. Stat Med 29(11):1228–1238. doi:10.1002/sim.3865

    PubMed  Google Scholar 

  21. Anderson WF, Camargo MC, Fraumeni JF Jr, Correa P, Rosenberg PS, Rabkin CS (2010) Age-specific trends in incidence of noncardia gastric cancer in US adults. JAMA 303(17):1723–1728. doi:10.1001/jama.2010.496

    Article  PubMed  CAS  Google Scholar 

  22. Anderson WF, Jatoi I, Tse J, Rosenberg PS (2010) Male breast cancer: a population-based comparison with female breast cancer. J Clin Oncol 28(2):232–239. doi:10.1200/JCO.2009.23.8162

    Article  PubMed  Google Scholar 

  23. Grimley PM, Matsuno RK, Rosenberg PS, Henson DE, Schwartz AM, Anderson WF (2009) Qualitative age interactions between low-grade and high-grade serous ovarian carcinomas. Cancer Epidemiol Biomarkers Prev 18(8):2256–2261. doi:10.1158/1055-9965.EPI-09-0240

    Article  PubMed  Google Scholar 

  24. Fritz AG (2000) International classification of diseases for oncology: ICD-O, 3rd edn. World Health Organization, Geneva

    Google Scholar 

  25. World Health Organization (2004) Pathology and genetics of tumours of the urinary system and male genital organs. IARC Press, Lyon, Oxford University Press [distributor], Oxford

  26. Waheeb R, Hofmann MC (2011) Human spermatogonial stem cells: a possible origin for spermatocytic seminoma. Int J Androl 34(4 Pt 2):e296–e305. doi:10.1111/j.1365-2605.2011.01199.x (discussion e305)

    Article  PubMed  CAS  Google Scholar 

  27. Holford TR (1983) The estimation of age, period and cohort effects for vital rates. Biometrics 39(2):311–324

    Article  PubMed  CAS  Google Scholar 

  28. Clayton D, Schifflers E (1987) Models for temporal variation in cancer rates II: Age-period-cohort models. Stat Med 6(4):469–481

    Article  PubMed  CAS  Google Scholar 

  29. Robertson C, Gandini S, Boyle P (1999) Age-period-cohort models: a comparative study of available methodologies. J Clin Epidemiol 52(6):569–583

    Article  PubMed  CAS  Google Scholar 

  30. Holford TR (1991) Understanding the effects of age, period, and cohort on incidence and mortality rates. Annu Rev Public Health 12:425–457. doi:10.1146/annurev.pu.12.050191.002233

    Article  PubMed  CAS  Google Scholar 

  31. Rosenberg PS, Anderson WF (2011) Age-period-cohort models in cancer surveillance research: ready for prime time? Cancer Epidemiol Biomark Prev 20(7):1263–1268. doi:10.1158/1055-9965.epi-11-0421

    Article  Google Scholar 

  32. Lerro CC, McGlynn KA, Cook MB (2010) A systematic review and meta-analysis of the relationship between body size and testicular cancer. Br J Cancer 103(9):1467–1474

    Article  PubMed  CAS  Google Scholar 

  33. McGlynn KA, Cook MB (2009) The epidemiology of testicular cancer. In: Cooney KA, Foulkes WD (eds) Male reproductive cancers: epidemiology, pathology and genetics, vol Cancer Genetics series. Springer Publications, New York

    Google Scholar 

  34. Daling JR, Doody DR, Sun X, Trabert BL, Weiss NS, Chen C, Biggs ML, Starr JR, Dey SK, Schwartz SM (2009) Association of marijuana use and the incidence of testicular germ cell tumors. Cancer 115(6):1215–1223. doi:10.1002/cncr.24159

    Article  PubMed  Google Scholar 

  35. Trabert B, Sigurdson AJ, Sweeney AM, Strom SS, McGlynn KA (2011) Marijuana use and testicular germ cell tumors. Cancer 117(4):848–853. doi:10.1002/cncr.25499

    Article  PubMed  Google Scholar 

  36. Pettersson A, Richiardi L, Nordenskjold A, Kaijser M, Akre O (2007) Age at surgery for undescended testis and risk of testicular cancer. N Engl J Med 356(18):1835–1841

    Article  PubMed  CAS  Google Scholar 

  37. Wanderas EH, Tretli S, Fossa SD (1995) Trends in incidence of testicular cancer in Norway 1955–1992. Eur J Cancer 31A(12):2044–2048

    Article  PubMed  CAS  Google Scholar 

  38. Moger TA, Aalen OO, Halvorsen TO, Storm HH, Tretli S (2004) Frailty modelling of testicular cancer incidence using Scandinavian data. Biostatistics 5(1):1–14. doi:10.1093/biostatistics/5.1.1

    Article  PubMed  Google Scholar 

  39. Zippin C, Lum D, Hankey BF (1995) Completeness of hospital cancer case reporting from the SEER Program of the National Cancer Institute. Cancer 76(11):2343–2350

    Article  PubMed  CAS  Google Scholar 

  40. Nathan H, Pawlik TM (2008) Limitations of claims and registry data in surgical oncology research. Ann Surg Oncol 15(2):415–423. doi:10.1245/s10434-007-9658-3

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The study was supported by Intramural Program of the National Cancer Institute, National Institutes of Health, Department of Health and Human Services.

Conflict of interest

There are no financial disclosures from any of the authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael B. Cook.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPT 576 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Speaks, C., McGlynn, K.A. & Cook, M.B. Significant calendar period deviations in testicular germ cell tumors indicate that postnatal exposures are etiologically relevant. Cancer Causes Control 23, 1593–1598 (2012). https://doi.org/10.1007/s10552-012-0036-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-012-0036-5

Keywords

Navigation