Abstract
Background
Prior to 1999–2000, breast cancer incidence rates had risen for decades, though more among older than younger women.
Materials and methods
To further explore the impact of advancing age-at-diagnosis upon breast cancer incidence, we used the National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) program (1974–2003).
Results
Over time, we observed age interactions by tumor grade, stage, and race. For example, among women ages <40 years, high-grade lesions were more common than low-grade tumors for all time periods. Among women ages 40+ years, high-grade lesions were more common during early time periods then trend lines crossed, after which low-grade tumors were more common than high-grade lesions. Notably, the transition (crossover point) occurred earlier with advancing age-at-diagnosis.
Conclusion
The reversal (crossing) of incidence rates from high to low-grade tumors among women 40+ years is a qualitative age interaction, probably due to changing age-related risk factor and/or screening patterns, where mammography preferentially detected tumors of low malignant potential among older women. Though once thought to be rare or artifactual, qualitative age interactions suggest breast cancer heterogeneity. Indeed, if real, qualitative age interactions (effect modifications) imply different etiologic pathways for early-onset and late-onset types of breast cancer.
Similar content being viewed by others
References
Ries LAG, Harkins D, Krapcho M, Mariotto A, Miller BA, Feuer EJ et al (2006) SEER Cancer Statistics Review, 1975–2003, National Cancer Institute, based on November 2005 SEER data submission, posted to the SEER web site, 2006
Howe HL, Wu X, Ries LA, Cokkinides V, Ahmed F, Jemal A et al (2006) Annual report to the nation on the status of cancer, 1975–2003, featuring cancer among U.S. Hispanic/Latino populations. Cancer 107(8):1711–1742
Clarke CA, Glaser SL, Uratsu CS, Selby JV, Kushi LH, Herrinton LJ (2006) Recent declines in hormone therapy utilization and breast cancer incidence: clinical and population-based evidence. J Clin Oncol 24(33):e49–e50
Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ (2007) Cancer statistics, 2007 CA Cancer. J Clin 57(1):43–66
Ravdin PM, Cronin KA, Howlader N, Berg CD, Chlebowski RT, Feuer EJ et al (2007) The decrease in breast-cancer incidence in 2003 in the United States. N Engl J Med 356(16):1670–1674
Jemal A, Ward E, Thun MJ (2007) Recent trends in breast cancer incidence rates by age and tumor characteristics among U.S. women. Breast Cancer Res 9(3):R28
Glass AG, Lacey JV Jr, Carreon JD, Hoover RN (2007) Breast cancer incidence, 1980 2006: combined roles of menopausal hormone therapy, screening mammography, and estrogen receptor status. J Natl Cancer Inst 99(15):1152–1161
Anderson WF, Reiner AS, Matsuno RK, Pfeiffer RM (2007) Shifting breast cancer trends in the United States. J Clin Oncol EPub ahead of print
SEER (2006) Surveillance, Epidemiology, and End Results (SEER) Program (http://www.seer.cancer.gov) SEER*Stat Database: Incidence-Connecticut Historical, Aug 1999 Sub (1935–1997), National Cancer Institute, DCCPS, Surveillance Research Program, Cancer Statistics Branch
Fox MS (1979) On the diagnosis and treatment of breast cancer. JAMA 241(5):489–494
Adami H-O (1984) Breast cancer incidence and mortality. Aspects on aetiology, time trends and curability. Acta Chir Scand 519(Suppl):9–14
Holford TR, Cronin KA, Mariotto AB, Feuer EJ (2006) Chapter4: changing patterns in breast cancer incidence trends. J Natl Cancer Inst Monogr 36:19–25
Clemmesen J (1948) Carcinoma of the breast Br J Radiol 21(252):583–590
Lilienfeld AM, Johnson EA (1955) The age distribution in female breast and genital cancers. Cancer 8:875–882
Moolgavkar SH, Lee JA, Hade RD (1978) Comparison of age-specific mortality from breast cancer in males in the United States and Japan. J Natl Cancer Inst 60(6):1223–1225
De Waard F (1979) Premenopausal and postmenopausal breast cancer: one disease or two? J Natl Cancer Inst 63(3):549–552
SEER (2006) Surveillance, Epidemiology, and End Results (SEER) Program (http://www.seer.cancer.gov) SEER*Stat Database: Incidence-SEER 9 Regs Public-use, Nov 2004 sub (1973–2003), National Cancer Institute, DCCPS, Surveillance Research Program, Cancer Statistics Branch, released April 2006, based on November 2005 submission
Berg JW, Hutter RV (1995) Breast cancer Cancer 75(1 Suppl):257–269
SEER (2004) ICD-O-3 Coding materials [cited; Available from: http://seer.cancer.gov/icd-o-3/
Tavassoli FA, Devilee P (eds) (2003) Pathology and genetics of tumours of the breast and female genital organs. IARC Press, Lyon
Devesa SS, Donaldson J, Fears T (1995) Graphical presentation of trends in rates. Am J Epidemiol 141(4):300–304
McCullagh P, Nelder JA (1989) Generalized linear models. Chapman and Hall, New York
Anderson WF, Matsuno RK, Sherman ME, Lissowska J, Gail MH, Brinton LA et al (2007) Estimating age-specific breast cancer risks: a descriptive tool to identify age interactions. Cancer Causes Control 18:439–447
Gail M, Simon R (1985) Testing for qualitative interactions between treatment effects and patient subsets. Biometrics 41(2):361–372
Anderson WF, Chatterjee N, Ershler WB, Brawley OW (2002) Estrogen receptor breast cancer phenotypes in the surveillance, epidemiology, and end results database. Breast Cancer Res Treat 76(1):27–36
Chu KC, Tarone RE, Kessler LG, Ries LAG, Hankey BF, Miller BA et al (1996) Recent trends in U. S. breast cancer incidence, survival, and mortality rates. J Natl Cancer Inst 88(21):1571–1579
Anderson WF, Jatoi I, Devesa SS (2006) Assessing the impact of screening mammography: breast cancer incidence and mortality rates in Connecticut (1943–2002). Breast Cancer Res Treat 99:333–340
Last JM (1995) A dictionary of epidemiology, 3rd edn. Oxford University Press, Oxford
Pike MC, Krailo MD, Henderson BE, Casagrande JT, Hoel DG (1983) ‘Hormonal’ risk factors, ‘breast tissue age’ and the age-incidence of breast cancer. Nature 303(5920):767–770
Colditz GA, Rosner BA (2006) What can be learnt from models of incidence rates? Breast Cancer Res 8(3):208
Thomas DB (1993) Breast cancer in men Epidemiol Rev 15(1):220–231
Anderson WF, Matsuno RK (2006) Breast cancer heterogeneity: a mixture of at least two main types? J Natl Cancer Inst 98(14):948–951
Narod SA, Dube MP (2001) Biologic characteristics of interval and screen-detected breast cancers. J Natl Cancer Inst 93(2):151–152
Swan J, Breen N, Coates RJ, Rimer BK, Lee NC (2003) Progress in cancer screening practices in the United States: results from the 2000 National Health Interview Survey. Cancer 97(6):1528–1540
Anderson WF, Jatoi I, Devesa SS (2005) Distinct breast cancer incidence and prognostic patterns in the NCI’s SEER program: suggesting a possible link between etiology and outcome. Breast Cancer Res Treat 90(2):127–137
Anderson WF, Pfeiffer RM, Dores GM, Sherman ME (2006) Comparison of age frequency distribution patterns for different histopathologic types of breast carcinoma. Cancer Epidemiol Biomarkers Prev 15(10):1899–1905
Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA et al (2000) Molecular portraits of human breast tumours. Nature 406(6797):747–752
Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A et al (2003) Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A 100(14):8418–8423
Burstein HJ (2005) The distinctive nature of HER2-positive breast cancers. N Engl J Med 353(16):1652–1654
Peto R (1982) Statistical aspects of cancer trials. Chapman and Hall, London
Janerich DT, Hoff MB (1982) Evidence for a crossover in breast cancer risk factors. Am J Epidemiol 116(5):737–742
Lubin JH, Burns PE, Blot WJ, Lees AW, May C, Morris LE et al (1982) Risk factors for breast cancer in women in northern Alberta, Canada, as related to age at diagnosis. J Natl Cancer Inst 68(2):211–217
Schedin P (2006) Pregnancy-associated breast cancer and metastasis. Nat Rev Cancer 6(4):281–291
Cleary MP, Maihle NJ (1997) The role of body mass index in the relative risk of developing premenopausal versus postmenopausal breast cancer. Proc Soc Exp Biol Med 216(1):28–43
Colditz GA, Rosner B (2000) Cumulative risk of breast cancer to age 70 years according to risk factor status: data from the Nurses’ health study. Am J Epidemiol 152(10):950–964
Althuis MD, Fergenbaum JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME (2004) Etiology of hormone receptor-defined breast cancer: a systematic review of the literature. Cancer Epidemiol Biomarkers Prev 13(10):1558–1568
Hankey BF, Miller B, Curtis R, Kosary C (1994) Trends in breast cancer in younger women in contrast to older women. J Natl Cancer Inst Monogr 16:7–14
Brinton LA, Benichou J, Gammon MD, Brogan DR, Coates R, Schoenberg JB (1997) Ethnicity and variation in breast cancer incidence. Int J Cancer 73(3):349–355
Hilsenbeck SG, Ravdin PM, de Moor CA, Chamness GC, Osborne CK, Clark GM (1998) Time-dependence of hazard ratios for prognostic factors in primary breast cancer. Breast Cancer Res Treat 52:227–237
Acknowledgments
This research was supported in part by the Intramural Research Program of the NIH/National Cancer Institute.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Anderson, W.F., Chen, B.E., Brinton, L.A. et al. Qualitative age interactions (or effect modification) suggest different cancer pathways for early-onset and late-onset breast cancers. Cancer Causes Control 18, 1187–1198 (2007). https://doi.org/10.1007/s10552-007-9057-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10552-007-9057-x