Annual Report to the Nation on the Status of Cancer, 1975-2011, Featuring Incidence of Breast Cancer Subtypes by Race/Ethnicity, Poverty, and State

Background: The American Cancer Society (ACS), Centers for Disease Control and Prevention (CDC), National Cancer Institute (NCI), and North American Association of Central Cancer Registries (NAACCR) collaborate annually to produce updated, national cancer statistics. This Annual Report includes a focus on breast cancer incidence by subtype using new, national-level data. Methods: Population-based cancer trends and breast cancer incidence by molecular subtype were calculated. Breast cancer subtypes were classified using tumor biomarkers for hormone receptor (HR) and human growth factor-neu receptor (HER2) expression. Results: Overall cancer incidence decreased for men by 1.8% annually from 2007 to 2011. Rates for women were stable from 1998 to 2011. Within these trends there was racial/ethnic variation, and some sites have increasing rates. Among children, incidence rates continued to increase by 0.8% per year over the past decade while, like adults, mortality declined. Overall mortality has been declining for both men and women since the early 1990’s and for children since the 1970’s. HR+/HER2- breast cancers, the subtype with the best prognosis, were the most common for all races/ethnicities with highest rates among non-Hispanic white women, local stage cases, and low poverty areas (92.7, 63.51, and 98.69 per 100000 non-Hispanic white women, respectively). HR+/HER2- breast cancer incidence rates were strongly, positively correlated with mammography use, particularly for non-Hispanic white women (Pearson 0.57, two-sided P < .001). Triple-negative breast cancers, the subtype with the worst prognosis, were highest among non-Hispanic black women (27.2 per 100000 non-Hispanic black women), which is reflected in high rates in southeastern states. Conclusions: Progress continues in reducing the burden of cancer in the United States. There are unique racial/ethnic-specific incidence patterns for breast cancer subtypes; likely because of both biologic and social risk factors, including variation in mammography use. Breast cancer subtype analysis confirms the capacity of cancer registries to adjust national collection standards to produce clinically relevant data based on evolving medical knowledge.

[1]  R. Tiwari,et al.  (www.interscience.wiley.com) DOI: 10.1002/sim.3733 Estimating average annual per cent change in trend analysis , 2022 .

[2]  W. Anderson,et al.  Breast cancer heterogeneity: a mixture of at least two main types? , 2006, Journal of the National Cancer Institute.

[3]  N. Howlader,et al.  Use of imputed population-based cancer registry data as a method of accounting for missing information: application to estrogen receptor status for breast cancer. , 2012, American journal of epidemiology.

[4]  A. Kurian,et al.  Age-specific incidence of breast cancer subtypes: understanding the black-white crossover. , 2012, Journal of the National Cancer Institute.

[5]  J. Knowelden,et al.  Cancer Epidemiology and Prevention , 1976, British Journal of Cancer.

[6]  C. Muir,et al.  International Classification of Diseases for Oncology , 1990 .

[7]  C. P. Oliver,et al.  Possible relationship between menopause and age at onset of breast cancer , 1950, Cancer.

[8]  Pragna Patel,et al.  Recent trends in cutaneous melanoma incidence and death rates in the United States, 1992-2006. , 2011, Journal of the American Academy of Dermatology.

[9]  Kathleen A Cronin,et al.  US incidence of breast cancer subtypes defined by joint hormone receptor and HER2 status. , 2014, Journal of the National Cancer Institute.

[10]  Benjamin J. Raphael,et al.  Multiplatform Analysis of 12 Cancer Types Reveals Molecular Classification within and across Tissues of Origin , 2014, Cell.

[11]  Anthony Rhodes,et al.  American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer (unabridged version). , 2010, Archives of pathology & laboratory medicine.

[12]  L. Shulman.  The Decrease in Breast-Cancer Incidence in 2003 in the United States , 2008 .

[13]  E. Feuer,et al.  Permutation tests for joinpoint regression with applications to cancer rates. , 2000, Statistics in medicine.

[14]  Y. Liao,et al.  Misclassification of Survey Responses and Black-White Disparity in Mammography Use, Behavioral Risk Factor Surveillance System, 1995-2006 , 2011, Preventing chronic disease.

[15]  Jarvis T. Chen,et al.  Geocoding and monitoring of US socioeconomic inequalities in mortality and cancer incidence: does the choice of area-based measure and geographic level matter?: the Public Health Disparities Geocoding Project. , 2002, American journal of epidemiology.

[16]  John Van Hoewyk,et al.  A multivariate technique for multiply imputing missing values using a sequence of regression models , 2001 .

[17]  Daniel S. Miller,et al.  The annual report to the nation on the status of cancer, 1973–1997, with a special section on colorectal cancer , 2000, Cancer.

[18]  Guidelines for Using Confidence Intervals for Public Health Assessment , 2002 .

[19]  K. Ebeling,et al.  [Breast cancer--epidemiology and prevention]. , 1991, Zeitschrift fur arztliche Fortbildung.

[20]  E. Feuer,et al.  SEER Cancer Statistics Review, 1975-2003 , 2006 .

[21]  A. Jemal,et al.  Annual Report to the Nation on the status of cancer, 1975‐2010, featuring prevalence of comorbidity and impact on survival among persons with lung, colorectal, breast, or prostate cancer , 2014, Cancer.

[22]  I. Ellis,et al.  Pathological prognostic factors in breast cancer. , 1999, Critical reviews in oncology/hematology.

[23]  A. Jemal,et al.  Annual report to the nation on the status of cancer, 1975‐2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates , 2010, Cancer.

[24]  Kevin A. Henry,et al.  Associations of Census-Tract Poverty with Subsite-Specific Colorectal Cancer Incidence Rates and Stage of Disease at Diagnosis in the United States , 2014, Journal of cancer epidemiology.

[25]  R. Schwab,et al.  Reproductive risk factors and breast cancer subtypes: a review of the literature , 2014, Breast Cancer Research and Treatment.

[26]  C. Klabunde,et al.  Challenges in Meeting Healthy People 2020 Objectives for Cancer-Related Preventive Services, National Health Interview Survey, 2008 and 2010 , 2014, Preventing chronic disease.

[27]  H. Adami,et al.  Overdiagnosis of Invasive Breast Cancer Due to Mammography Screening: Results From the Norwegian Screening Program , 2012, Annals of Internal Medicine.

[28]  C. Perou,et al.  Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. , 2006, JAMA.

[29]  Charles Wiggins,et al.  Annual report to the nation on the status of cancer, 1975-2004, featuring cancer in American Indians and Alaska Natives. , 2007, Cancer.

[30]  Daniel S. Miller,et al.  Annual report to the nation on the status of cancer, 1973-1996, with a special section on lung cancer and tobacco smoking. , 1999, Journal of the National Cancer Institute.

[31]  K. Lunetta,et al.  Parity, lactation, and breast cancer subtypes in African American women: results from the AMBER Consortium. , 2014, Journal of the National Cancer Institute.

[32]  J. Martin,et al.  Births: preliminary data for 2012. , 2013, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[33]  Hyune-Ju Kim,et al.  Kim H-J, Fay MP, Feuer EJ, Midthune DN, ‘ Permutation tests for joinpoint regression with applications to cancer rates’. Statistics in Medicine 2000 19:335–351 , 2001 .

[34]  Eric J Feuer,et al.  The decrease in breast-cancer incidence in 2003 in the United States. , 2007, The New England journal of medicine.

[35]  Philip S Rosenberg,et al.  Incidence of breast cancer in the United States: current and future trends. , 2011, Journal of the National Cancer Institute.

[36]  A. Jemal,et al.  Annual report to the nation on the status of cancer, 1975–2001, with a special feature regarding survival , 2004, Cancer.

[37]  K. Flegal,et al.  Prevalence and trends in obesity among US adults, 1999-2008. , 2010, JAMA.

[38]  Daniel S. Miller,et al.  Cancer incidence and mortality, 1973‐1995 , 1998 .

[39]  N. Howlader,et al.  The impact of underreported Veterans Affairs data on national cancer statistics: analysis using population-based SEER registries. , 2009, Journal of the National Cancer Institute.

[40]  F. Pompei,et al.  Peak and decline in cancer incidence, mortality, and prevalence at old ages , 2012, Cancer.

[41]  Anthony Rhodes,et al.  American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. , 2010, Archives of pathology & laboratory medicine.

[42]  C. Perou,et al.  The Triple Negative Paradox: Primary Tumor Chemosensitivity of Breast Cancer Subtypes , 2007, Clinical Cancer Research.

[43]  Jarvis T. Chen,et al.  Choosing area based socioeconomic measures to monitor social inequalities in low birth weight and childhood lead poisoning: The Public Health Disparities Geocoding Project (US) , 2003, Journal of epidemiology and community health.

[44]  C. Perou,et al.  How many etiological subtypes of breast cancer: two, three, four, or more? , 2014, Journal of the National Cancer Institute.

[45]  David J Lee,et al.  Cancer Incidence in First Generation U.S. Hispanics: Cubans, Mexicans, Puerto Ricans, and New Latinos , 2009, Cancer Epidemiology, Biomarkers & Prevention.

[46]  I. Ellis,et al.  Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. , 2002, Histopathology.

[47]  V. Moyer,et al.  Screening for Prostate Cancer: U.S. Preventive Services Task Force Recommendation Statement , 2012, Annals of Internal Medicine.

[48]  Carolyn A. Liebler,et al.  A practical approach to using Multiple-Race response data: A bridging method for publicuse microdata , 2008, Demography.

[49]  C. Perou,et al.  Human epidermal growth factor receptor-2 and estrogen receptor expression, a demonstration project using the residual tissue respository of the Surveillance, Epidemiology, and End Results (SEER) program , 2008, Breast Cancer Research and Treatment.

[50]  Ruth Etzioni,et al.  A reality check for overdiagnosis estimates associated with breast cancer screening. , 2014, Journal of the National Cancer Institute.

[51]  D. Joseph,et al.  Breast cancer screening among adult women--Behavioral Risk Factor Surveillance System, United States, 2010. , 2012, MMWR supplements.

[52]  Jiaquan Xu,et al.  Deaths: preliminary data for 2011. , 2012 .

[53]  P. Wingo,et al.  Cancer incidence and mortality, 1973-1995: a report card for the U.S. , 1998, Cancer.

[54]  K. Dodd,et al.  Population-based Estimate of the Prevalence of HER-2 Positive Breast Cancer Tumors for Early Stage Patients in the US , 2010, Cancer investigation.

[55]  Deborah Schrag,et al.  Annual report to the nation on the status of cancer, 1975-2002, featuring population-based trends in cancer treatment. , 2005, Journal of the National Cancer Institute.

[56]  X. Shu,et al.  Associations of hormone-related factors with breast cancer risk according to hormone receptor status among white and African American women. , 2014, Clinical breast cancer.

[57]  A. Nobel,et al.  Concordance among Gene-Expression – Based Predictors for Breast Cancer , 2011 .

[58]  A. Ananthakrishnan,et al.  Epidemiology of primary and secondary liver cancers. , 2006, Seminars in interventional radiology.

[59]  P. Prorok,et al.  Lead time and overdiagnosis. , 2014, Journal of the National Cancer Institute.

[60]  Steven Woloshin,et al.  When do changes in cancer survival mean progress? The insight from population incidence and mortality. , 2014, Journal of the National Cancer Institute. Monographs.

[61]  E. John,et al.  Heterogeneity of breast cancer subtypes and survival among Hispanic women with invasive breast cancer in California , 2014, Breast Cancer Research and Treatment.

[62]  Robert N. Anderson,et al.  Annual Report to the Nation on the Status of Cancer, 1975–2009, Featuring the Burden and Trends in Human Papillomavirus (HPV)–Associated Cancers and HPV Vaccination Coverage Levels , 2013, Journal of the National Cancer Institute.

[63]  Russell V. Lenth,et al.  Statistical Analysis With Missing Data (2nd ed.) (Book) , 2004 .

[64]  L. Tanoue,et al.  The National Comprehensive Cancer Network , 1998, Cancer.

[65]  Kevin A. Henry,et al.  The Relationship Between Area Poverty Rate and Site-Specific Cancer Incidence in the United States , 2014, Cancer.

[66]  F. Frasca,et al.  Worldwide Increasing Incidence of Thyroid Cancer: Update on Epidemiology and Risk Factors , 2013, Journal of cancer epidemiology.

[67]  P. Morris,et al.  Biological subtypes of breast cancer: current concepts and implications for recurrence patterns. , 2013, The quarterly journal of nuclear medicine and molecular imaging : official publication of the Italian Association of Nuclear Medicine (AIMN) [and] the International Association of Radiopharmacology (IAR), [and] Section of the Society of....

[68]  H. Iwase,et al.  [Breast cancer]. , 2006, Nihon rinsho. Japanese journal of clinical medicine.

[69]  Xianglin L. Du,et al.  Impact of enhanced detection on the increase in thyroid cancer incidence in the United States: review of incidence trends by socioeconomic status within the surveillance, epidemiology, and end results registry, 1980-2008. , 2013, Thyroid : official journal of the American Thyroid Association.

[70]  Xiao-Cheng Wu,et al.  Annual Report to the Nation on the Status of Cancer, 1975–2005, Featuring Trends in Lung Cancer, Tobacco Use, and Tobacco Control , 2008, Journal of the National Cancer Institute.

[71]  F. Boscoe.  Subdividing the age group of 85 years and older to improve US disease reporting. , 2008, American journal of public health.

[72]  A. Gill,et al.  Increasing incidence of thyroid cancer is due to increased pathologic detection. , 2008, Surgery.

[73]  Ahmedin Jemal,et al.  Annual Report to the Nation on the status of cancer, 1975‐2008, featuring cancers associated with excess weight and lack of sufficient physical activity , 2012, Cancer.

[74]  H. Margolis,et al.  The past incidence of hepatitis C virus infection: Implications for the future burden of chronic liver disease in the United States , 2000, Hepatology.

[75]  Dl Hoyert,et al.  National Vital Statistics Reports NCHS.pdf , 2012 .

[76]  P. Rosenberg,et al.  Tracking and evaluating molecular tumor markers with cancer registry data: HER2 and breast cancer. , 2014, Journal of the National Cancer Institute.

[77]  Ram C Tiwari,et al.  Efficient interval estimation for age-adjusted cancer rates , 2006, Statistical methods in medical research.

[78]  Michael J Thun,et al.  Recent trends in breast cancer incidence rates by age and tumor characteristics among U.S. women , 2007, Breast Cancer Research.

[79]  F. de Waard,et al.  The bimodal age distribution of patients with mammary carcinoma. Evidence for the existence of 2 types of human breast cancer , 1964, Cancer.

[80]  Racial and ethnic differences in breastfeeding initiation and duration, by state - National Immunization Survey, United States, 2004-2008. , 2010, MMWR. Morbidity and mortality weekly report.

[81]  Recinda Sherman,et al.  Why an alternative algorithm for identification of Hispanic subgroups is useful. , 2009, Journal of registry management.

[82]  E. Feuer,et al.  Impact of reporting delay and reporting error on cancer incidence rates and trends. , 2002, Journal of the National Cancer Institute.

[83]  Ahmedin Jemal,et al.  Annual Report to the Nation on the status of cancer, 1973–1999, featuring implications of age and aging on U.S. cancer burden , 2002, Cancer.

[84]  D. Rubin,et al.  Statistical Analysis with Missing Data. , 1989 .

[85]  D. Henson,et al.  Re: Age-specific incidence of breast cancer subtypes: understanding the Black-White crossover. , 2013, Journal of the National Cancer Institute.

[86]  H M Rosenberg,et al.  Age standardization of death rates: implementation of the year 2000 standard. , 1998, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[87]  Margo J. Anderson,et al.  The Census , 1921, The Hospital.

[88]  E. Winer,et al.  Clinicopathologic features, patterns of recurrence, and survival among women with triple‐negative breast cancer in the National Comprehensive Cancer Network , 2012, Cancer.

[89]  H M Rosenberg,et al.  Annual report to the nation on the status of cancer (1973 through 1998), featuring cancers with recent increasing trends. , 2001, Journal of the National Cancer Institute.

[90]  Robert N. Anderson,et al.  Annual Report to the Nation on the Status of Cancer, 1975–2007, Featuring Tumors of the Brain and Other Nervous System , 2011, Journal of the National Cancer Institute.

[91]  T. Naab,et al.  Basal cell-like (triple-negative) breast cancer, a predictor of distant metastasis in African American women. , 2008, American journal of surgery.

[92]  A. Jemal,et al.  Annual report to the nation on the status of cancer, 1975-2000, featuring the uses of surveillance data for cancer prevention and control. , 2003, Journal of the National Cancer Institute.

[93]  P. Trott,et al.  International Classification of Diseases for Oncology , 1977 .

[94]  A. Kurian,et al.  Occurrence of breast cancer subtypes in adolescent and young adult women , 2012, Breast Cancer Research.

[95]  Xiaocheng Wu,et al.  Annual report to the nation on the status of cancer, 1975–2003, featuring cancer among U.S. Hispanic/Latino populations , 2006, Cancer.

[96]  A. Jemal,et al.  Breast Cancer Incidence Rates in U.S. Women Are No Longer Declining , 2011, Cancer Epidemiology, Biomarkers & Prevention.

[97]  David K. Espey,et al.  Methods for improving cancer surveillance data in American Indian and Alaska Native populations , 2008, Cancer.

[98]  Ahmedin Jemal,et al.  Association of race/ethnicity, socioeconomic status, and breast cancer subtypes in the National Cancer Data Base (2010–2011) , 2014, Breast Cancer Research and Treatment.

[99]  Nicole A. Lazar,et al.  Statistical Analysis With Missing Data , 2003, Technometrics.

[100]  E. Feuer,et al.  Bias Associated With Self-Report of Prior Screening Mammography , 2009, Cancer Epidemiology Biomarkers & Prevention.

[101]  L. Newman,et al.  Higher population‐based incidence rates of triple‐negative breast cancer among young African‐American women , 2011, Cancer.

[102]  A. Kurian,et al.  Lifetime risks of specific breast cancer subtypes among women in four racial/ethnic groups , 2010, Breast Cancer Research.

[103]  Ali H. Mokdad,et al.  Behavioral risk factor surveillance system. , 1989, Iowa medicine : journal of the Iowa Medical Society.

[104]  Victor R. Preedy,et al.  Behavioral Risk Factor Surveillance System , 2010 .