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The American Cancer Society, the Centers for Disease Control and Prevention (CDC), the National Cancer Institute, and the North American Association of Central Cancer Registries (NAACCR) collaborate annually to provide updated information on cancer occurrence and trends in the United States. This year’s report highlights brain and other nervous system (ONS) tumors, including nonmalignant brain tumors, which became reportable on a national level in 2004.
Cancer incidence data were obtained from the National Cancer Institute, CDC, and NAACCR, and information on deaths was obtained from the CDC’s National Center for Health Statistics. The annual percentage changes in age-standardized incidence and death rates (2000 US population standard) for all cancers combined and for the top 15 cancers for men and for women were estimated by joinpoint analysis of long-term (1992–2007 for incidence; 1975–2007 for mortality) trends and short-term fixed interval (1998–2007) trends. Analyses of malignant neuroepithelial brain and ONS tumors were based on data from 1980–2007; data on nonmalignant tumors were available for 2004–2007. All statistical tests were two-sided.
Overall cancer incidence rates decreased by approximately 1% per year; the decrease was statistically significant (P < .05) in women, but not in men, because of a recent increase in prostate cancer incidence. The death rates continued to decrease for both sexes. Childhood cancer incidence rates continued to increase, whereas death rates continued to decrease. Lung cancer death rates decreased in women for the first time during 2003–2007, more than a decade after decreasing in men. During 2004–2007, more than 213 500 primary brain and ONS tumors were diagnosed, and 35.8% were malignant. From 1987–2007, the incidence of neuroepithelial malignant brain and ONS tumors decreased by 0.4% per year in men and women combined.
The decrease in cancer incidence and mortality reflects progress in cancer prevention, early detection, and treatment. However, major challenges remain, including increasing incidence rates and continued low survival for some cancers. Malignant and nonmalignant brain tumors demonstrate differing patterns of occurrence by sex, age, and race, and exhibit considerable biologic diversity. Inclusion of nonmalignant brain tumors in cancer registries provides a fuller assessment of disease burden and medical resource needs associated with these unique tumors.
Since our first Report to the Nation, published in 1998, documented the first sustained decrease in cancer death rates since the 1930s (1), the American Cancer Society, the Centers for Disease Control and Prevention (CDC), the National Cancer Institute (NCI), and the North American Association of Central Cancer Registries (NAACCR) have collaborated annually to produce a report on the status of cancer in the United States. Each subsequent year, reports have updated information on trends in incidence and death rates and featured in-depth analyses of selected topics (2–12). The current report provides the latest information on trends for all cancers combined, childhood cancers, and for the top 15 cancers for each of the five major racial and ethnic groups by sex. Furthermore, this article presents a comprehensive assessment of the incidence of malignant and nonmalignant brain tumors in children and adults by race, sex, age group, and tumor histological type. National collection of nonmalignant brain tumors began in 2004 following the passage of Public Law 107-260, the Benign Brain Tumor Cancer Registries Amendment Act. The historical incidence, mortality, and survival by histological type, age, and era of diagnosis for malignant brain and other nervous system (ONS) tumors are presented.
Population-based cancer registries that are NAACCR members and participate in the NCI’s Surveillance, Epidemiology, and End Results (SEER) Program, and/or the CDC’s National Program of Cancer Registries were used to obtain information on newly diagnosed invasive cancers and benign and borderline brain tumors. Incident cases were classified by site and histology according to the International Classification of Diseases for Oncology (ICD-O) edition in use at the time of diagnosis, converted to the Third Edition coding (13) and categorized according to SEER site groups (14).
Incidence data were not available uniformly for every period, geographic area, and racial and ethnic group in the United States (Supplementary Table 1, available online). The longest continuous incidence data were available from the nine original SEER registries (SEER 9) covering about 10% of the US population. Long-term (1975–2007) trends based on data from the SEER 9 registries are included in Supplementary Table 2 (available online). Data providing better coverage of the US population (about 14%) were available from the SEER 13 registries and form the basis of our long-term incidence trend (1992–2007) analysis for all races and ethnicities combined (15). Beginning in 1995, following the advent of the National Program of Cancer Registries, coverage of the US population increased dramatically. Data from NAACCR covering 40 population-based cancer registries were used to assess short-term (1998–2007) trends. Data from 46 NAACCR population-based cancer registries were used to estimate 5-year (2003–2007) average annual age-standardized incidence rates for all races and ethnicities combined and for each of the five major racial and ethnic populations (white, black, Asian and Pacific Islander [API], American Indian/Alaska Native [AI/AN] who reside in counties covered by the Indian Health Service [IHS] Contract Health Service Delivery Area [CHSDA], and Hispanic). The 40 and 46 registries met NAACCR’s data quality criteria for every year included in the analysis; these registries covered 83.6% and 93% of the US population, respectively.
All primary brain and ONS tumors (ICD-O-3 codes C70.0–72.9 and C75.1–75.3, respectively), including malignant, borderline, and benign behaviors diagnosed in 2004–2007 were identified from 46 states in the NAACCR dataset. A neuropathologist reviewed the brain and ONS site and histology combinations and recommended excluding 1771 cases (0.8%) from analysis because of unlikely combinations. Consistent with the SEER site re-code convention, tumors coded to the nasal and nasopharyngeal regions also were excluded.
Data on approximately 76 000 malignant and 137 000 non-malignant brain and ONS tumors were analyzed. Within the brain and ONS, seven major histological groups were used in analyses (16,17). Tumors of neuroepithelial tissue were divided into eight specific histological subgroups (16). Tumors of neuroepithelial tissue coded as nonmalignant by registries, but for which only a malignant behavior code existed in ICD-O-3, were considered malignant. Consistent with previous practice, pilocytic astrocytomas were considered malignant. Malignant and papillary meningioma and meningeal sarcomatosis were categorized as malignant, whereas all other benign and uncertain or atypical meningioma histologies were categorized as nonmalignant, according to the ICD-O-3 behavior codes. Childhood brain and ONS tumors also were grouped using International Classification of Childhood Cancers (ICCC) definitions (18).
Cause of death is based on death certificate information reported to state vital statistics offices and compiled into a national file through the CDC National Center for Health Statistics National Vital Statistics System (19) and categorized according to SEER anatomic site groups (14) to maximize comparability among ICD and ICD-O versions. The underlying causes of death were selected according to the version of the ICD codes and selection rules in use at the time of death (ICD-6 to ICD-10) (20–24). We examined long-term (1975–2007) mortality trends for all races and ethnicities combined. Short-term (1998–2007) trends and 5-year (2003–2007) average annual age-standardized death rates were calculated for all cancer sites combined and for the top 15 cancer sites for men and women in each of the five major racial and ethnic populations. Death rates for the AI/AN population were based on deaths in counties served by IHS CHSDA because estimated rates based on CHSDA counties have been reported to be more accurate for this group (10,25).
County-level population estimates, summed to the state and national level, were used as denominators in calculations of incidence rates (26). The National Center for Health Statistics and the Census Bureau collaborate to provide NCI with bridged single-race annual population estimates, with annual reestimates calculated back to the most recent decennial census to accommodate multiracial data (27). The NCI makes slight modifications to the Hawaii population estimates based on additional local information (26).
For most states, population estimates as of July 1 of each year were used to calculate annual incidence and death rates. For Louisiana, Alabama, Mississippi, and Texas, where residents were displaced by Hurricanes Katrina and Rita, NCI made adjustments to the 2005 incidence data and underlying population data. The national total population estimates are not affected by these adjustments (further details are available at http://seer.cancer.gov/popdata/methods.html).
Age-specific and age-standardized rates were expressed per 100 000 persons (or per 1 000 000 children), based on 2000 US standard population, and generated using SEER*Stat Software, Version 6.6.2 (http://www.seer.cancer.gov/seerstat) (28). Rates were suppressed if the numerator was less than 16 observations, consistent with our previous work (1–12).
Trends in age-standardized cancer incidence and US death rates were analyzed using joinpoint regression, which involves fitting a series of joined straight lines on a logarithmic scale to the trends in the annual age-standardized rates (http://www.srab.cancer.gov/joinpoint). We allowed a maximum of three joinpoints in models for the period 1992–2007 (Table 1), four joinpoints in models for the period 1975–2007 (Table 2 and Supplementary Table 2, available online), and up to two joinpoints for the period 1998–2007 for short-term fixed interval incidence (Table 3) and mortality analyses (Table 4). The joinpoint method is described in detail elsewhere (29). We present the long-term (1975–2007 and 1992–2007) trends in incidence using annual percent changes (APCs; ie, the slope of the line segment) based on observed data and APCs adjusted for reporting delays (which affect mostly recent years). Delay-adjustment is a statistical method to correct for unreported (delayed) or updated cancer cases. Delay-adjusted APCs, used in our description of results, are available only for long-term incidence data (Table 1 and Supplementary Table 2, available online) (30). The average APC (AAPC), a summary measure to compare fixed interval trends by race and ethnicity, is estimated as a geometric weighted average of the joinpoint APC trend analysis, with the weights equal to the lengths of each segment during the prespecified fixed interval (http://srab.cancer.gov/joinpoint/aapc.html) (31). The APC was suppressed if the numerator was less than 10 cancers for any year, consistent with our previous methods (1–12).
In describing long- and short-term trends with estimates of APC and AAPC, the terms “increase” or “decrease” signify that the slope (APC or AAPC) of the trend was statistically significant (P < .05) using a t test (APC) or Z test (AAPC). For non-statistically significant trends, we used terms such as “level,” “stable,” “non-statistically significant increase,” or “non-statistically significant decrease.” All statistical tests were two-sided.
Trend analysis showed that overall cancer incidence rates for all racial and ethnic groups combined decreased by 0.8% per year during the most recent period, 2003–2007 (Table 1); a statistically significant decrease of 0.6% per year was noted in women, whereas a non-statistically significant decrease of 0.8% per year was noted in men that was influenced by a recent (2005–2007) non-statistically significant increase in prostate cancer incidence. When prostate cancer was excluded from the trend analysis, there was a statistically significant decrease in cancer incidence for all sites combined (data not shown). Incidence for prostate and breast cancers, two of the most frequently diagnosed cancers, showed possible changing trends. Cancer of the prostate showed a non-statistically significant annual increase of 3.0% in 2005–2007, after a statistically significant decrease in 2001–2005. The trend analysis of breast cancer in women showed a decrease from 1999 until 2007. However, inspection of the annual breast cancer incidence rates during this period (data not shown) revealed that, after a sharp decrease in rates in 2002–2003, the lower rates subsequently remained stable. The cancer rates among children (0–19 years of age) showed an increase of 0.6% per year for both the most recent 5-year period (2003–2007) and the entire period (1992–2007).
During the period 2003–2007, incidence rates for five of the 15 most common cancers among men demonstrated a statistically significant decrease: lung and bronchus (lung), colon and rectum (colorectal), oral cavity and pharynx (oral), stomach, and malignant brain tumors. Trends in four cancers among men (melanoma of the skin, kidney and renal pelvis [kidney], pancreas, and liver and intrahepatic bile duct [liver]) showed statistically significant increases during the period 2003–2007, whereas trends for prostate, urinary bladder (bladder), and esophageal cancers and leukemia, myeloma, and non-Hodgkin lymphoma did not demonstrate a statistically significant increase or decrease. Among women, statistically significant increasing trends were noted in three of the four cancers that were increasing in men (kidney, pancreas, melanoma of the skin); leukemia and thyroid cancer also increased. Statistically significant decreasing trends for women included cancers of the breast, lung, colon and rectum, corpus uteri (uterus), cervix uteri (cervix), bladder, and oral cavity. No statistically significant trends in non-Hodgkin lymphoma, malignant brain tumors, and cancer of the ovary were observed.
Since the early 1990s, overall cancer death rates have shown a statistically significant decreasing trend among both men and women; whereas for children, cancer death rates have decreased since the mid-1970s (Table 2). Trends in death rates during the most recent 10- and 5-year periods (1998–2007 and 2003–2007) continued to decrease for seven of the top 15 cancer types in both men and women (colon and rectum, brain, stomach, and kidney cancers, and non-Hodgkin lymphoma, leukemia, and myeloma); for cancers of the lung, prostate, and oral cavity in men; and for breast and bladder cancers in women. In contrast, during the corresponding time intervals, death rates from liver cancer and melanoma of the skin in men and those for liver and pancreatic cancers in women continued to exhibit statistically significant increases. Notably, lung cancer death rates in women revealed a statistically significant decrease during the period 2003–2007, following long-term increases during the period 1975–2003, and cervical cancer death rates stabilized after decreasing for many decades. It also is noteworthy that long-term trends in death rates may mask important changes during the shorter term. For example, the 10-year AAPC (1998–2007) for lung cancer in women showed a small non-statistically significant decrease of 0.2% that was composed of a statistically significant increase of 0.3% from 1995 to 2003, followed by a statistically significant decrease of 0.9% from 2003 to 2007 (Table 2).
Black men had the highest cancer incidence rate for 2003–2007 of any racial and ethnic group (Table 3). Except among Hispanics, the top three cancer sites for men in each population group were, in rank order, prostate, lung, and colorectal cancers; among Hispanics, the colorectal cancer rate was slightly higher than the rate of lung cancer. Among women, white women had the highest overall incidence rates. Breast cancer was the most commonly diagnosed cancer among women regardless of race and ethnicity. Lung and colorectal cancers ranked second and third (respectively) among women of all races combined and for white, black, and AI/AN women. However, these rankings were reversed among API and Hispanic women. For all populations, cancer of the uterus ranked fourth. Beyond the top three cancer sites for men and top four for women, cancer rankings varied by race and ethnicity.
Incidence rates for all cancer sites combined decreased between 1998 and 2007 in both men and women in all populations; although the decrease was non-statistically significant among black or AI/AN women (Table 3). Childhood (ages 0–19 years) cancer incidence increased in all populations, although the increase was non-statistically significant for API and AI/AN children. Prostate cancer incidence showed a statistically significant decrease among AI/AN and Hispanic men. Breast cancer incidence rates decreased in all women, but the decrease was of smaller magnitude and non-statistically significant for black and API women. Among men, lung cancer incidence rates decreased for all populations; among women, no statistically significant change was observed in any racial or ethnic group. Colorectal cancer rates decreased among both men and women in all population groups, but the decrease was non-statistically significant for AI/AN women. Cancer of the uterus increased among black, API, and Hispanic women but not among white women. Incidence rates of esophageal cancer increased among white men but decreased among blacks and Hispanics.
Overall cancer death rates from 1998–2007 decreased for all race, ethnic, and sex groups except AI/AN women, among whom the decrease was non-statistically significant (Table 4). However, the largest average annual percentage decrease occurred in black and Hispanic men, approximately 2.5% per year. During the corresponding time interval, overall cancer death rates also showed a statistically significant decrease of 1%–2% per year for children aged 0–19 years in each racial and ethnic group, except in Hispanics and AI/AN, in whom rates were stable. Similarly, death rates in each racial and ethnic group decreased for each of the three major cancers in men and women (lung, colorectal, prostate, or breast), except the trends for prostate and colon cancers among AI/AN men and for lung cancer among women of all racial groups were non-statistically significant. A statistically significant increase in liver cancer death rates was noted among white men and women and black and Hispanic men, whereas the increase in pancreatic cancer death rates was noted only in white men and women.
The distribution of malignant, benign, and borderline brain and ONS tumors during the period 2004–2007 is shown for adults in Table 5 and for children in Table 6. Nonmalignant tumors were about twice as common as malignant tumors among adults (aged ≥20 years). Women had an overall brain tumor incidence rate of 26.55 per 100 000 persons; men had a corresponding rate of 22.37. Tumors of neuroepithelial tissue were the most common histological group of malignant brain tumor, occurring more frequently in men than women. Glioblastoma, which occurred 1.6 times more frequently in men, was the most common subtype of neuroepithelial tumor. The most common type of nonmalignant adult brain tumor was meningioma, which was 2.3 times more common in women than in men, with an incidence rate of 12.42 per 100 000 vs 5.46 per 100 000 persons, respectively. The rate of meningioma in women was by far the highest incidence rate for any type of brain tumor in either sex. In contrast to neuroepithelial tumors, 94.9% of which were malignant, only 2.1% of meningiomas were malignant.
Incidence rates among children aged 0–19 years were much lower than in adults (48.47 per 1 000 000 children vs 24.55 per 100 000 adults), but the tumors were much more likely to be malignant in children: 65.2% vs 33.7% malignant in adults. Boys had only slightly more tumors of neuroepithelial tissue than girls (35.71 in boys vs 32.62 in girls per 1 000 000 children), yet adult men had incidence rates of neuroepithelial tumors 1.4 times higher than women. Tumors of the meninges were more likely to be malignant in children when compared with adults and occurred in boys and girls with similar frequency. Tumors of neuroepithelial tissue were more likely to be malignant in adults, whereas germ cell tumors were more likely to be malignant in children. Tumors of the nerve sheath were rarely malignant, and lymphomas of the brain were relatively rare in both adults and children.
Whites had the highest incidence rates of brain and ONS tumors (19.0 per 100 000 persons), followed by Hispanics (17.8 per 100 000 persons) and blacks (17.7 per 100 000 persons) (Table 7). AI/ANs had lower incidence rates of brain and ONS tumors (15.3 per 100 000 persons), and APIs had the lowest incidence rates (13.5 per 100 000 persons). Glioblastoma was the most common type of malignant brain tumor, with whites having the highest incidence rates, followed by Hispanics, blacks, and AI/ANs; with APIs having roughly one-half the rate of these tumors when compared with whites. The two most common types of nonmalignant brain tumors were higher among blacks compared with whites. Meningioma was the most common brain tumor, with black women having the highest incidence rates overall (9.7 per 100 000 persons), and black men having the highest incidence rates among men. Blacks and Hispanics had the highest incidence rates of tumors of the sellar region; however, acoustic neuromas occurred more than twice as often among whites compared with blacks.
Childhood brain and ONS tumor counts and incidence rates using ICCC-3 definitions are presented in Table 8. This classification system is used widely with childhood brain and ONS tumors but does not allow for comparison with adults. Childhood cancer incidence rates presented in Table 8 may differ from those presented elsewhere in this article because of the different classification systems used to produce the tables.
Childhood brain and ONS tumors demonstrate unique age-specific incidence patterns by sex and type of tumor classification (Supplementary Table 3, available online). The incidence rate remained below six per 100 000 persons until age 25–29 years, after which the incidence increased steadily until age 84 years. By sex, incidence rates were higher in boys through age 10–14 years, after which the incidence rates became higher in women, primarily because of the large increase in meningiomas in this group (Supplementary Tables 4 and 5, available online). Incidence rates were higher in men or similar to women for all age groups for most tumors of neuroepithelial tissue, nerve sheath tumors, germ cell tumors, and lymphomas; however, women had a much higher incidence rate of meningioma than men, beginning with age group 20–24 years. Incidence rates for tumors of the sellar region were higher in women until age 45–49 years; however, this pattern was reversed at 50 years and older. Acoustic neuromas began increasing from age 40 years, peaked at ages 65–69 years, after which the incidence rates decreased.
Trends of malignant neuroepithelial tumors by histological group are shown in Figure 1 and Supplementary Table 6 (available online). The incidence of these tumors in men and women combined increased at a rate of 1.9% per year from 1980 to 1987 and decreased at a rate of 0.4% per year from 1987 to 2007, resulting in a minimal net change from 1980 to 2007. However, trends in incidence rates differed markedly among histological groups within this category. Marked changes in incidence rates for primary brain lymphomas also were observed (data not shown).
Relative survival (14) for brain and ONS tumors is strongly related to age at diagnosis, histological type, and era of diagnosis, as demonstrated in Figure 2. Five-year survival for all malignant tumors of neuroepithelial tissue as well as for most histological types and age groups has increased over time. Five-year survival among children and adolescents with all malignant tumors of neuroepithelial tissue combined increased from 62.9% for those diagnosed in 1980–1989 to 75.3% in 2000–2006 (Supplementary Table 7, available online). Favorable survival and trends also were observed for those aged 20–39 years, for whom 5-year survival increased from 54.1% in 1980–1989 to 65.1% in 2000–2006. However, among those diagnosed at age 40–64 years, survival increased from only 16.1% to 26.6%; among those diagnosed at age 65 years or older, the 5-year survival was under 5%, even in the most recent period (2003–2007). Among the most common tumors, the 5-year survival for pilocytic astrocytoma increased from 90.1% in 1980–1989 to 96.4% in 2000–2006 among children aged 0–19 years. Survival was nearly as high in those aged 20–39 years and increased markedly in those aged 40 years or older, from 46.1% in 1980–1989 to 83.5% in 2000–2006. In contrast, there was relatively little improvement in survival for astrocytomas during this time interval. Irregular trends and low survival for glioblastoma were observed in the two youngest age groups (0–19 and 20–39 years), with 5-year survival exceeding 20% only in the most recent time period. In the two older age groups (40–64 and ≥65 years), glioblastoma survival exceeded 5% at 5 years only in those aged 40–64 years diagnosed in 2000–2006. Five-year survival for oligodendroglioma and anaplastic oligodendroglioma in those aged 0–19 years increased from 70.2% to 90.8% in 2000–2006. Survival of greater than 75% was observed for those aged 20–39 years, in each time period. Although survival increased over time for those aged 40–64 years and those 65 years and older, it remained generally lower than in the younger age groups. In contrast, survival trends for neuroepithelial tumors in the grouping “embryonal, primitive, and medulloblastoma” differed by age group, with marked increases for those in the 0–19 and 20–39 year age ranges but marked decreases for those aged 40 years and older. Survival for malignant gliomas, not otherwise specified, showed greater improvement over time than for mixed gliomas.
Death rates for malignant brain tumors during 1999–2007 were stable in children (aged 0–19 years) but decreased in adults (aged ≥20 years) at a rate of 1.2% per year. Death rates for benign brain tumors decreased in both children (−2.5% per year) and adults (−2.2% per year). Trends in mortality for malignant vs non-malignant brain tumors could not be examined for earlier time periods because of inconsistencies in ICD coding over time.
This “Annual Report to the Nation” is the first to document a statistically significant decrease in lung cancer incidence and death rates among women from 2003 to 2007 (Tables 1 and and2),2), more than a decade after the rates began to decrease in men. Although cigarette smoking peaked in men who served in World War II and were born in the early 1920s, it peaked in women born in the late 1930s (32,33). The decrease in lung cancer rates in women that we are seeing now reflects the later uptake of cigarette smoking among women. The decrease in lung cancer rates in women can be expected to continue for at least two decades as women in the older generations with higher lung cancer risk are replaced by the subsequent younger generations with lower risk. But trends may be interrupted as women born around 1960, who have higher lung cancer and smoking rates, enter the high-risk age groups (11,34,35). In contrast to women, lung cancer rates in men are expected to continue to decrease in the subsequent younger generations (11).
In addition to lung cancer, death rates in the most recent period (2003–2007) showed a statistically significant decrease for seven of the remaining 14 leading cancers among both men and women (cancers of the colorectum, kidney, stomach, brain, leukemia, non-Hodgkin lymphoma, and myeloma) as well as for prostate and oral cancer among men and cancers of the breast, ovary, and bladder among women. As a result, death rates from all cancers combined continued to decrease among both men and women and in all racial and ethnic groups, except among AI/AN women. These decreases indicate real progress in cancer control, reflecting a combination of primary prevention, early detection, and treatment (2–12). However, death rates continued to increase for cancers of the pancreas and liver among men and women, and for uterine cancer in women, cancers for which there are no established screening tests. Among men, death rates also increased for melanoma, for which population screening is not recommended but prevention and early detection strategies are available (36,37). Among children, long-term (1975–2007) trends in death rates continued to decrease, although at a slower pace during the recent decade than in earlier years.
The overall cancer incidence rates showed a statistically significant decrease during the most recent period (2003–2007) in women, but the decrease was not statistically significant in men. These trends are driven largely by trends in the most common cancer sites (lung, colorectal, prostate, and female breast), accounting for more than 50% of the overall rates in both men and women (38). Incidence rates decreased for cancers of the lung, colorectum, and oral cavity in both men and women; for breast, cervix, uterine, and bladder cancers in women; and for stomach and brain cancers in men. In contrast, incidence rates increased for kidney and pancreatic cancers and melanoma in both men and women, for liver cancer in men, and for thyroid cancer and leukemia in women. Prostate cancer rates showed a non-statistically significant increase. Factors that contribute to these trends were discussed previously (4,7,8,11,12,34,35) and include changes in risk factors, screening modalities, and diagnostic practices.
Of the leading cancers, prostate cancer and breast cancer are of special note because they are the most frequently diagnosed cancers and second leading cause of cancer death among men and women, respectively. Prostate cancer incidence has fluctuated through the years, decreasing during 1992–1995, increasing during 1995–2001, decreasing during 2001–2005, and increasing again during 2005–2007, albeit non-statistically significantly (Table 1). Prostate cancer death rates have decreased substantially over time (39), but the contribution of prostate-specific antigen screening to this decrease and the risks and benefits for individual men remain uncertain (40–44).
Trends in breast cancer incidence over time reflect long-term changes in reproductive and other risk factors, introduction and prevalence of mammography screening, and use of hormones among postmenopausal women (45) (Table 1 and Supplementary Table 1, available online). Breast cancer incidence rates stabilized from 2003 to 2007 (46) after decreasing sharply between 2002 and 2003, which was temporally associated with the dramatic decrease in the use of postmenopausal hormonal replacement therapy (47,48). The stabilization of the rates after the sharp decrease between 2002 and 2003 may in part reflect the role of hormonal replacement therapy as a promoting agent rather than as an initiating agent in the development of breast cancer (DeSantis et al., unpublished data). Meanwhile, breast cancer death rates continued to exhibit a statistically significant decrease. Mammography screening generally is accepted to reduce breast cancer mortality and has been recommended for some time, although recommendations have varied among organizations with respect to age at initiation for average risk women, screening intervals, and screening modalities, especially for high-risk women (49–55).
Of concern is the long-term increase in cancer incidence rates among children, which may be because of larger increases in incidence rates for the lymphoid leukemias and proportionately smaller increases for other childhood cancers (56). Considerable progress has occurred for many types of childhood cancers, resulting in decreases in cancer death rates among children since 1975, although the rate of decrease has slowed since the mid-1990s. These decreases have resulted from refinements in treatment that substantially improved survival for many childhood cancers. However, for some types of childhood cancer, including some brain tumors, progress has been more modest and current treatments remain inadequate (56).
Differences in rates and trends in incidence and death rates for specific cancers for different racial and ethnic groups and for men and women suggest differences in risk behaviors, socioeconomic status, and access to and use of screening and treatment (57,58). It is particularly important to monitor these trends to identify opportunities and set priorities for cancer control interventions. Where possible, it is important to examine multiple indices and risk indicators at the national, state, and local level. In addition, although not always feasible in national reports, it is important to recognize that categorizing the population by broad racial and ethnic categories may mask important differences within and among populations.
We provided a comprehensive evaluation of the incidence and mortality for all primary (malignant and nonmalignant) brain and ONS tumors, as well as trends in incidence and survival on a national level. This report expands on the descriptive epidemiology of primary brain tumors presented by the Central Brain Tumor Registry of the United States in its annual statistical report (16). Collection of nonmalignant (benign or uncertain behavior) tumors began nationwide in diagnosis year 2004, allowing for 4 years of data (2004–2007) to be presented here. Nonmalignant tumors accounted for the majority of all brain tumors, representing two-thirds of all adult and one-third of all childhood (aged 0–19 years) brain tumors. Capturing surveillance data on nonmalignant brain tumors has demonstrated that meningioma is the most common form of brain tumor in the United States. Differing patterns by race, sex, and age were seen for different types of malignant and nonmalignant brain tumors. Although the reasons for these differences have not been elucidated, they may prove important for discovering differences in the etiology of these diverse tumors.
An important finding of the current analysis is the relative stability of the long-term incidence trends of malignant tumors of the neuroepithelial tissue. During the 27-year (1980–2007) time period studied, an increase of 1.9% per year during 1980–1987 was counterbalanced by a decrease of 0.4% per year during the remaining 20 years, resulting in nearly identical incidence rates at the beginning and end of the study. However, marked differences in trends were observed for histological groups within this category of tumors. As with many cancers, trends may be influenced by a number of factors, including changes in diagnostic techniques and changes in coding and classification. The introduction of computed tomography scans in the 1970s and magnetic resonance imaging scans and stereotactic biopsy in the mid-1980s (59) has led to less invasive methods for diagnosing these tumors and contributed in part to fluctuations in the incidence rates over time. Revisions in the World Health Organization’s histological classification of ONS tumors and the ICD-O also occurred during the period of the study, along with changes in the multiple primary rules for malignant brain tumors and the introduction of multiple primary rules for nonmalignant brain tumors. Brain and ONS tumors have been particularly difficult to diagnose pathologically because they often are heterogeneous histologically, genetically, and therapeutically (17,60). However, progress in understanding the molecular pathogenesis of malignant gliomas has begun to allow for better classification of these tumors (61–63).
In contrast to tumors of neuroepithelial tissue, marked changes in the incidence of lymphomas of the brain have been observed, likely because of increases in AIDS-related lymphomas in the 1980s, followed by decreases in AIDS-related lymphomas after the introduction of highly active antiretroviral therapy in the 1990s (64). The short time period for which data on nonmalignant brain tumors are available in the United States precluded analysis of temporal trends.
Modest improvements in survival for many types of brain and ONS tumors likely result from improvements in diagnostic and surgical techniques, radiotherapy, chemotherapy, biological therapy, and the use of multimodality therapy (65,66). Despite improvements in treatment, major prognostic factors include the histology of the tumor, whether complete surgical resection is achieved, and the age of the patient at diagnosis (66). Late effects of therapy for childhood brain tumors are substantial and include neurocognitive deficiencies, hormone deficits, growth impairment, second primary brain tumors, and ototoxicity related to platinum chemotherapy (67–69).
Several reviews of risk factors for brain tumors have been published recently (70–78). The relatively low variation in incidence and death rates for cancer of the brain and ONS nationally and internationally suggests that environmental risk factors do not play a major role in this disease (70–74). In fact, other than hereditary tumor syndromes (17) and increased familial risk without a known syndrome (79–82), the only known modifiable causal risk factor for brain tumors is exposure to ionizing radiation (71–74,78). Variability in age at onset and molecular tumor characteristics suggests that risk factors for brain tumors may differ by histological type (16,17,75,75–77). An example is the mostly consistent inverse association that has been observed between history of atopic disease, including allergies and asthma, and risk of glioma (72–74,83–97) and possibly meningioma (78,95–98); but no association with nerve sheath tumors has been found (84).
Several reviews summarize studies evaluating exposure to cellular phones and the risk of brain tumors (78,99–102). Short-term (<10 years) exposures to cellular telephones appear to have no association with risk of brain tumors. However, the association with long-term (>10 years) use remains unclear, primarily because of the relatively recent adoption of widespread use of cellular phones, as well as issues of bias and study design. Acoustic neuromas are of particular interest with regard to cellular phone use because of the proximity of these tumors to the phone. However, studies that have examined this association have mixed results and limited numbers of long-term users; further studies with longer term follow-up will be needed to evaluate whether there is an increased risk of acoustic neuromas associated with the use of cellular phones (99–102). A recent study using data from SEER 9 registries for 1977–2006 found decreasing or stable brain cancer incidence rate trends for whites in most age groups except among women aged 20–29 years in 1992–2006, which was driven by a rising incidence of frontal lobe cancers (103). We examined age- and sex-specific trends in overall malignant brain cancer incidence rates among whites in the SEER 13 registries from 1992 to 2007 and NAACCR data for 1995–2007 (Supplementary Table 8, available online). Although the short time period for which non-malignant data are available in the United States precludes analysis of temporal trends, the relatively large number of acoustic neuromas identified in the first 4 years of data collection suggests that etiologic studies will be possible in the future.
High-quality cancer surveillance data now cover 93% of the US population for incidence and the entire population for mortality; however, certain limitations in data sources, data collection, and analyses may have influenced the findings of this report. First, state and national population estimates are provided annually by the Census Bureau to estimate intercensal populations. Differences between the numerator (incidence data) and denominator (US Census population data) can occur in the designation of race and/or ethnicity, place of residency, age, single vs multiple races, and the like. Every effort is made to ensure that the definition of the numerator and denominator are the same. Intercensal population estimates based on numbers updated by birth and death data are more subject to error than the estimates based on the actual count. Although these population estimates are believed to be the most accurate available, errors in the estimates may increase as time passes from the original recording of Census data. The NCI developed modifications to these Census estimates to attempt to account for changes in 2005 county-level populations because of displacement of people after Hurricanes Katrina and Rita in the most-affected counties of Louisiana, Mississippi, Alabama, and Texas. Censal and other data are used to classify the incidence cases, and census definitions are used to determine residency for the incidence cases. Race and ethnicity, however, generally are self-reported, but for the incidence cases, this information may come from a wider group of sources (patient, relative, nurse, doctor, coroner, funeral director). To enhance race and ethnicity, determination for the incidence cases, special studies and algorithms are used. For example, a match of incidence cases to IHS rosters is undertaken to correct the possible underreporting of AI/ANs, and NAACCR has developed guidelines and algorithms for enhancing Hispanic-Latino and API identification. Consistency over time in definitions for both census and incidence data is an issue, and efforts have been made to bridge single race and multiple race reporting (more information available on http://www.cdc.gov/nchs/nvss/bridged_race.htm). Second, joinpoint models were used to describe long-term (1992–2007) and short-term (1998–2007) trends. The AAPC, a summary measure of a trend over a prespecified fixed interval based on an underlying joinpoint model, was used to describe all trend data. The joinpoint model is preferable to single linear regression when a sufficient number of years are available for analysis because it enables identification of recent changes in magnitude and direction of trends. However, it may mask the underlying data and give an impression of a continuous increase or decrease over time when this is not the case. In addition, although methods have been adapted recently to adjust for delayed reporting of aggregated data similar to earlier published methods used for incidence from the nine oldest SEER registries (30), methods have not been tested on data from registries outside of SEER and were employed in our analysis only for SEER 9 and SEER 13. Delayed reporting may affect the most recent joinpoint segments, overestimating recent decreases and underestimating recent increases.
Third, US Department of Veterans Affairs (VA) hospitals traditionally have been a major source of data for cancers diagnosed among veterans, representing approximately 3%–8% of cancer diagnoses among men. A 2007 policy change regarding the transfer of VA cancer data to state central cancer registries has resulted in incomplete reporting of VA hospital cases in some but not all state registries. This change has affected reporting from the third quarter of the 2004 diagnosis year through the current time period. As a result, cancer incidence rates among men for 2005–2007 are thought to be underestimated by 0.8%–2% for all cancers combined, according to independent statistical analyses conducted by the CDC and SEER. The level of underreporting varied from 0.5% to 4% according to cancer site, race, and age group (14,104). The amount of underestimation also may vary by local VA facility reporting patterns and the VA’s contribution to the total number of cancers. Progress in collecting VA data has been made in many states with the enactment of special data-sharing agreements with the VA. Over time, as cancer registries receive these missing VA cases, national cancer incidence estimates will be more complete and accurate.
Fourth, as routinely noted in the Annual Reports to the Nation (1–12), the broad racial and ethnic groups categorized for our analyses may mask variations in the cancer burden by country of origin; for example, Chinese and Vietnamese in the API group (105) and Cubans and Mexicans in the Hispanic group (9,106), or by other unique characteristics of high- or low-risk populations (107–110). Also, cancer rates for populations may be limited by difficulties in ascertaining race and ethnicity information from medical records, death certificates, and census reports (25).
The observed decreases in overall cancer incidence and death rates in nearly all racial and ethnic groups are highly encouraging. This progress could be accelerated by comprehensively applying existing cancer control knowledge of cancer prevention, early detection, and treatment to public health and clinical practices. Unfortunately, at this point in time, not all cancer sites are amenable to cancer control practices, and innovative methods to study these cancers and rare tumors must be developed. For example, the relative rarity of brain tumors, including many histological subtypes, has required investigators to establish consortia and pooled studies, especially for studies of genetic risk factors and gene–environment interaction (70,111–114). Many advances are being made in the molecular characterization of brain and ONS tumors and many other types of cancer. Tumor biospecimen banking linked with treatment and outcome information will be particularly important in studying the prognostic and predictive value of such markers and in developing targeted therapies (115–117) to improve effectiveness, lessen toxicity, and measure response to therapy more quickly. It is too early to assess the impact of some treatment advances or the progress in targeted therapy that is expected to emerge in future years.
The US population aged 65 years and older is expected to double in size by 2030 (about 71 million persons) compared with the number reported in the 2000 census (118). Improvements in health and welfare also mean that individuals are expected to live longer, often with a range of health conditions that include the diagnosis of cancer. Even with declining cancer incidence rates, the absolute number of individuals diagnosed with cancer will continue to increase because of these population changes, leading to increased demand for cancer-related medical services through the spectrum of diagnosis, active treatment, and posttreatment medical management. Effective management of the cancer burden will require the application of sound cancer control strategies in prevention, detection, treatment, and survivorship, as well as resources to provide good quality of care. Continued utilization of quality population-based data systems and translation of evidence-based clinical and basic research findings to public health practices are essential to the development of public policies for cancer.
The American Cancer Society, the National Cancer Institute of the National Institutes of Health, the Centers for Disease Control and Prevention, the Central Brain Tumor Registry of the United States, and the North American Association of Central Cancer Registries. Funding to pay for the Open Access publication charges associated with the article was provided by the National Cancer Institute.
The findings and conclusions in this article are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. The authors would like to acknowledge the contribution of central population- and hospital-based cancer registry staff who collected and compiled the incidence data used in this study. In addition, we thank Andrew Lake, Martin Krapcho, and Rick Firth, of Information Management Services, Inc, for assisting in statistical analyses; Dr Janet Bruner, who reviewed the brain site/histology combinations; Dr Susan Chang, for her input on our early draft; and the Central Brain Tumor Registry of the United States for supporting Dr Bridget McCarthy’s efforts and expertise.