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Article first published online: 13 NOV 2007
Published 2007 American Cancer Society
Volume 112, Issue 1, pages 181–192, 1 January 2008
How to Cite
Wingo, P. A., Tucker, T. C., Jamison, P. M., Martin, H., McLaughlin, C., Bayakly, R., Bolick-Aldrich, S., Colsher, P., Indian, R., Knight, K., Neloms, S., Wilson, R. and Richards, T. B. (2008), Cancer in Appalachia, 2001–2003. Cancer, 112: 181–192. doi: 10.1002/cncr.23132
Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.
This is a US government work and, as such, is in the public domain.
- Issue published online: 17 DEC 2007
- Article first published online: 13 NOV 2007
- Manuscript Accepted: 3 JUL 2007
- Manuscript Revised: 1 JUL 2007
- Manuscript Received: 18 APR 2007
- cancer incidence;
- health disparities;
- National Program of Cancer Registries (NPCR);
Researchers have not been able to examine cancer incidence rates in Appalachia because high-quality data have not been uniformly available across the region. This study is the first to report cancer incidence rates for a large proportion of the Appalachian population and describe the differences in incidence rates between Northern, Central, and Southern Appalachia.
Forty-four states and the District of Columbia provided information for the diagnosis years 2001 through 2003 from cancer registries that met high-quality data criteria. Eleven of 13 states with counties in Appalachia, covering 88% of the Appalachian population, met these criteria; Virginia and Mississippi were included for 2003 only. SEER*Stat was used to calculate age-adjusted rates per 100,000 population and 95% gamma confidence limits.
Overall, cancer incidence rates were higher in Appalachia than in the rest of the US; the rates for lung, colon/rectum, and other tobacco-related cancers were particularly high. Central Appalachia had the highest rates of lung (men: 143.8; women: 75.2) and cervical cancer (11.2)—higher than the other 2 regions and the rest of the US. Northern Appalachia had the highest rates for prostate, female breast, and selected other sites, and Southern Appalachia had the lowest overall cancer incidence rates.
Cancer incidence rates in Appalachia are higher than in the rest of the US, and they vary substantially between regions. Additional studies are needed to understand how these variations within Appalachia are associated with lifestyle, socioeconomic factors, urban/rural residence, and access to care. Cancer 2008. Published 2007 by the American Cancer Society.
The part of the eastern US classified as Appalachia has been characterized by high rates of poverty and health disparities,1–6 and several studies have linked high poverty with cancer incidence and mortality.7–10 Death rates for all cancer sites combined, lung cancer in men, colorectal cancer in men and women, and cervical cancer have been shown to be significantly higher in Appalachia than in the rest of the US,11–12 and incidence rates for lung, colon/rectum, and cervix in the Appalachian areas of Kentucky, Pennsylvania, and West Virginia were significantly higher than in the areas covered by the Surveillance, Epidemiology, and End Results (SEER) Program.13 Until recently, however, it has not been possible to examine cancer incidence rates across Appalachia because data from high-quality registries have not been uniformly available throughout the region.
Researchers have proposed various criteria to define Appalachia,14–17 but the boundaries most widely accepted are those determined by the Appalachian Regional Commission (ARC).18 Established in 1965, the ARC has defined and redefined the boundaries of Appalachia several times. This study used the most recent ARC definition, which includes 410 counties in 13 states. To account for the diversity within Appalachia, the ARC created 3 regional subdivisions: Northern, Central, and Southern Appalachia (Fig. 1). These regions have very different socioeconomic characteristics, with indicators for Central Appalachia being appreciably less favorable, particularly in the rural areas, than the remainder of the US and the other Appalachian regions.1, 19 Southern Appalachia compares more favorably with the rest of the US in terms of the mean household income and the percentage of the population below the federal poverty index, and in the northern region the percentage of persons aged 25 years or older with a high school diploma is similar to that for the US.19 The mean household income in the northern region, however, is lower than that for the US.
This study describes the incidence of cancer in Appalachia, compares incidence there to the rest of the US, and illustrates how cancer incidence rates differ between Appalachia's 3 regions.
MATERIALS AND METHODS
Information on newly diagnosed cancer cases in the US is based on data collected by the National Program of Cancer Registries (NPCR) of the Centers for Disease Control and Prevention20 and the SEER Program of the National Cancer Institute.21 The SEER Program has collected incidence data from population-based cancer registries since 1973 and currently supports registries in 9 states and 5 metropolitan areas, covering 26% of the US population.21 In 1994, NPCR began providing funds and technical assistance to selected states to collect population-based incidence data.20 Currently, 45 states, the District of Columbia, and 3 US territories participate in NPCR, which covers 96% of the US population.
Because the quality of cancer incidence data varies by registry, registry data are evaluated according to objective standards established by national organizations.22–23 Registry data for the diagnosis years 2001–2003 (submitted January 31, 2006, from NPCR registries and submitted November 1, 2005, from SEER registries) met the following high-quality data criteria for inclusion in this analysis: 1) case ascertainment was at least 90% complete, based on the incidence-to-mortality rate ratio method; 2) at least 97% of cases passed a standard set of computerized edits; 3) less than 5% of cases were reported by death certificate only; and 4) information was missing for less than 3% of cases on sex, 5% on race, and 3% on age at diagnosis.22–23 Because Appalachia is defined by ARC along county boundaries (Fig. 1), all states with counties in Appalachia were also required to have less than 3% of their cases missing information about county of residence at diagnosis.
Data from 11 of 13 state cancer registries in Appalachia met all high-quality data criteria and covered 88% of the total Appalachian population (Fig. 1). Data from 9 states were for the diagnosis years 2001 through 2003; data from Mississippi and Virginia were for the diagnosis year 2003 only; data from Maryland and Tennessee were excluded. Population coverage in Northern Appalachia was 98% complete (all Appalachian counties in New York, Pennsylvania, Ohio, and selected Appalachian counties in West Virginia). Coverage in Central Appalachia was 75% complete (all Appalachian counties in Kentucky and selected Appalachian counties in Virginia and West Virginia). Coverage in Southern Appalachia was 80% complete (all Appalachian counties in Mississippi, Alabama, Georgia, North Carolina, South Carolina, and selected Appalachian counties in Virginia). High-quality registry data for the US rates are based on counties not in Appalachia and are from 44 states and the District of Columbia. These states cover approximately 91% of the US population; data from Arizona, North Dakota, South Dakota, Maryland, Tennessee, and Wyoming were excluded.
SEER*Stat was used to calculate age-adjusted cancer incidence rates.24 All rates were expressed per 100,000 population and were age-adjusted to the 2000 US standard million population by 5-year age groups25–26; 95% gamma confidence limits (CL) were calculated for the age-standardized rates.27
To map the cancer burden throughout Appalachia, the incidence rates for Appalachian counties included in this study were ranked from largest to smallest for male lung cancer, female lung cancer, prostate cancer, and female breast cancer. Counties with fewer than 16 cases were not ranked to discourage misinterpretation or misuse of rates that are unstable because counts were small. The resulting ranked lists of counties for each of the 4 sites were then divided into tertiles for the maps shown in Figures 2A, 2B, 3, and 4.
For all cancer sites combined, incidence rates among both men and women residing in Appalachia were higher than rates for the rest of the US (Tables 1, 2). Rates varied by Appalachian region and, in general, were higher in the Central and Northern Appalachia than in Southern Appalachia.
|Population Coverage (%)||Appalachia||United States (Counties not in Appalachia)|
|Southern Appalachia‡||Central Appalachia§||Northern Appalachia∥||Total|
|Primary Site||Rate||95% CI||Rate||95% CI||Rate||95% CI||Rate||95% CI||Rate||95% CI|
|Oral cavity and pharynx||16.7||15.9||17.5||17.2||15.5||19.1||15.5||14.9||16.1||16.1||15.6||16.5||15.3||15.1||15.4|
|Colon and rectum||59.2||57.7||60.7||69.7||66.1||73.4||71.0||69.6||72.3||66.7||65.7||67.7||59.7||59.4||60.0|
|Liver and intrahepatic bile duct||6.6||6.1||7.2||5.3||4.3||6.4||6.3||5.9||6.7||6.4||6.1||6.7||8.1||8.0||8.2|
|Lung and bronchus||105.4||103.4||107.4||143.8||138.8||149.1||99.1||97.5||100.7||105.0||103.8||106.2||84.3||84.0||84.7|
|Melanomas of the skin||21.8||20.9||22.7||22.0||20.0||24.1||18.8||18.1||19.5||20.2||19.6||20.7||20.0||19.9||20.2|
|Kidney and renal pelvis||17.3||16.5||18.1||19.6||17.8||21.6||18.3||17.6||19.0||18.0||17.5||18.5||17.6||17.5||17.8|
|Brain and other nervous system||7.8||7.3||8.4||7.5||6.4||8.8||8.3||7.8||8.8||8.0||7.7||8.3||7.5||7.4||7.6|
|Population Coverage (%)||Appalachia||United States (Counties not in Appalachia)|
|Southern Appalachia‡||Central Appalachia§||Northern Appalachia∥||Total|
|Primary Site||Rate||95% CI||Rate||95% CI||Rate||95% CI||Rate||95% CI||Rate||95% CI|
|Oral Cavity and pharynx||6.3||5.9||6.7||5.4||4.5||6.3||5.7||5.4||6.1||5.9||5.7||6.2||5.9||5.8||6.0|
|Colon and rectum||41.0||39.9||42.1||53.2||50.6||56.0||51.4||50.4||52.4||47.8||47.1||48.5||43.6||43.4||43.8|
|Liver and Intrahepatic bile duct||2.2||2.0||2.5||2.3||1.7||2.9||2.4||2.2||2.6||2.3||2.2||2.5||2.9||2.8||2.9|
|Lung and bronchus||52.8||51.6||54.1||75.2||72.0||78.5||57.0||55.9||58.0||56.9||56.1||57.7||52.7||52.4||52.9|
|Melanomas of the skin||14.6||13.9||15.2||16.2||14.6||17.8||13.2||12.6||13.8||13.9||13.5||14.3||12.9||12.8||13.0|
|Uterine corpus, NOS||18.9||18.1||19.6||25.3||23.4||27.3||30.3||29.5||31.2||25.4||24.8||25.9||22.6||22.5||22.8|
|Kidney and renal pelvis||9.0||8.5||9.5||10.0||8.9||11.3||10.1||9.6||10.6||9.7||9.4||10.0||9.1||9.0||9.2|
|Brain and other nervous system||5.7||5.3||6.1||5.0||4.2||6.0||6.3||5.9||6.7||6.0||5.7||6.2||5.4||5.3||5.4|
|Breast, in situ||25.8||25.0||26.7||19.1||17.5||20.8||26.3||25.6||27.1||25.5||25.0||26.1||28.1||28.0||28.3|
The lung cancer rate for Appalachian men was nearly 25% higher than the rate for men living in the rest of the US (Table 1). The lung cancer incidence rates among men in all 3 regions of Appalachia were higher than the US rate (84.3) (Table 1, Fig. 2A), with the highest rate in Central Appalachia (143.8) and the lowest rate in Northern Appalachia (99.1). The lung cancer rate for Appalachian women was 8% higher than the rate for women in the rest of the US, and these rates also varied by region (Table 2, Fig. 2B). Like men, the highest lung cancer incidence rate for Appalachian women occurred in Central Appalachia (75.2), where the rate was 43% higher than the rate for women in the rest of the US (52.7). The lowest rate was in Southern Appalachia (52.8).
Other tobacco-related cancers showed similar patterns. Among men, the rate for cancer of the larynx for all of Appalachia was higher than for US men (Table 1). Like lung cancer, rates in all 3 regions were higher than for the rest of the US (7.1), with the highest rate in Central Appalachia (10.7). For bladder cancer, the rate in Northern Appalachia (43.6) was higher than the rate for US men (36.1), but the rate in Southern Appalachia was lower (33.0). The rate of oral and pharyngeal cancer among men in Appalachia overall was also higher than the rate for US men, and rates were significantly higher in the central and southern regions. Among women, incidence rates for cancers of the larynx and urinary bladder were higher overall than the rates for women living in the rest of the US; the rates of laryngeal cancer for women in Central Appalachia (2.7) and bladder cancer in Northern Appalachia (11.2) were particularly high (Table 2).
Colorectal cancer incidence rates among both men and women residing in Appalachia overall were higher than rates among men and women in the rest of the US (Tables 1, 2). The rates were particularly high for men and women in Northern and Central Appalachia with men having a rate of approximately 70 per 100,000 and women, 52 per 100,000. For both men and women, the rates in Southern Appalachia were lower than in the rest of the US.
The rates of gynecologic cancers varied across Appalachia (Table 2). Within Appalachia, the highest rate for cervical cancer was in Central Appalachia (11.2), a rate that was 35% higher than the rate in the rest of the US. For uterine corpus and ovary, the highest rates within Appalachia were in the northern region. The rate of uterine cancer (30.3) was 34% higher in Northern Appalachia than the US rate (22.6), and the rate of ovarian cancer (14.5) was 12% higher than the US rate (12.9).
For Appalachia as a whole, prostate cancer was the most common malignancy in men, but the incidence rate was generally lower than the rate for men in the rest of the US (Table 1). The highest rate of prostate cancer occurred among men residing in Northern Appalachia (Table 1, Fig. 3), where the rate was nearly identical to the rate for the rest of the US (Northern Appalachia: 156.7, US: 156.4). For testicular cancer, rates in Appalachia and the rest of the US were similar. Northern Appalachia, however, had a higher rate of testicular cancer than the rest of the US.
Invasive breast cancer was the most common malignancy among women in Appalachia (Table 2). Women residing in Central Appalachia had the lowest breast cancer rate (107.3), and women residing in Northern Appalachia had the highest rate (122.6) (Table 2, Fig. 4), a rate that was similar to the rate for the rest of the US (121.0).
For Appalachia as a whole, the rate of in situ breast cancer was lower than the rate for the rest of the country (Table 2). The rate of in situ disease was much lower in Central Appalachia than for the other Appalachian regions and the rest of the US (Central Appalachia: 19.1, US: 28.1).
Other regional differences involved less common sites. For cancer of the esophagus and Hodgkin lymphoma among men and thyroid cancer among women, the highest rate was in the northern region. For melanomas of the skin, women in Central and both men and women in Southern Appalachia had higher rates than in the rest of the US. Finally, men and women residing in Appalachia had lower rates of stomach and liver and intrahepatic bile duct cancer than US men and women (Tables 1, 2).
This study found higher overall rates of cancer in Appalachia than in the rest of the US. It is the first study to provide detailed information on cancer incidence rates for a large proportion of the Appalachian population by including data from cancer registries in 11 of 13 states with counties in Appalachia, covering 88% of this population. Previous studies described the cancer burden only in selected states (eg, the incidence of cervical dysplasia and cervical carcinoma in the Appalachian region of Kentucky28 and, more recently, cancer incidence in the Appalachian regions of Kentucky, Pennsylvania, and West Virginia).13
Appalachia generally had higher rates of lung and colorectal cancer but lower rates of prostate and female breast cancer than the rest of the US, and the findings are consistent with the results published by Lengerich et al.,13 although the breast cancer results did not achieve statistical significance. Of greater interest, perhaps, are the substantial variations in cancer incidence rates within Appalachia. In this study, Central and Northern Appalachia had higher overall cancer incidence rates than Southern Appalachia and the rest of the US. Central Appalachia had higher rates of lung and laryngeal cancer than the other 2 regions of Appalachia and the rest of the US, and women in Central Appalachia had the highest rates of cervical cancer. Both lung and cervical cancer have been associated with high rates of poverty,7–9 and Central Appalachia has the most severe indicators of poverty in the region.19 Central Appalachia also had the lowest rates of in situ female breast cancer, a circumstance that may be indicative of low use of mammography screening in this population. A previous study of breast and cervical cancer screening in Appalachia showed that women with a lower household income or who were older or less educated were less likely to get Papanicolaou (Pap) tests and mammography than younger women or women with higher income or education.29 In addition, Appalachian women cite concerns about economics and embarrassment as barriers to screening.30
In contrast, Southern Appalachia, which has the most favorable socioeconomic indicators of the 3 regions,19 had lower overall cancer incidence rates than either of the other 2 regions within Appalachia for both men and women. Southern Appalachia also had the lowest rates of colorectal cancer for men and women, leukemia for men, and lung, uterine, and thyroid cancer for women.
The highest rates for malignancies of the female breast and prostate were found in Northern Appalachia. Northern Appalachia also had the highest rates of bladder cancer for both men and women, esophagus, testis and non-Hodgkin lymphoma for men, and uterus and thyroid for women.
These regional differences throughout Appalachia support the concept that Appalachia is not a homogeneous area and likely reflect actual differences in the socioeconomic conditions (eg, higher unemployment) and characteristics of the population, such as demographics, use of cancer screening tests, access to care (eg, costs, limited health insurance, lower availability of health care providers), health behaviors (eg, tobacco use, poor diet, physical inactivity), and exposure to cancer-causing agents.29, 31, 32 Differences in cancer registry operations, such as completeness of case reporting and timeliness, may also explain some of the study findings.
The higher rates of lung cancer in Appalachia as compared with the rest of the US are likely related to the high prevalence of adult tobacco use in the Appalachian region. The lung cancer rates in Central Appalachia are especially high. Kentucky and West Virginia are ranked among the top 5 states for high prevalence of adult smoking and per capita cigarette consumption (based on sales of packs). These same states have a low cost of cigarettes per pack and a low percentage of the population protected by nonsmoking policies in the workplace.33
Several cautions for interpreting the findings from this study should be considered. First, this study did not cover the entire population of Appalachia nor did it include data for all 3 diagnosis years for every state with counties in Appalachia. No data from Tennessee or Maryland were included, and data from Virginia and Mississippi were included only for 2003. Analyses that excluded Virginia and Mississippi were not materially different from the study findings. Still, this study included high-quality data from population-based cancer registries covering 88% of the population living in Appalachia, a much higher proportion than in previous studies.13, 28 However, if the burden of cancer in the Appalachian population excluded from this study (12%) differed appreciably from that in the population examined, then the findings will not accurately represent cancer in all of Appalachia. Second, the incidence rates estimated for the specific regions within Appalachia may be biased because population coverage varied across the regions. The central and southern regions did not include data from the Appalachian counties in Tennessee; similarly, the northern region did not include data from Appalachian counties in Maryland. Finally, the differences in completeness of case ascertainment and delays in reporting may have affected the observed incidence rates.34 If the completeness of case ascertainment is significantly higher in some states with Appalachian counties and significantly lower in others, then these differences could introduce bias. Only data from state cancer registries that met an objective standard for completeness of at least 90% were included in the analysis—the same standard used for the United States Cancer Statistics.20 Thirty-eight states had completeness estimates of at least 95%, and 6 states had estimates that ranged from 90% to 94%, including 4 states in Appalachia (1 each in the northern and central regions and 2 in the south).
These limitations notwithstanding, the present study provides a comprehensive first look at the burden of cancer across the regions of Appalachia. Cancer rates in general were appreciably higher in Appalachia overall than in the rest of the US, and rates varied greatly between the regions within Appalachia. The central region, marked by high rates of poverty, had much higher rates of lung and cervical cancer than the other regions in Appalachia and the rest of the US. Northern Appalachia also had high rates of selected cancers. In contrast, the cancer incidence rates in the Southern Appalachian region were very similar to those found in the rest of the US for men and were lower than rates in the rest of the US for women. Southern Appalachia, particularly in its urban areas, has experienced substantial economic growth and prosperity in the past decade.19 These findings support the idea that socioeconomic conditions are associated with higher incidence rates for some cancers. Future analyses by black/white race across the 3 regions could provide additional insights.
High-quality cancer incidence data are essential to the prevention, treatment, and control of disease,20, 35 and the need for such data in Appalachia was noted recently by the Appalachia Cancer Network.36 Cancer incidence data can be used to monitor the cancer burden over time, identify populations within the state with the highest risk of cancer, provide information for the allocation of healthcare resources (eg, screening among healthy populations and treatment for recurrence or progression of disease, for the effects or complications of treatment, for pain control, and for end-of-life issues), respond to public concerns and inquiries about cancer, evaluate cancer prevention and control activities (eg, incidence data can provide prompt evidence of the effects of a screening program), and provide data to advance clinical and epidemiologic research. For example, the Kentucky Cancer Registry identified geographic areas with low rates of early-stage breast cancer and high rates of late-stage disease and expanded mammography outreach activities in these areas37; Alabama Statewide Cancer Registry colon cancer data were linked to county level measures of socioeconomic status and physician density; the study found that being black and poor was related to being diagnosed at a late stage38; the Colorado Central Cancer Registry data are being used to investigate occupational exposures at the Rocky Flats Environmental Technology Site.39 The first-ever cancer incidence data presented in this report for the 3 regions of Appalachia provide the foundation to guide the distribution of scarce resources for preventing and controlling disease in this underserved population.
Historically, Appalachia has been marked by high rates of poverty.40 The substantial variations in the cancer burden reported in this study and the socioeconomic conditions within the region should be carefully considered when planning programs for cancer control.19 Specific emphasis should be given to tobacco control in Central Appalachia and screening for breast, cervical, and colorectal cancers in Central and Northern Appalachia. Other critical next steps include developing and implementing unique intervention strategies at the community level, building cancer coalitions like those initiated for rural Appalachia in New York and Pennsylvania,41 and tailoring culturally appropriate health messages to address the cancer burden identified for each region in Appalachia.
- 12005 [cited 2005 Apr 3]; available from URL: http://www.arc.gov., . Economic review of Appalachia. Appalachian Regional Commission. ARC website
- 3An American Challenge: A Report on Economic Trends and Social Issues in Appalachia. Dubuque, IA: Kendall-Hunt; 1995..
- 5Recent trends in poverty in the Appalachian region. Madison: University of Wisconsin, Applied Population Laboratory; 2000. available from URL: http://www.arc.gov/index.do?nodeId=57..
- 6Appalachia: where place matters in health. Prev Chronic Dis [serial online]. 2006 October. Available from URL: http://www.cdc.gov/pcd/issues/2006/oct/06_0067.htm., .
- 11Centers for Disease Control and Prevention. Cancer death rates — Appalachia, 1994–1998. MMWR. 2002; 51: 527–529.
- 14Appalachia — A Regional Geography: Land, People and Development. Boulder, CO: Westview Press; 1984., , .
- 15The Southern Appalachian Region: A Survey. Lexington: University of Kentucky; 1962..
- 16The Southern Highlander and His Homeland. New York: Russell Sage Foundation; 1921..
- 17Our Southern Highlanders. New York: Macmillian; 1913..
- 18Appalachian Regional Commission. ARC website 2005 [cited 2005 August 15]; available from URL: http://www.arc.gov.
- 192005 [cited 2003 June 15]; available from URL: http://www.arc.gov.. Appalachia at the millennium: an overview of results from census 2000. Population Reference Bureau. Appalachian Regional Commission. ARC website
- 20United States Cancer Statistics Working Group. United States Cancer Statistics: Incidence and Mortality 2003. 5th ed. Atlanta, GA: Department of Health and Human Services, Centers for Disease Control and Prevention and National Cancer Institute; 2006.
- 21SEER Cancer Statistics Review, 1975–2003, National Cancer Institute. Bethesda, MD, available from URL: http://seer.cancer.gov/csr/1975_2003/, based on November 2005 SEER data submission, posted to the SEER web site, 2006., , , et al.
- 22Certification for population-based cancer registries. J Reg Manage. 1999; 26: 24–27., , .
- 23Measuring the quality of central cancer registries: the NAACCR perspective. J Reg Manage. 2001; 28: 41–44., .
- 24National Cancer Institute. SEER*Stat 4.2, Surveillance Epidemiology and End Results Program. Bethesda, MD: Division of Cancer Prevention and Control, National Cancer Institute; 2002. Available from URL: http://seer.cancer.gov.
- 25Bureau of the Census. Population estimates. Bureau of the Census 2002. Available from URL: http://eire.census.gov/popest/data/countiesl.php.
- 26Statistical Methods for Rates and Proportions. New York: John Wiley & Sons; 2005..
- 30Assessing awareness and knowledge of breast and cervical cancer among Appalachian women. Prev Chronic Dis. [serial online] 2006 October. Available from: http://www.cdc.gov/pcd/issues/2006/oct/06_0031.htm., .
- 31Cancer in Appalachia Ohio. Ohio Department of Health Cancer Surveillance Report. Chronic Disease and Behavioral Epidemiology/Ohio Cancer Incidence Surveillance System, Bureau of Health Surveillance-Prevention, Ohio Department of Health, June 2002., , .
- 33Sustaining state programs for tobacco control: data highlights for 2004. Centers for Disease Control and Prevention, Atlanta, GA. Available from URL: http://www.cdc.gov/tobacco/datahighlights/index.htm.
- 35Using central cancer registry data for cancer control. In: MenckH,DeapenD,PhillipsJ,TuckerT, eds. Central Cancer Registries: Design, Management and Use. Dubuque, IA: Kendall/Hunt; 2007: 313–323..
- 37Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion. Division of Cancer Prevention and Control. Cancer registries: the foundation for cancer prevention and control, at-a-glance 2001. Atlanta, GA; 2002.
- 39Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Division of Cancer Prevention and Control. Cancer registries: the foundation for cancer prevention and control, 2003 program fact sheet 2003. Atlanta, GA; 2004.
- 40Sowing seeds in the mountains: community-based coalitions for cancer prevention and control. Bethesda, MD: National Cancer Institute; 1994., , .
- 41Initiatives of 11 rural Appalachian cancer coalitions in Pennsylvania and New York. Prev Chronic Dis [serial online] 2006 October. Available from URL: http://www.cdc.gov/pcd/issues/2006/oct/06_0045.htm., , , , .