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Assessing the Burden of HPV-Associated Cancers in the United States Supplement to Cancer
Cervical Cancer Incidence in the United States in the US-Mexico Border Region, 1998–2003 Steven S. Coughlin, PhD1 Thomas B. Richards, MD1 Kiumarss Nasseri, DVM, MPH, PhD2 Nancy S. Weiss, MPH, PhD3 Charles L. Wiggins, PhD, MSPH4 Mona Saraiya, MD, MPH1 David G. Stinchcomb, MA, MS5 Veronica M. Vensor, MS6y Carrie M. Nielson, PhD, MPH7
BACKGROUND. Cervical cancer mortality rates have declined in the United States, primarily because of Papanicolaou testing. However, limited information
1
states and with those of nonborder states. Differences were examined by age,
Epidemiology and Applied Research Branch, Division of Cancer Prevention and Control, Centers for Disease Control and Prevention, Atlanta, Georgia. 2
Public Health Institute, California Cancer Registry, Santa Barbara, California. 3 Texas Cancer Registry, Texas Department of State Health Services, Austin, Texas. 4
New Mexico Tumor Registry, University of New Mexico, Albuquerque, New Mexico. 5
Division of Cancer Control and Population Sciences, National Cancer Institute, Bethesda, Maryland. 6
Arizona Department of Health Services, Phoenix, Arizona. 7 Oregon Health and Science University, Portland, Oregon.
Steven S. Coughlin’s current address: Environmental Epidemiology Service, Department of Veterans Affairs. y
Deceased.
This supplement to Cancer was supported by Cooperative Agreement Number U50 DP424071-04 from the Centers for Disease Control and Prevention (CDC). The findings and conclusions in this report are those of the authors and do not necessarily reflect the views of the Centers for Disease Control and Prevention or the National Cancer Institute.
is available about the incidence of the disease in the US-Mexico border region, where some of the poorest counties in the United States are located. This study was undertaken to help compare the patterns of cervical cancer incidence among women in the US-Mexico border region and other parts of the United States.
METHODS. Age-adjusted cervical cancer incidence rates for border counties in the states bordering Mexico (California, Arizona, New Mexico, Texas) for the years 1998 to 2003 were compared with the rates for nonborder counties of the border race, ethnicity, rural residence, educational attainment, poverty, migration, stage of disease, and histology.
RESULTS. Overall, Hispanic women had almost twice the cervical cancer incidence of non-Hispanic women in border counties, and Hispanic women in the border states had higher rates than did non-Hispanic women in nonborder states. In contrast, cervical cancer incidence rates among black women in the border counties were lower than those among black women in the nonborder states. Among white women, however, incidence rates were higher among those in nonborder states. Differences in cervical cancer incidence rates by geographic locality were also evident by age, urban/rural residence, migration from outside the United States, and stage of disease.
CONCLUSIONS. Disparities in cervical cancer incidence in the US-Mexico border counties, when the incidence is compared with that of other counties and geographic regions, are evident. Of particular concern are the higher rates of latestage cervical cancer diagnosed among women in the border states, especially because such cervical cancer is preventable. Cancer 2008;113(10 suppl):2964– 73. Published 2008 by the American Cancer Society.*
KEYWORDS: cervical cancer, healthcare access, Hispanics, incidence. Address for reprints: Steven S. Coughlin, PhD, Environmental Epidemiology Service (135), Department of Veterans Affairs, 810 Vermont Ave., NW, Washington, DC 20420; Fax: (202) 266-4656; E-mail:
[email protected] *This article is a US Government work and, as such, is in the public domain in the United States of America.
Published 2008 by the American Cancer Society* DOI 10.1002/cncr.23748 Published online 3 November 2008 in Wiley InterScience (www.interscience.wiley.com).
Received April 14, 2008; revision received June 2, 2008; accepted June 6, 2008.
Cervical Cancer at the US-Mexico Border/Coughlin et al
T
he US-Mexico border region extends about 2000 miles, from the Pacific Ocean to the Gulf of Mexico. It includes some of the poorest counties in the United States.1 More than a third of US border families live at or below the poverty line, and the unemployment rate is 2.5 to 3.0 times higher than in the rest of the United States. Lack of access to healthcare is an important problem in the border region.1 Other problems include an uneven distribution of physicians and other healthcare providers, a shortage of bilingual health information, and a lack of culturally sensitive systems of care. The public health concerns of the US-Mexico border region include relatively low cervical cancer screening rates, especially among older Hispanic women, and relatively high death rates from cervical cancer.2–5 Cervical cancer mortality rates have declined in the United States, but little information has been available about the incidence of the disease in the US-Mexico border region, where poverty, lower education, and inadequate access to healthcare services are prevalent social problems. A recent report about cervical cancer in Texas from 1999 to 2003 suggested that some Texas women may be more likely than others to develop cervical cancer, depending on where they live.6 Hispanic women living in 32 counties along the Texas-Mexico border had a 19% higher cervical cancer mortality rate than Hispanic women living in nonborder areas. Among women in Texas who were diagnosed with cervical cancer, only 40.2% of Hispanic women in the border counties had earlystage disease, compared with 49.3% of nonborder Hispanic women. White women in rural counties of Texas had a 27% higher cervical cancer incidence rate than white women residing in urban counties of the state. An analysis of cervical cancer incidence data from California over the period 1988 to 2002 found some variation in incidence rates by race/ ethnicity and geographic locality.7 However, the incidence of cervical cancer in California counties adjacent to the US-Mexico border was not uniformly higher than in other counties in the state. To help clarify these relationships, we examined cervical cancer incidence among women in the USMexico border counties during the years 1998 to 2003 by age, race, Hispanic ethnicity, education, poverty, urban/suburban/rural residence, stage, histology, and the percentage of the county population who had migrated to the United States. Cervical cancer incidence among women in US-Mexico border counties was compared with the incidence in other counties in the 4 border states (California, Arizona, New Mexico, and Texas), and also with the incidence in nonborder states. The current analysis differs from
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that of other articles included in this Supplement in that the focus is on cervical cancer incidence and stage at diagnosis in the US-Mexico border region, the residents of which are disproportionately impacted by cervical cancer.
MATERIALS AND METHODS The databases used for all analyses were 1998 to 2003 data from the National Program of Cancer Registries (NPCR) and National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) program.8 The use of NPCR and SEER data allowed for a more comprehensive examination of cervical cancer incidence in border and nonborder counties of border states. Analyses were limited to 37 registries that met the US Cancer Statistics Publication Standard for data quality (USCS Publication Standard). Four of these registries (hereafter referred to as US-Mexico border states) were the state central registries for California, Arizona, New Mexico, and Texas. California is part of SEER and the NPCR, New Mexico is a SEER state, and Arizona and Texas are included in the NPCR. To provide the maximum number of cases with high-quality data, we used data for the years 1998 to 2003 for California, New Mexico, and Texas, whereas data for Arizona were limited to 1998 to 2002 (the years that met the USCS Publication Standard). The remaining 33 registries (hereafter referred to as those for nonborder states) included the central registries for the District of Columbia and 32 states (Alabama, Alaska, Arkansas, Colorado, Connecticut, Delaware, Florida, Idaho, Indiana, Iowa, Kansas, Kentucky, Louisiana, Maine, Massachusetts, Michigan, Missouri, Montana, Nebraska, New Jersey, New York, Ohio, Oklahoma, Oregon, Pennsylvania, Rhode Island, South Carolina, Utah, Vermont, Washington, West Virginia, and Wisconsin). Each of the nonborder states had high-quality data available from 1998 to 2003. Several different definitions of US-Mexico ‘‘border counties’’ have been proposed.9 For example, in Texas, variations have included 14 counties with boundaries that touch the US-Mexico border at some point; 32 counties in a Health Services Resources Administration (HRSA) border region, where ‘‘border counties’’ are defined as those counties where any part is within the 100-km (62.14 miles) region north of the US border with Mexico; and 43 counties in a South Texas border region.10 The HRSA definition of the border region presents some problems with certain counties; in California, for example, only a small portion of Riverside
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CANCER Supplement
November 15, 2008 / Volume 113 / Number 10
County is included in the 100-km region used for the HRSA definition. To reduce misclassification of geographic residence, we used the state definition of border counties for this analysis, rather than the HRSA definition, although in New Mexico and Texas the state definition and HRSA definition are identical. Table 1 provides a list of the 44 counties that the 4 border states (California, Arizona, New Mexico, Texas) defined as ‘‘border counties’’ and that we used for this study. The locations of these counties, and their population density, are shown in Figure 1. In this figure, the population density is derived from the LandScan world population database (LandScan 2002; Oak Ridge National Laboratory, Oak Ridge, Tenn),11 which has a grid cell size of 30 arc seconds (about 1 km2). High-density areas have between 2000 and 7000 people per square kilometer; low-density TABLE 1 Counties Identified as "Border Counties" by Border States (Arizona, California, New Mexico, and Texas) Border State
Border Counties
Arizona California New Mexico Texas
4 counties: Cochise, Pima, Santa Cruz, Yuma 2 counties: San Diego, Imperial 6 counties: Dona Ana, Grant, Hidalgo, Luna, Otero, Sierra 32 counties: Brewster, Brooks, Cameron, Crockett, Culberson, Dimmit, Duval, Edwards, El Paso, Frio, Hidalgo, Hudspeth, Jeff Davis, Jim Hogg, Kenedy, Kinney, La Salle, Maverick, McMullen, Pecos, Presidio, Real, Reeves, Starr, Sutton, Terrell, Uvalde, Val Verde, Webb, Willacy, Zapata, Zavala 44 counties
Total
areas have between 0 and 10 people per square kilometer. Results were aggregated for the purpose of examining the 44 counties in Table 1 as a single entity, as compared with the aggregated results for the remaining 316 counties in the border states. In addition, comparisons were made with aggregated results for the nonborder states as a single entity. Counties were categorized as ‘‘urban,’’ ‘‘suburban,’’ or ‘‘rural,’’ using the US Department of Agriculture 2003 Rural-Urban Continuum Codes.12 Codes 1-3 correspond to ‘‘urban’’ (metropolitan) counties (including metropolitan areas with populations of about 250,000 to greater than 1 million); codes 4-5 correspond to predominately suburban populations of 20,000 or greater, but less than 250,000; and codes 6-9 correspond to rural populations and small towns of up to 19,999. The analysis was limited to microscopically confirmed cases of invasive cervical carcinomas, as defined earlier (International Classification of Diseases for Oncology-3 8010-8671 and 8940-8941).13 The stage at diagnosis was categorized by using SEER Summary Stage 1977 for cancers from 1998 to 2000, and SEER Summary Stage 2000 for cancers from 2001 to 2003. Data for the 2 staging systems were combined, because the differences observed in comparative analyses were minimal.14 To minimize problems with small numbers, we combined the regional stage with the distant stage, resulting in 3 groups: early stage (localized),1 late stage,2 and
FIGURE 1. US-Mexico border counties and population density are shown for the United States, 2002.
Cervical Cancer at the US-Mexico Border/Coughlin et al
unknown stage/unstaged.3 Analysis of histology was limited to identification of percentages, rates (with 95% confidence intervals for those rates), and rate ratios by region for squamous cell carcinomas, adenocarcinomas, adenosquamous/glassy cell, small cell/neuroendocrine, and other/unspecified carcinomas. We examined invasive cervical cancer incidence rates in the US-Mexico border counties by age categories, race (white, black, Asian/Pacific Islander), Hispanic ethnicity, urban/suburban/rural residence, educational attainment (percentage of county population aged 25 years or more who did not graduate from high school), poverty (percentage of persons in the county below the poverty level), the percentage of persons in a county living in the same house for over 5 years (as a potential marker for individuals more likely to have an established physician to make screening recommendations and also to have an established social network to encourage screening), and the percentage of persons who moved from outside the United States into the county. In this analysis, Hispanic ethnicity was not mutually exclusive of race.13 The categories for education, poverty, no migration, and moved from outside the United States were calculated by dividing the percentage for each variable into 2 groups. The dividing point for creating the 2 groups was the median percentage for the border counties for that variable. Age-specific rates, direct age-adjusted incidence rates, and rate ratios were calculated in SEER Stat (National Cancer Institute, Bethesday, Md) using the 2000 US standard population with 19 age groups, and expressed per 100,000 females. The 19 age groups were: 5 y 59.16% >59.17% Moved from outside the US 2.81% >2.82% Age-adjusted rate
Nonborder States (Reference Group)
Other Counties in Border States
Cases
Rate
Rate Ratio (95% CI)
Cases
Rate
Rate Ratio (95% CI)
Cases
Rate
Rate Ratio
1,583 101 92
9.5{ 10.5 11.5
1.1 (1.1-1.2) 1.2 (0.9-1.4) 1.2 (0.9-1.5)
13,753 561 687
9.2{ 10.0{ 9.5
1.1 (1.1-1.1) 1.1 (1.0-1.2) 1.0 (0.9-1.1)
35,157 3,500 5,300
8.5 9.0 9.7
1.0 1.0 1.0
1,621 28 91
9.8{ 5.1{ 9.1
1.2 (1.2-1.3) 0.4 (0.3-0.6) 1.1 (0.8-1.3)
12,177 1,421 1,097
9.3{ 10.6{ 8.1
1.1 (1.1-1.2) 0.8 (0.8-0.9) 1.0 (0.9-1.0)
34,842 7,083 966
8.1 12.8 8.5
1.0 1.0 1.0
1,048 728
13.9 7.0{
1.1 (1.0-1.1) 0.8 (0.8-0.9)
5,118 9,883
14.8{ 7.9{
1.1 (1.1-1.2) 0.9 (0.9-1.0)
3,826 40,206
13.2 8.4
1.0 1.0
1,250 526
8.8 12.9
1.0 (1.0-1.1) 1.0 (0.9-1.2)
14,994 k
9.3{ k
1.1 (1.1-1.1) k
43,633 324
8.6 12.4
1.0 1.0
1,250 526
8.8 12.5
1.0 (1.0-1.1) 1.0 (0.9-1.1)
14,904 97
9.3{ 8.9{
1.1 (1.1-1.1) 0.7 (0.6-0.9)
42,583 1,374
8.6 12.6
1.0 1.0
1,504 272
9.3{ 12.8{
1.1 (1.0-1.1) 1.4 (1.3-1.6)
14,580 421
9.3{ 9.3
1.1 (1.1-1.1) 1.0 (0.9-1.1)
26,631 17,326
8.5 8.9
1.0 1.0
71 1,705 1,776
12.0{ 9.6 9.7{
1.4 (1.1-1.8) 1.0 (1.0-1.1) 1.1 (1.1-1.2)
3,605 11,396 15,001
9.2{ 9.3 9.3{
1.1 (1.0-1.1) 1.0 (1.0-1.0) 1.1 (1.0-1.1)
30,221 13,736 44,032
8.5 9.1 8.7
1.0 1.0 1.0
CI indicates confidence interval (calculated with Tiwari et al16 modification). Percentages indicate percent of total cases for that subcategory. Percentage
