PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of pubhealthrepLink to Publisher's site
 
Public Health Rep. 2011 Nov-Dec; 126(6): 806–815.
PMCID: PMC3185316
Breast and Cervical Cancer Screening Patterns Among American Indian Women at IHS Clinics in Montana and Wyoming
Robin Taylor Wilson, PhD,a Jennifer Giroux, MD, MPH,b Kathryn Rita Kasicky, MD,c Bethany Hemlock Fatupaito, MPH,d Eric C. Wood, PhD,e Renee Crichlow, MD,f Neil A. Sun Rhodes, MD, MPH,g Jennifer Tingueley, MD, MPH,h Andrea Walling,i Kathryn Langwell, MA,j and Nathaniel Cobb, MDk
aPennsylvania State University College of Medicine and Penn State Hershey Cancer Institute, Hershey, PA
bIndian Health Service (IHS), Division of Epidemiology and Disease Prevention, Aberdeen Area IHS, and Great Plains Tribal Chairmen's Health Board, Rapid City, SD
cWake Forest School of Medicine, Winston-Salem, NC
dMontana Wyoming Tribal Leaders Council, Billings, MT
eU.S. Geological Survey, Sioux Falls, SD
fUniversity of Minnesota, Department of Family and Community Medicine, Minneapolis, MN
gBrowning Community Hospital, Indian Health Service, Browning, MT
hCenter for Family Medicine, Sioux Falls, SD
iUniversity of Washington Family Medicine Residency Program, Billings, MT
jSundance Research Institute, Sundance, WY
kIndian Health Service, National Epidemiology and Disease Prevention, Albuquerque, NM
Address correspondence to: Robin Taylor Wilson, PhD, Pennsylvania State University College of Medicine, Department of Public Health Sciences, Division of Epidemiology, 500 University Dr., Mail Code CH69, Hershey, PA 17033, Phone: 717-531-7178, Fax: 717-531-5779, ; rwilson/at/psu.edu.
Objectives
We investigated factors associated with primary and secondary breast and cervical cancer screening among American Indian (AI) women receiving care from the Indian Health Service (IHS) in Montana and Wyoming.
Methods
Rates of primary screening (i.e., screening without evidence of a prior abnormal) and secondary screening during a three-year period (2004–2006) were determined in an age- and clinic-stratified random sample of 1,094 women at six IHS units through medical record review.
Results
Three-year mammography prevalence rates among AI women aged ≥45 years were 37.7% (95% confidence interval [CI] 34.1, 41.3) for primary and 58.7% (95% CI 43.9, 73.5) for secondary screening. Among women aged ≥18 years, three-year Pap test prevalence rates were 37.8% (95% CI 34.9, 40.6) for primary and 53.2% (95% CI 46.0, 60.4) for secondary screening. Primary mammography screening was positively associated with number of visits and receiving care at an IHS hospital (both p<0.001). Primary Pap test screening was inversely associated with age and positively associated with the number of patient visits (both p<0.001). Secondary mammography screening was inversely associated with driving distance to an IHS facility (p=0.035).
Conclusion
Our results are consistent with other surveys among AI women, which report that Healthy People 2010 goals for breast (90%) and cervical (70%) cancer screening have not been met. Improvements in breast and cervical cancer screening among AI women attending IHS facilities are needed.
There are significant regional differences in breast and cervical cancer incidence among American Indian/Alaska Native (AI/AN) women in the United States. Among AI/AN women, American Indian (AI) women living in the Northern Plains region have the second highest incidence of both breast cancer (115.9 per 100,000 population) and cervical cancer (12.5 per 100,000 population).1,2 The Northern Plains region, as defined by the National Institutes of Health, includes the Aberdeen, Bemidji, and Billings Areas of the Indian Health Service (IHS) that encompass several states (Illinois, Indiana, Iowa, Michigan, Minnesota, Montana, Nebraska, South Dakota, Wisconsin, and Wyoming). In the U.S. overall, compared with non-Hispanic white women, AI/AN women have a lower incidence of breast cancer, a higher incidence of cervical cancer, and a risk of death that is 50%–80% higher once diagnosed with cancer.1,35 For both cancer sites, AI/AN women are more likely than non-Hispanic white women to be diagnosed with a late-stage cancer.1,47
In the Northern Plains, AI women have an incidence of metastatic cervical cancer that is six times higher than for non-Hispanic white women in the same region.5 Rates of screening among women in Montana and Wyoming without a prior abnormal result (primary screening) and with a prior abnormal result (secondary screening) have not been described.
The purpose of this study was to estimate the three-year prevalence of primary and secondary mammography and Papanicolaou (Pap) test screening for breast and cervical cancer, respectively, and to determine factors associated with primary cancer screening among AI women receiving care from the IHS in Montana and Wyoming.
Study population and sampling frame
The study population consisted of AI women aged ≥18 years who received care at IHS facilities on five reservations in Montana and one reservation in Wyoming. These reservations serve a clinic population of approximately 6,554 women aged ≥45 years and 9,980 women aged 18–44 years.8 Each reservation contains one IHS service unit that provides administrative oversight of one or more IHS clinic and/or hospital locations. A stratified random sampling was conducted by service unit (n=6 service units) and age group (18–44, 45–64, and ≥65 years of age). The study was powered to determine the prevalence of screening (610%) within each age group and service unit. The Breast Cancer Screening Study (BCSS) sample is a subset of the Cervical Cancer Screening Study (CCSS). Compared with U.S. Census Bureau population estimates, the IHS active user population was approximately 75% (16,534/22,136) of AI women aged ≥20 years in Montana and Wyoming at the time of this study.9
Women who were aged ≥18 years during the study period (January 1, 2004, to December 31, 2006), with at least two clinic visits (excluding visits to the emergency room) to the same facility during a 78-month period (between January 1, 2001, and July 1, 2007), were included in the study. Women having a mastectomy and/or hysterectomy prior to January 1, 2004, were excluded from the analysis of breast cancer screening and cervical cancer screening.
Chart review and data entry
We reviewed electronic and paper copies of charts at all hospitals and clinics at the participating reservations. A standardized data-collection instrument was used to record the following: age, percent AI blood quantum, ZIP code of residence, facility type (hospital vs. clinic), date of last visit, purpose of last visit (e.g., preventive, follow-up for chronic disease, inpatient stay, or urgent care), total number of medical visits to the health facility during the study period (excluding dental and pharmacy visits), hysterectomy, mastectomy, dates of all mammograms and Pap tests during the study period, and the reason for the mammogram and/or Pap test (e.g., screening, diagnosis of symptoms, or abnormal follow-up).
The study period for determination of mammogram, Pap test, and number of visits was January 1, 2004, to December 31, 2006. For medical history prior to the study period (i.e., prior hysterectomy, prior mastectomy, prior abnormal mammogram result, and prior abnormal Pap test result), we reviewed all available chart and electronic records at each IHS facility. A 10% subsample of abstraction instruments was verified for quality assurance of electronic data entry, and no errors in data entry were found.
Distance to nearest IHS facility and mammogram
Lists of facilities approved to provide mammography were obtained for 2004–2006 from the U.S. Food and Drug Administration. IHS facilities included hospitals and outpatient clinics. All facilities were mapped using ArcGIS 9.0.10 Because the majority of women did not have street addresses, the distances to the nearest mammography facility and the nearest IHS facility for each participant were calculated using the ZIP code centroid of residence (i.e., the geometric center of the ZIP code area).
Statistical analysis
We stratified the analysis by type of screening (breast or cervical) and also by history of a previous abnormal Pap test or mammogram. We calculated differences in categorical and continuous bivariate statistics using Chi-square and t-test statistics, respectively. We used the Wilcoxon rank-sum test to determine the statistical significance of differences in median age. To adjust for the independent effects of several factors, we conducted multivariable analyses using logistic regression. All p-values were two-sided, and p≤0.05 was considered statistically significant. We used the Hosmer-Lemeshow (H-L) goodness-of-fit test statistic to determine the fit of the multivariable models. We considered p≤0.15 to indicate a significant lack of fit.
We identified 1,278 women aged ≥18 years (723 women aged ≥45 years) meeting the study inclusion criteria at the six reservations in Montana and Wyoming. Excluded from the respective analyses were 16 women with a prior mastectomy, 177 women with a prior hysterectomy (including three women with a supracervical hysterectomy), and seven women with both a prior mastectomy and hysterectomy, resulting in a total study population of 1,094 women for the CCSS (i.e., women aged ≥18 years) and 700 women for the BCSS (i.e., women aged ≥45 years).
The demographic characteristics of the study population are summarized in Table 1. Women in the BCSS had a mean age of 60.5 years, with 31.6% having a recorded blood quantum of ≥50%, 45.7% receiving care through an IHS hospital, and 54.3% receiving care through an IHS clinic. Women in this study were on average 13.1 miles (range: 0.0–176.3) from the nearest IHS facility and 16.1 miles (range: 0.0–79.9) from the nearest mammography facility. Women in the CCSS had a median age of 45.0 years, 34.5% had a recorded blood quantum of ≥50%, 45.8% received care primarily at an IHS hospital, and 54.2% received care primarily at an IHS clinic. The average distance to the nearest IHS facility was 12.7 miles (range: 0.0–176.3).
Table 1.
Table 1.
Characteristics of American Indian women ≥18 years of age receiving care from the IHS in Montana and Wyoming, 2004–2006
Among BCSS women aged ≥45 years, 37.7% (95% CI 34.1, 41.3) had a mammogram during the three-year study period, of whom 8.0% had an abnormal result (Table 2). Among women receiving a mammogram during the three-year period, the reason for receiving a mammogram was predominantly screening (82.2%), followed by prior abnormal mammogram (5.3%), symptoms (3.8%), or baseline mammogram (3.4%). Among women with a prior abnormal mammogram, 58.7% received a mammogram during the three-year study period.
Table 2.
Table 2.
Prevalence of breast and cervical cancer screening among American Indian women ≥18 years of age receiving care from the Indian Health Service: Montana and Wyoming, 2004–2006
Among CCSS women aged ≥18 years, the prevalence of Pap test screening was 37.8% (95% CI 34.9, 40.6), of whom 6.3% had an abnormal Pap result. The predominant reason for a Pap test was screening (91.5%). A total of 188 women (17.2% of the total study sample) had documentation of a prior abnormal Pap test, of whom 53.2% received a Pap test. During the three-year study period, 7.4% of women were recorded as having a referral for a Pap test (Table 2).
Prevalence of screening by prior status (normal vs. abnormal)
In bivariate statistics among women without a prior history of an abnormal mammogram, the prevalence of mammogram was higher among women with blood quantum recorded as ≥50% (44.1%, p=0.004), those receiving care predominantly from hospitals (44.1%, p<0.001), and those having a greater number of visits (55.3% of those having ≥26 visits, p<0.001) (Table 3). Distance to mammography was also associated with the prevalence of screening; screening was greatest among women living in a town with a mammography facility (40.0%) and lowest among women residing 1–14 miles away from a mammography facility (27.9%, p=0.019). There was no association between the prevalence of mammography and distance to the nearest IHS facility.
Table 3.
Table 3.
Three-year prevalence of mammogram according to prior abnormal mammogram status among American Indian women ≥45 years of age receiving care from the IHS: Montana and Wyoming, 2004–2006
Among women with a prior abnormal mammogram, there was a statistically significant association with residing nearest an IHS facility: 70.0% of the women were screened at a facility in the same town, 66.7% of the women were screened at a facility 1–14 miles away, and 28.6% of women lived 15–29 miles from an IHS facility (p=0.035) (Table 3). In contrast with women without a prior abnormal mammogram, among women with a prior abnormal mammogram, there was no association with blood quantum, type of IHS facility, number of visits, or distance to the nearest mammography facility.
Cervical cancer screening among women without a prior abnormal Pap test was inversely associated with age (p<0.001) (Table 4). Among women aged ≥65 years, 19.3% received a Pap test during the three-year period compared with 41.2% of women aged 18–44 years. In addition, cervical cancer screening was also positively associated with the total number of visits, with a higher prevalence of screening among women having a greater number of visits (p<0.001), and inversely associated with the distance to the nearest IHS facility: more than 30.0% of women living in the same town or <30 miles from a facility received a Pap test during the three-year period compared with only 21.4% of those living ≥30 miles away (p=0.012).
Table 4.
Table 4.
Three-year prevalence of Pap test according to prior abnormal Pap test status among American Indian women ≥18 years of age receiving care from the IHS: Montana and Wyoming, 2004–2006
Among women with a prior abnormal Pap test, 45.0% of women aged ≥65 years received a Pap test during the three-year period compared with 52.8% of women aged 18–44 years, although this difference was not statistically significant (Table 4). As with women who did not have a prior abnormal Pap test, the prevalence of receiving a Pap test during the three-year period was associated with the number of visits (p<0.001). Women with ≤2 visits during the three-year period had an 18.4% prevalence of Pap test, compared with 69.8% of women with 10–25 visits and 68.3% of women with ≥26 visits during the three-year period. Unlike women without a prior abnormal Pap test, there was no association with distance to the nearest IHS facility among women with a prior abnormal Pap test.
Adjusted odds of not receiving screening
Among women aged ≥45 years without a prior abnormal mammogram, there was an independent association between the number of visits (p<0.001) and type of facility, adjusting for age, blood quantum, and distance to mammography screening (H-L goodness-of-fit test, p=0.296). The likelihood of receiving a mammography was inversely associated with the number of visits during the three-year period, with the highest risk of not being screened among women with ≤2 visits during the study period (OR=16.9, 95% CI 8.6, 33.3). Women who received their care primarily at an IHS clinic (OR=1.8, 95% CI 1.2, 2.8) were more likely not to have been screened compared with women receiving care primarily at an IHS hospital. After adjusting using multiple logistic regression, there was no longer a statistically significant association with blood quantum (Table 5).
Table 5.
Table 5.
Multivariable odds of not receiving cervical or breast cancer screening without a prior abnormal Pap test or mammogram for American Indian women ≥18 years of age receiving care from the IHS: Montana and Wyoming, 2004-–2006
Among women aged ≥18 years without a prior abnormal Pap test, there was an independent association between age (p<0.001) and number of visits (p<0.001), adjusting for blood quantum, type of facility, and distance to screening (H-L goodness-of-fit test, p=0.165) (Table 5). Women who were aged ≥65 years were 5.7 times (95% CI 3.5, 9.3) more likely not to have received a Pap test during the three-year period compared with women aged 18–44 years. The risk of not receiving a Pap test was highest among women with ≤2 visits during the three-year period (OR=20.8, 95% CI 11.9, 36.4), and decreased monotonically with a greater number of visits (3–9 visits: OR=4.9, 95% CI 3.1, 7.6; 10–25 visits: OR=1.9, 95% CI 1.3, 2.9). After adjusting using multiple logistic regression, there was no significant association with blood quantum, type of IHS facility, or distance to the nearest IHS facility.
Primary cancer screening
Healthy People 2010 (now Healthy People 2020) objectives were to achieve Pap tests for at least 90% (now 93%) of women aged ≥18 years within the preceding three years and a mammogram among 70% (now 81%) of women aged ≥40 years within the preceding two years.11
Our results are consistent with reports that find AI women have among the lowest breast and cervical cancer screening rates in the United States.1216 The prevalence of mammography and Pap tests identified by our study of existing IHS patient records is similar to a reservation-based survey in the Northern Plains of self-reported breast (51%) or cervical (50%) cancer screening,17 but roughly half that of estimates based on a telephone survey.13 There are several reasons why telephone surveys may estimate a higher prevalence of cancer screening among AI women, including the comparatively lower percentage of AI households in this region with landline telephones (approximately 30%–60%);18,19 greater health status and preventive health behaviors among members of households with phones, compared with those without phones;18 response bias (i.e., women who respond to telephone surveys may also be more likely than women who do not respond to telephone surveys to have been screened);20 inaccurate recall during the time period in question;21,22 and social desirability bias (i.e., respondents report the most socially desirable answer to questions and may, therefore, overreport a history of cancer screening).2325 Compared with medical records, self-reported cancer screening prevalence may be inflated by as much as 20 percentage points—a phenomenon that appears to be independent of race/ethnicity.21,26 Finally, it should be noted that, although we identified women with at least two nonemergency clinic visits to the same IHS facility, our medical record review may have underestimated the true prevalence of cancer screening because care received at non-IHS hospitals and clinics was not captured in our dataset.
The mammogram prevalence rate reported in this study is consistent with mammogram prevalence rates among Medicaid recipients (31.7%–38.5% for two-year rates),27,28 uninsured women (32.2% for annual rates),20 women reporting having no personal health-care provider (45.4% for two-year rates),29 AI women in the Southwest (44.0% for two-year rates),30 and AI women reporting perceived medical discrimination (33.9% for annual rates).31 Chlebowski et al. reported in 2005 significantly lower breast cancer screening rates among AI women enrolled in the Women's Health Initiative.12 Similarly, in a cohort of low-income women with breast cancer receiving care through California's Breast and Cervical Cancer Treatment Program, Thind et al. reported in 2009 that 64% of breast cancers were found as a result of symptomatic presentation and not through mammography screening.32 In a case-series review at an urban IHS hospital, Tillman and colleagues reported that 79% of AI women with breast cancer first presented with physical symptoms and/or a palpable mass on initial exam.33
Pap test prevalence rates found by this study were similar to those found among Medicaid recipients (31.6% for three-year results)27 and uninsured women (42.2% for annual results).20 A 2006 Government Performance and Results Act internal review, comprising the same IHS facilities used in this study, identified a 58% prevalence of Pap tests among women aged 22–64 years with at least two visits to the same facility within the past year (Personal communication, Diane Jeanotte, IHS Billings Area, October 2006). Despite the differences in estimates across studies, however, nearly all studies found that screening rates among AI women were lower than most other racial/ethnic groups and have not met Healthy People 2010 goals.
Secondary cancer screening
Among women with an abnormal mammogram or Pap test result, our study suggests that more than 40% are not receiving annual follow-up screening. Fewer than half of the women receiving services through the National Breast and Cervical Cancer Early Detection Program were followed according to established guidelines for management of equivocal or mildly abnormal cervical cytology.34
Referral rates
Existing IHS hospital records do not indicate high rates of referral for either mammogram (1.3%) or Pap test (7.4%). It is possible that we did not fully capture referrals that were made but not recorded in the electronic or paper chart. During the time period of this study, electronic referrals were used at some IHS facilities, while referrals were tracked by hard copy at other facilities. In the U.S., rates of referral among women who have not been screened are generally low. Coughlin et al. reported that among women with a doctor visit in the last year but no recent Pap test, 86.7% reported that their doctor had not recommended a Pap test.35 Using the National Health Interview Survey, Sabatino et al. reported in 2006 that 71% of recently unscreened women seen by a health-care provider in the prior year reported no recommendation for mammography.36
Age and cancer screening
Among young (aged <30 years) and older (aged ≥65 years) age groups, AI women in the Northern Plains have the highest incidence of cervical cancer in the U.S. Notably, a recent national cancer surveillance project reported that cervical cancer incidence rates among AI women in the U.S. are highest in those aged ≥65 years.5 The comparatively low screening rates reported in our study (19.3% of women aged ≥65 years vs. 41.2% of women aged 18–44 years) suggest that the higher incidence rates in this age group are related to lower rates of Pap test screening.
Tobacco use and high parity have been associated with a higher risk of cervical cancer among women infected with human papillomavirus.37 Among AI women in the Northern Plains, the prevalence of current smokers is 37.7%, which is considerably higher than the prevalence reported for non-Hispanic white women (22.2%).13 The combination of higher tobacco use and lower screening rates among older women may also explain the higher incidence and mortality from late-stage cervical cancer among AI women in the Northern Plains.
Distance to screening facility
Our study did not find a significant association between distance from participant residence to the nearest screening facility and likelihood of receiving primary cancer screening. This finding is consistent with an analysis of Surveillance, Epidemiology, and End Results Program (known as SEER) and Medicare linked data in California, which reported that the number of mammography facilities per 1,000 women in each residential area was not as important as other factors, including a higher likelihood of screening among AI women who lived in areas with a higher AI population density.38 It is likely that distance still influences decisions about seeking cancer screening, as it may require separate visits, particularly for follow-up of abnormal results. For example, in this study, secondary mammography screening was inversely associated with driving distance to IHS facility (p=0.035).
Limitations
This study had several limitations. First, because our study inclusion criteria required two visits to the same facility during the six-year period prior to the start of the study, the women selected for this study may not be representative of women who did not seek medical care during the same time period. Second, we were unable to account for care provided at other non-IHS locations or for migration of women in and out of the study population during the study period. Therefore, breast and cervical cancer screenings given in other IHS areas and through private providers were not accounted for in this study.
Third, because the majority of AI women in this study lived at rural route addresses and did not have street addresses, it is likely that the distance to the closest IHS hospital/clinic and mammography facility determined using the ZIP code centroid did not accurately estimate the true distance. However, because we analyzed distance by categories of distance, if there was a substantial influence of distance upon screening in this study population, one would have expected to see a difference between residing in the same town and living, for example, 30 or more miles away. In addition, this study did not account for the medical practice environment,39,40 physician characteristics,41,42 or physician-patient relationships29 that may influence recommendations for patient screening, as well as other patient characteristics (e.g., family history of breast or cervical cancer, patient knowledge regarding cancer screening, or willingness to accept care from a male provider)43 and community characteristics that may influence the likelihood of receiving cancer screening services.35,44
Another limitation of our study was that the Compacted Tribes in this region, which control their own medical care apart from IHS, were not represented due to time limitations on data collection. Finally, this study had no information regarding the status of initiation of sexual activity; cervical cancer screening guidelines recommend the initiation of screening among women after the initiation of sexual activity.
Strengths
This study also had several strengths, including (1) its use of a representative sample of women receiving care at the Billings Area IHS, (2) investigation of characteristics associated with both primary and secondary cancer screening, and (3) being one of a few studies of breast and cervical cancer among AI women that did not rely upon self-reported screening behavior, but identified screening procedures through existing hospital and clinic records during a three-year period.
CONCLUSION
Our results are consistent with other surveys that indicate Healthy People 2010 goals for breast and cervical cancer have not been met for AI women. Improvements in breast and cervical cancer screening among AI women attending IHS facilities are needed. Randomized studies may help clarify whether improvement efforts should best be targeted to clinicians, patients, and/or communities.
Acknowledgments
The authors thank the following individuals for their assistance in this study: Diane Jeanotte, Terry Dennis, Kris Four Star, Desiree Bell, Helen Butterfly, Margaret Cooper, and Teresa Red Eagle from the Indian Health Service (IHS); Anna LaFountain from the Montana Family Medicine Residency Program; Gary A. Chase (in memoriam), Vernon Chinchilli, and Kathleen Hay from the Pennsylvania State University (Penn State); Craig Chandler, Arlana Farwell, Cheryl Nagel, Olivia Hemlock, and Chantelle Big Back from the Rocky Mountain Tribal Epidemiology Center; Sue Miller from the State of Montana; and Joe Grandpre and MaryAnne Purtzer from the State of Wyoming.
Footnotes
Approval for the study was received by the participating Tribes in Montana and Wyoming, the Billings Area IHS Institutional Review Board (IRB), the Wyoming State Department of Health IRB, and the Penn State IRB.
This work was supported by Agency for Healthcare Research and Quality Grant #02 R24HS014034-04 awarded to the Montana Wyoming Tribal Leaders Council. The findings and conclusions in this article are those of the authors and do not necessarily represent the official position of IHS.
1. Wingo PA, King J, Swan J, Coughlin SS, Kaur JS, Erb-Alvarez JA, et al. Breast cancer incidence among American Indian and Alaska Native women: US, 1999-2004. Cancer. 2008;113(5 Suppl):1191–202. [PubMed]
2. Wiggins CL, Espey DK, Wingo PA, Kaur JS, Wilson RT, Swan J, et al. Cancer among American Indians and Alaska Natives in the United States, 1999-2004. Cancer. 2008;113(5 Suppl):1142–52. [PubMed]
3. Espey DK, Wu XC, Swan J, Wiggins C, Jim MA, Ward E, et al. Annual report to the nation on the status of cancer, 1975-2004, featuring cancer in American Indians and Alaska Natives. Cancer. 2007;110:2119–52. [PubMed]
4. Clegg LX, Li FP, Hankey BF, Chu K, Edwards BK. Cancer survival among US whites and minorities: a SEER (Surveillance, Epidemiology, and End Results) program population-based study. Arch Intern Med. 2002;162:1985–93. [PubMed]
5. Becker TM, Espey DK, Lawson HW, Saraiya M, Jim MA, Waxman AG. Regional differences in cervical cancer incidence among American Indians and Alaska Natives, 1999-2004. Cancer. 2008;113(5 Suppl):1234–43. [PubMed]
6. Dennis TD. Cancer stage at diagnosis, treatment, and survival among American Indians and non-American Indians in Montana. Cancer. 2000;89:181–6. [PubMed]
7. Leman RF, Espey D, Cobb N. Invasive cervical cancer among American Indian women in the Northern Plains, 1994-1998: incidence, mortality, and missed opportunities. Public Health Rep. 2005;120:283–7. [PMC free article] [PubMed]
8. Department of Health and Human Services (US), Indian Health Service, Billings Area. IHS and Billings Area user population report: fiscal year 2006. Billings (MT): IHS; 2006.
9. Census Bureau (US) 2005-2009 American Community Survey 5-year estimates. Washington: Census Bureau; 2011.
10. ESRI. ArcGIS: Version 9.0. Redlands (CA): ESRI; 2004.
11. Department of Health and Human Services (US) Healthy People 2010 objectives: cancer. [cited 2011 Jul 13]. Available from: URL: http://www.healthypeople.gov/2010/Data/midcourse/html/focusareas/FA03Objectives.htm.
12. Chlebowski RT, Chen Z, Anderson GL, Rohan T, Aragaki A, Lane D, et al. Ethnicity and breast cancer: factors influencing differences in incidence and outcome. J Natl Cancer Inst. 2005;97:439–48. [PubMed]
13. Steele CB, Cardinez CJ, Richardson LC, Tom-Orme L, Shaw KM. Surveillance for health behaviors of American Indians and Alaska Natives—findings from the Behavioral Risk Factor Surveillance System, 2000-2006. Cancer. 2008;113(5 Suppl):1131–41. [PubMed]
14. Denny CH, Holtzman D, Cobb N. Surveillance for health behaviors of American Indians and Alaska Natives. Findings from the Behavioral Risk Factor Surveillance System, 1997–2000. MMWR Surveill Summ. 2003;52(7):1–13. [PubMed]
15. Wampler NS, Saba L, Rahman SM, Dignan M, Voeks JH, Strzelczyk J. Factors associated with adherence to recommendations for screening mammography among American Indian women in Colorado. Ethn Dis. 2006;16:808–14. [PubMed]
16. Eberth JM, Huber JC, Jr, Rene A. Breast cancer screening practices and correlates among American Indian and Alaska Native women in California, 2003. Womens Health Issues. 2010;20:139–45. [PMC free article] [PubMed]
17. Pandhi N, Guadagnolo BA, Kanekar S, Petereit DG, Smith MA. Cancer screening in Native Americans from the Northern Plains. Am J Prev Med. 2010;38:389–95. [PMC free article] [PubMed]
18. Pearson D, Cheadle A, Wagner E, Tonsberg R, Psaty BM. Differences in sociodemographic, health status, and lifestyle characteristics among American Indians by telephone coverage. Prev Med. 1994;23:461–4. [PubMed]
19. Census Bureau (US) Statistical brief: housing of American Indians on reservations—equipment and fuels. Washington: Department of Commerce (US), Census Bureau, Economics and Statistics Administration; 1995.
20. Adams EK, Breen N, Joski PJ. Impact of the National Breast and Cervical Cancer Early Detection Program on mammography and Pap test utilization among white, Hispanic, and African American women: 1996-2000. Cancer. 2007;109(2 Suppl):348–58. [PubMed]
21. Gordon NP, Hiatt RA, Lampert DI. Concordance of self-reported data and medical record audit for six cancer screening procedures. J Natl Cancer Inst. 1993;85:566–70. [PubMed]
22. Nelson DE, Holtzman D, Bolen J, Stanwyck CA, Mack KA. Reliability and validity of measures from the Behavioral Risk Factor Surveillance System (BRFSS) Soz Praventivmed. 2001;46(Suppl 1):S3–42. [PubMed]
23. Link MW, Battaglia MP, Frankel MR, Osborn L, Mokdad AH. Address-based versus random-digit-dial surveys: comparison of key health and risk indicators. Am J Epidemiol. 2006;164:1019–25. [PubMed]
24. McHorney CA, Kosinski M, Ware JE., Jr Comparisons of the costs and quality of norms for the SF-36 health survey collected by mail versus telephone interview: results from a national survey. Med Care. 1994;32:551–67. [PubMed]
25. Kempf AM, Remington PL. New challenges for telephone survey research in the twenty-first century. Annu Rev Public Health. 2007;28:113–26. [PubMed]
26. Hiatt RA, Perez-Stable EJ, Quesenberry C, Jr, Sabogal F, Otero-Sabogal R, McPhee SJ. Agreement between self-reported early cancer detection practices and medical audits among Hispanic and non-Hispanic white health plan members in northern California. Prev Med. 1995;24:278–85. [PubMed]
27. DuBard CA, Schmid D, Yow A, Rogers AB, Lawrence WW. Recommendation for and receipt of cancer screenings among Medicaid recipients 50 years and older. Arch Intern Med. 2008;168:2014–21. [PubMed]
28. DuBard CA, Yow A, Bostrom S, Attiah E, Griffith B, Lawrence W. Racial/ethnic differences in quality of care for North Carolina Medicaid recipients. N C Med J. 2009;70:96–101. [PubMed]
29. Cardarelli R, Kurian AK, Pandya V. Having a personal healthcare provider and receipt of adequate cervical and breast cancer screening. J Am Board Fam Med. 2010;23:75–81. [PubMed]
30. Schumacher MC, Slattery ML, Lanier AP, Ma KN, Edwards S, Ferucci ED, et al. Prevalence and predictors of cancer screening among American Indian and Alaska Native people: the EARTH study. Cancer Causes Control. 2008;19:725–37. [PMC free article] [PubMed]
31. Crawley LM, Ahn DK, Winkleby MA. Perceived medical discrimination and cancer screening behaviors of racial and ethnic minority adults. Cancer Epidemiol Biomarkers Prev. 2008;17:1937–44. [PMC free article] [PubMed]
32. Thind A, Diamant A, Hoq L, Maly R. Method of detection of breast cancer in low-income women. J Womens Health (Larchmt) 2009;18:1807–11. [PMC free article] [PubMed]
33. Tillman L, Myers S, Pockaj B, Perry C, Bay RC, Al-kasspooles M. Breast cancer in Native American women treated at an urban-based Indian health referral center 1982-2003. Am J Surg. 2005;190:895–902. [PubMed]
34. Benard VB, Lawson HW, Eheman CR, Anderson C, Helsel W. Adherence to guidelines for follow-up of low-grade cytologic abnormalities among medically underserved women. Obstet Gynecol. 2005;105:1323–8. [PubMed]
35. Coughlin SS, Berkowitz Z, Hawkins NA, Tangka F. Breast and colorectal cancer screening and sources of cancer information among older women in the United States: results from the 2003 Health Information National Trends Survey [published erratum appears in Prev Chronic Dis 2007;4:A114] Prev Chronic Dis. 2007;4:A57. [PMC free article] [PubMed]
36. Sabatino SA, Burns RB, Davis RB, Phillips RS, McCarthy EP. Breast cancer risk and provider recommendation for mammography among recently unscreened women in the United States. J Gen Intern Med. 2006;21:285–91. [PMC free article] [PubMed]
37. Castellsague X, Munoz N. Chapter 3: cofactors in human papillomavirus carcinogenesis—role of parity, oral contraceptives, and tobacco smoking. J Natl Cancer Inst Monogr. 2003;31:20–8. [PubMed]
38. Mobley LR, Kuo TM, Clayton LJ, Evans WD. Mammography facilities are accessible, so why is utilization so low? Cancer Causes Control. 2009;20:1017–28. [PMC free article] [PubMed]
39. Abdel-Malek N, Chiarelli AM, Sloan M, Stewart DE, Mai V, Howlett RI. Influence of physician and patient characteristics on adherence to breast cancer screening recommendations. Eur J Cancer Prev. 2008;17:48–53. [PubMed]
40. Phillips KA, Haas JS, Liang SY, Baker LC, Tye S, Kerlikowske K, et al. Are gatekeeper requirements associated with cancer screening utilization? Health Serv Res. 2004;39:153–78. [PMC free article] [PubMed]
41. Bhosle M, Samuel S, Vosuri V, Paskett E, Balkrishnan R. Physician and patient characteristics associated with outpatient breast cancer screening recommendations in the United States: analysis of the National Ambulatory Medical Care Survey Data 1996-2004. Breast Cancer Res Treat. 2007;103:53–9. [PubMed]
42. Cassard SD, Weisman CS, Plichta SB, Johnson TL. Physician gender and women's preventive services. J Womens Health. 1997;6:199–207. [PubMed]
43. Coe K, Martin L, Nuvayestewa L, Attakai A, Papenfuss M, De Zapien JG, et al. Predictors of Pap test use among women living on the Hopi reservation. Health Care Women Int. 2007;28:764–81. [PubMed]
44. Roetzheim R, Fox SA, Leake B, Houn F. The influence of risk factors on breast carcinoma screening of Medicare-insured older women. National Cancer Institute Breast Cancer Screening Consortium. Cancer. 1996;78:2526–34. [PubMed]
Articles from Public Health Reports are provided here courtesy of
Association of Schools of Public Health