- Email: [email protected]
Racial trends in mammography rates: a population-based study
Racial trends in mammography rates: a population-based study Anees B. Chagpar, MD, MSc, MPH, Hiram C. Polk Jr., MD, and Kelly M. McMasters, MD, PhD, Louisville, Ky
Background. The rates of mammography have been declining over the last 5 years. The objective of this study was to examine racial disparities in this trend. Methods. The National Health Interview Survey is a population-based interview survey conducted annually. Caucasian and African-American women over 40 years of age who completed the cancer module of this survey in 2000 and 2005 formed the cohort of interest for this study. Results. In 2000, 69.8% of Caucasian and 64.4% of African-American women over the age of 40 had had a mammogram within the preceding 2 years. In 2005, these rates declined to 66.7% and 62.9% respectively. This decline only reached statistical significance in the Caucasian population (P = .0006 vs P = .4998). While on univariate analysis a significant difference was seen between rates of mammography in Caucasian and African-American women (P < .0001), multivariate analysis controlling for education, income, and insurance status, did not find race to be a significant independent predictor of mammography rates in each year. Conclusion. Rates of mammography are declining, particularly in Caucasian populations. While minority women are less likely to report having had a mammogram, this apparent racial disparity is explained by differences in education, income and insurance status. (Surgery 2008;144:467-72.) From the Division of Surgical Oncology, Department of Surgery, University of Louisville, Ky
BETWEEN 2001 AND 2004, there was an 8.6% reduction in the incidence of breast cancer in the United States.1 While this reduction was due, in part, to a decline in the use of hormone replacement therapy, there was also a significant decline in screening mammography and clinical breast examinations among women 40 years of age and older.2 This is particularly concerning given the proven efficacy of screening mammography in improving early detection and survival in breast cancer patients, as demonstrated by 8 randomized controlled trials.3-12 Access to medical care, and particularly preventive screening, is a politically charged issue. Economically and socially disadvantaged populations have poorer access to quality care, often leading to suboptimal outcomes. African-American patients often are disadvantaged in terms of Presented at the Society of University Surgeons Annual Meeting, held in Huntington Beach, California on February 13–15, 2008. Accepted for publication May 22, 2008. Reprint requests: Anees B. Chagpar, 315 E. Broadway, Suite #312, Louisville, KY 40202. E-mail: anees.chagpar@nortonhealthcare. org. 0039-6060/$ - see front matter Ó 2008 Mosby, Inc. All rights reserved. doi:10.1016/j.surg.2008.05.006
education, income and insurance status. Previous studies have demonstrated a survival difference between Caucasian and African-American breast cancer patients, with some studies suggesting that these differences may be attributed in part to racial disparities in terms of mammographic screening. A number of national programs, such as the Breast and Cervical Cancer Early Detection Program and the subsequent Breast and Cervical Cancer Treatment Act of 2000, have provided resources to improve screening rates nationally, particularly in African-American patients. The current downward trend in screening mammography is concerning; and it is unclear as to whether this trend has affected both Caucasians and AfricanAmericans to the same extent. Such issues are critical in the implementation of future national screening programs, and will serve to inform health policy. The objective of this study was to assess racial disparities in the recent trend in mammographic screening rates in a populationbased study. METHODS Each year the National Center for Health Statistics (NCHS), Centers for Disease Control and Prevention conducts the National Health Interview Survey (NHIS). The NHIS has been conducted annually since its inception in 1957. It is a national SURGERY 467
468 Chagpar, Polk, and McMasters
population-based face-to-face survey which is designed to be representative of the American civilian non-institutionalized population. This survey consists of 2 main components: the ‘‘Basic Module,’’ containing basic health and demographic information, and ‘‘Supplements,’’ which relate to specific areas of interest. The Basic Module, which remains largely unchanged from year to year, consists of 3 components: the Family Core, the Sample Child Core, and the Sample Adult Core. The Family Core component collects information on everyone in the family, and its sample also serves as a sampling frame for additional integrated surveys, as needed. Information collected for all family members includes household composition and socio-demographic characteristics among other factors. From each family in the NHIS, 1 sample child (if any children under age 18 are present) and 1 sample adult are randomly selected, and information on each is collected with the Sample Child Core and the Sample Adult Core questionnaires. In 2000 and 2005, sample adults also completed a cancer supplement, which collected information regarding use of mammography and other cancer screening modalities. Nationally, the NHIS uses about 400 interviewers, trained and directed by health survey supervisors in the 12 U.S. Census Bureau Regional Offices. The interviewers receive thorough training on an annual basis in basic interviewing procedures and in the concepts and procedures unique to the NHIS. The NHIS is conducted using computer-assisted personal interviewing (CAPI). This method presents the questionnaire on computer screens to each interviewer and guides the interviewer through it, automatically routing the interviewer to appropriate questions based on answers to previous questions. Interviewers enter survey responses directly into the computer, and the CAPI program determines if the selected response is within an allowable range, checks it for consistency against other data collected during the interview, and saves the responses into a survey data file. This technology reduces the time required for transferring, processing, and releasing data, and ensures the accurate flow of the questionnaire. The survey sample is re-evaluated every 10 years in order to better reflect the changing U.S. population. The sample is chosen in such a way that each person in the population has a known non-zero probability of selection. These probabilities of selection, along with 9 adjustments for nonresponse and post-stratification, are reflected
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in the sample weights that are provided in the data files provided by the NHIS. These weights, which account for the multistage sample design to reflect the civilian noninstitutionalized population of the United States, are used for data analysis. In addition to the design and ratio adjustments, weights are further modified by adjusting them to the 2000 Census-based population estimates for sex, age, and race/ethnicity populations (post-stratification). Because of this complex sample design involving stratification, clustering, and multistage sampling, and the resulting adjusted sampling weights, statistical software that provides the capability of variance estimation and hypothesis testing for complex sample designs (e.g. Survey Data Analysis (SUDAAN)) is needed. In 2000, the NHIS surveyed 32,374 adults, representing a final response rate of 72.1%.13 Of these, 8774 Caucasian and 1623 African-American women over the age of 40 were surveyed, representing 51,709,917 Caucasian and 6,529,827 AfricanAmerican women in this age group in the US population. In 2005, 31,428 adults were surveyed, representing a final response rate of 69.0%.14 Of these, 8759 Caucasian and 1573 African-American women over the age of 40 were surveyed, representing 56,611,569 Caucasian and 7,627,337 African-American women in this age group in the US population. These women over the age of 40 were considered the cohort of interest for this study. Mammography screening rates of Caucasian and African-American women surveyed in 2000 and 2005 were compared using chi-square tests. For women who reported not having had a mammogram within the past 2 years, the reason for this non-compliance was compared between the 2 racial groups, in 2000 and 2005. Given that education level, insurance status, and income may confound the primary relationship of race on mammography screening rates, we performed a multivariate analysis using logistic regression to determine the independent effect of race controlling for these 3 factors on mammography rates in 2000 and 2005. Given the complicated sampling scheme used in the NHIS to make the survey nationally representative, population estimates were obtained by weighting each observation by the appropriate sample weights given by each survey. The sample weights account for the probabilities of selection, along with adjustments for non-response and post-stratification. All statistics were performed using SAS Version 9.1.3, and SUDAAN software.
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Table I. Sociodemographic features Proportion (%) of women over 40 years of age 2000
2005
Feature
Caucasian
AA
P-value
Caucasian
AA
P-value
Median age (yrs) Highest education achieved Less than high school High school / GED Some college Associate degree Bachelors degree Masters/Doctoral Annual household income < $20,000 $20,000–$75,000 >$75,000 Insurance status Not covered Medicaid Medicare Private
58.2
55.7
P < .0001 P = .0048
58.4
55.7
P < .0001 P = .0003
2.2 2.7 9.9 10.3 12.6 32.8
6.5 3.6 4.7 7.7 16.6 32.9
3.6 5.3 10.3 11.5 11.4 35.8
0 1.8 9.6 11.8 8.9 35.2
17.4 57.3 25.3
32.0 51.3 16.7
13.8 56.5 29.7
25.5 55.0 19.5
7.00 4.15 30.2 55.9
12.9 13.0 20.4 48.7
8.4 4.9 29.8 54.3
14.1 14.7 20.9 45.7
P < .0001
P < .0001
P < .0001
P < .0001
AA = African-American.
RESULTS Of the 10,994 women over the age of 40 surveyed in 2000, 8774 (84.4%) were Caucasian and 1623 (10.7%) were African-American. Of the 11,128 women over the age of 40 surveyed in 2005, 8759 (82.2%) were Caucasian and 1573 (11.1%) were African-American. Sociodemographic features of these groups are shown in Table I. Significant differences in educational level, insurance status, and income were seen in both 2000 and 2005 between Caucasian and African-American women. Overall, the rate of ever having had a mammogram declined from 80.8% in 2000 to 79.5% in 2005 (P < .0001), and the rate of having had a mammogram within the preceding 2 years declined from 68.5% in 2000 to 65.5% in 2005 (P = .0005). Univariate comparisons of mammographic screening rates between the Caucasian and African-American populations are shown in Table II. In each year, African-American women were less likely than Caucasian women to report ever having had a mammogram or having had a mammogram within the preceding 2 years. While a downward trend in mammography screening was seen in both populations, this achieved statistical significance only in the Caucasian population. A multivariate model controlling for education level, insurance status, and income, was performed to determine the independent effect of race on reporting ever having had a mammogram in 2000
and 2005. These results are shown in Table III. A second multivariate model controlling for education level, insurance status, and income, was performed to determine the independent effect of race on reporting having had a mammogram within the preceding 2 years in 2000 and 2005. These results are shown in Table IV. In all analyses, race was not a significant predictor of mammographic screening when sociodemographic factors were taken into consideration. Women who did not have a mammogram within the preceding 2 years were asked what the reason for this was. Uniformly, the main reason cited was that they simply ‘‘didn’t think about it.’’ The second most common reason, cited for both Caucasian and African-American women in 2005, was that their physician didn’t order a mammogram or didn’t say they needed one (13.5% and 13.4%, respectively). The proportion of women who claimed this was the reason they didn’t have a mammogram within the preceding 2 years increased from 2000 (12.5% and 9.6%, for Caucasian and African-American women, respectively). Cost remained a significant deterrent to mammographic screening for both Caucasian and African-American women in the 2005 survey with 10.3% of each of these populations indicating that this was the main reason they had not had a mammogram within the preceding 2 years. This proportion had increased for both populations from the 2000 survey in which 7.9% of Caucasians
470 Chagpar, Polk, and McMasters
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Table II. Univariate analysis of mammographic screening by race and year Proportion (%) women reporting having had a mammogram Ever
Caucasian AA P-value
Within the past 2 years
2000
2005
P-value
2000
2005
P-value
82.2 76.3 <.0001
81.0 74.0 <.0001
<.0001 .5082
69.8 64.4 <.0001
66.7 62.9 <.0001
.0006 .4998
Table III. Multivariate model of ever having had a mammogram 2000 Factor Race Caucasian AA Education < High school High school/GED Some college Associate degree Bachelors degree Masters/Doctoral Income < $20,000 $20,000–$75,000 >$75,000 Insurance status Not covered Medicaid Medicare Private
OR (95% CI)
2005 P-value
OR (95% CI)
.8448 1.00 1.07 (0.55 – 2.10)
.1107 1.00 0.59 (0.30 – 1.13)
.0121 1.00 6.06 1.39 2.11 1.66 2.61
(1.21 (0.38 (0.57 (0.40 (0.83
– – – – –
.7666 1.00 0.69 0.27 0.32 0.31 0.32
30.39) 5.15) 7.78) 6.96) 8.23)
(0.09 (0.04 (0.05 (0.04 (0.06
– – – – –
5.08) 1.80) 2.04) 2.18) 1.68)
.7129 1.00 1.29 (0.69 – 2.40) 1.00 (0.52 – 1.94)
.4376 1.00 1.56 (0.78 – 3.12) 0.99 (0.44 – 2.23)
.0898 1.00 1.99 (1.01 – 3.92) 1.66 (0.95 – 2.92) 2.66 (1.05 – 6.70)
and 8.1% of African-Americans cited cost as the main reason why they did not have a mammogram in the preceding 2 years. While cost was the third most common reason cited for not having had a mammogram within the preceding 2 years for African-American women surveyed in 2005, it was the fourth most common reason cited by Caucasian women. For Caucasian women in 2005, lack of time (i.e.; ‘‘I put it off’’ or ‘‘I didn’t get around to it’’) was the third most common reason cited for not having had a mammogram within the preceding 2 years (12.3% vs 7.8% for African-American women). This, too, increased from 2000, when the proportion of Caucasian and African-American women citing this reason for not having had a mammogram was 9.8% and 7.0%, respectively. DISCUSSION Mammographic screening across racial groups increased from 1987 to 2003.15 The proportion of women reporting having had a mammogram
P-value
<.0001 1.00 3.85 (1.81 – 8.17) 6.36 (3.07 – 13.17) 2.12 (0.81 – 5.55)
within the preceding 2 years increased from 30% in 1987 to 71% in 2003 for Caucasian women, and from 24% in 1987 to 70% in 2003 for African-American women.15 More recently, however, a reduction in mammographic screening has been noted in national studies.2,16 The racial differences in this trend have not been explored. Given the politically important issues of improving access to care in disadvantaged populations, and national programs designed to minimize disparities between Caucasian and African-American women with respect to screening mammography, this is of considerable interest. In this nationally representative, populationbased study, we found that African-American women were consistently less likely to report ever having had a mammogram or having had a mammogram in the preceding 2 years than Caucasian women. However, the absolute difference of women who reported having had a mammogram within the preceding 2 years between the 2 races
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Table IV. Multivariate model of having had a mammogram within preceding 2 years 2000 Factor Race Caucasian AA Education < High school High school/GED Some college Associate degree Bachelors degree Masters/Doctoral Income < $20,000 $20,000–$75,000 >$75,000 Insurance status Not covered Medicaid Medicare Private
OR (95% CI)
2005 P-value
OR (95% CI)
.2672 1.00 1.36 (0.79 – 2.35)
.6032 1.00 1.16 (0.66 – 2.06)
.0095 1.00 0.22 1.00 0.52 1.06 0.72
(0.05 (0.33 (0.17 (0.32 (0.27
– – – – –
.7538 1.00 1.24 1.17 2.06 1.52 1.02
0.94) 3.04) 1.60) 3.43) 1.92)
(0.24 (0.26 (0.49 (0.38 (0.26
– – – – –
6.43) 5.19) 8.76) 6.01) 3.95)
.8919 1.00 0.89 (0.55 – 1.45) 1.02 (0.57 – 1.83)
.6616 1.00 0.83 (0.46 – 1.51) 1.19 (0.60 – 2.37)
.0156 1.00 0.49 (0.27 – 0.91) 0.65 (0.36 – 1.17) 0.39 (0.18 – 0.84)
has diminished between 2000 and 2005 (5.4% vs 3.8%, respectively). Both racial groups have had a decline in mammographic screening between 2000 and 2005; however, this trend only reached statistical significance in Caucasian women. The absolute reduction in the proportion of Caucasian women who reported having had a mammogram within the preceding 2 years between 2000 and 2005 was 3.1%, while the absolute reduction in the proportion of African-American women who reported having had a mammogram within the preceding 2 years between 2000 and 2005 was 1.5%. A number of studies have found that AfricanAmerican women are less likely to adhere to mammographic screening guidelines.17-19 This may contribute, in part, to the more advanced presentation of breast cancer and worse survival rates in the African-American population.19,20 However, this effect does not seem to be driven primarily by race, but rather by the socioeconomic factors which correlate with minority race. We found that African-American women were significantly less likely to have mammographic screening than were Caucasian women in both 2000 and 2005. However, race was not an independent predictor of mammography screening on multivariate analysis controlling for education, insurance status, and income level. This implies that the apparent racial disparity in mammographic screening is mediated by socioeconomic factors that
P-value
.1031 1.00 0.45 (0.22 – 0.93) 0.66 (0.32 – 1.33) 0.38 (0.15 – 0.93)
often go along with race. This has been echoed by other studies, some of which demonstrated that once these socioeconomic variables are controlled, African-American women may, in fact, be more likely to be screened than Caucasian women.21,22 Still, the main reason for not having had a mammogram within the preceding 2 years is reported to be ‘‘not thinking about it,’’ regardless of race. ‘‘My doctor didn’t order it’’ was the second most common reason for not having had a mammogram within the preceding 2 years, regardless of race, in the 2005 survey. However, the third most common reason for not having had a mammogram within the preceding 2 years was cost for African-American women (10.3%) and time for Caucasian women (12.3%). These reported reasons for non-adherence to screening recommendations are of interest in engineering public health programs to enhance mammographic screening. The recent reduction in screening rates is of particular concern given the significant reduction in mortality from breast cancer associated with regular screening.23 The current study has a number of limitations. To begin with, as with many surveys, the NHIS did not have a 100% response rate. The response rates of 72.1% and 69.0% (in 2000 and 2005 respectively) are quite respectable for this type of national survey. Being derived from survey data, our conclusions are based entirely on self-report.
472 Chagpar, Polk, and McMasters
Although some studies have found self-report data to overestimate the true rate of mammography,15 others have found that this is a reliable measure for mammography.24,25 Regardless, any intrinsic bias related to the self-report nature of the NHIS survey should be evenly distributed between the 2 years and between the 2 racial groups. Therefore, the conclusions we reach on the basis of comparing like measures in this survey should be valid. The only concern may be if African-American women would systematically be more likely to overestimate their mammography usage in 2005 than in 2000. We have no reason to believe that this would necessarily be the case; however, this potential limitation should be noted. Furthermore, even if these data over-estimate mammography rates, the downward trend over time remains a matter of concern. If we accept the American Cancer Society’s statement that ‘‘until >90% of American women age >40 are receiving annual mammograms, the potential remains unrealized for a much more substantial reduction in breast cancer mortality,’’26 our finding that fewer than 70% of Caucasian and African-American women report having had a mammogram in the preceding 2 years leaves significant work to be done in improving screening.
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10.
11.
12.
13.
14.
15.
16.
17.
18.
REFERENCES 1. Ravdin PM, Cronin KA, Howlader N, et al. The decrease in breast-cancer incidence in 2003 in the United States. N Engl J Med 2007;356:1670-4. 2. Chagpar AB, McMasters KM. Trends in mammography and clinical breast examination: a population-based study. J Surg Res 2007;140:214-9. 3. Fletcher SW, Elmore JG. Clinical practice. Mammographic screening for breast cancer. N Engl J Med 2003;348: 1672-80. 4. Alexander FE, Anderson TJ, Brown HK, et al. 14 years of follow-up from the Edinburgh randomised trial of breastcancer screening. Lancet 1999;353:1903-8. 5. Andersson I, Janzon L. Reduced breast cancer mortality in women under age 50: updated results from the Malmo Mammographic Screening Program. J Natl Cancer Inst Monogr 1997:63-7. 6. Bjurstam N, Bjorneld L, Warwick J, et al. The Gothenburg Breast Screening Trial. Cancer 2003;97:2387-96. 7. Frisell J, Lidbrink E, Hellstrom L, et al. Followup after 11 years—update of mortality results in the Stockholm mammographic screening trial. Breast Cancer Res Treat 1997; 45:263-70. 8. Miller AB, To T, Baines CJ, et al. Canadian National Breast Screening Study-2: 13-year results of a randomized trial in women aged 50-59 years. J Natl Cancer Inst 2000;92: 1490-9. 9. Miller AB, To T, Baines CJ, et al. The Canadian National Breast Screening Study-1: breast cancer mortality after 11 to 16 years of follow-up. A randomized screening trial of
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mammography in women age 40 to 49 years. Ann Intern Med 2002;137:305-12. Nystrom L, Andersson I, Bjurstam N, et al. Long-term effects of mammography screening: updated overview of the Swedish randomised trials. Lancet 2002;359:909-19. Shapiro S. Periodic screening for breast cancer: the HIP Randomized Controlled Trial. Health Insurance Plan. J Natl Cancer Inst Monogr 1997:27-30. Tabar L, Yen MF, Vitak B, et al. Mammography service screening and mortality in breast cancer patients: 20-year follow-up before and after introduction of screening. Lancet 2003;361:1405-10. National Center for Health Statistics. Data File Documentation, National Health Interview Survey, 2000 (machine readable data file and documentation). Hyattsville, Maryland: National Center for Health Statistics; 2002. National Center for Health Statistics. Data File Documentation, National Health Interview Survey, 2005 (machine readable data file and documentation). Hyattsville, Maryland: National Center for Health Statistics, Centers for Disease Control and Prevention; 2006. Smigal C, Jemal A, Ward E, et al. Trends in breast cancer by race and ethnicity: update 2006. CA Cancer J Clin 2006;56: 168-83. Feldstein AC, Vogt TM, Aickin M, et al. Mammography screening rates decline: a person-time approach to evaluation. Prev Med 2006;43:178-82. Dailey AB, Kasl SV, Holford TR, et al. Perceived racial discrimination and nonadherence to screening mammography guidelines: results from the race differences in the screening mammography process study. Am J Epidemiol 2007;165:1287-95. Davis C, Emerson JS, Husaini BA. Breast cancer screening among African American women: adherence to current recommendations. J Health Care Poor Underserved 2005;16: 308-14. Smith-Bindman R, Miglioretti DL, Lurie N, et al. Does utilization of screening mammography explain racial and ethnic differences in breast cancer? Ann Intern Med 2006;144:541-53. Sassi F, Luft HS, Guadagnoli E. Reducing racial/ethnic disparities in female breast cancer: screening rates and stage at diagnosis. Am J Public Health 2006;96:2165-72. Jones AR, Caplan LS, Davis MK. Racial/ethnic differences in the self-reported use of screening mammography. J Community Health 2003;28:303-16. Bolen JC, Rhodes L, Powell-Griner EE, et al. State-specific prevalence of selected health behaviors, by race and ethnicity—Behavioral Risk Factor Surveillance System, 1997. MMWR CDC Surveill Summ 2000;49:1-60. U.S. Preventive Services Task Force. Screening for Breast Cancer: Recommendations and Rationale. February 2002. Agency for Healthcare Research and Quality, Rockville, MD. Available from: http://www.ahrq.gov/clinic/3rduspstf/ breastcancer/brcanrr.htm. 2006. King ES, Rimer BK, Trock B, et al. How valid are mammography self-reports? Am J Public Health 1990;80:1386-8. Zapka JG, Bigelow C, Hurley T, et al. Mammography use among sociodemographically diverse women: the accuracy of self-report. Am J Public Health 1996;86:1016-21. Byers T, Barrera E, Fontham ET, et al. A midpoint assessment of the American Cancer Society challenge goal to halve the U.S. cancer mortality rates between the years 1990 and 2015. Cancer 2006;107:396-405.
Background. The rates of mammography have been declining over the last 5 years. The objective of this study was to examine racial disparities in this trend. Methods. The National Health Interview Survey is a population-based interview survey conducted annually. Caucasian and African-American women over 40 years of age who completed the cancer module of this survey in 2000 and 2005 formed the cohort of interest for this study. Results. In 2000, 69.8% of Caucasian and 64.4% of African-American women over the age of 40 had had a mammogram within the preceding 2 years. In 2005, these rates declined to 66.7% and 62.9% respectively. This decline only reached statistical significance in the Caucasian population (P = .0006 vs P = .4998). While on univariate analysis a significant difference was seen between rates of mammography in Caucasian and African-American women (P < .0001), multivariate analysis controlling for education, income, and insurance status, did not find race to be a significant independent predictor of mammography rates in each year. Conclusion. Rates of mammography are declining, particularly in Caucasian populations. While minority women are less likely to report having had a mammogram, this apparent racial disparity is explained by differences in education, income and insurance status. (Surgery 2008;144:467-72.) From the Division of Surgical Oncology, Department of Surgery, University of Louisville, Ky
BETWEEN 2001 AND 2004, there was an 8.6% reduction in the incidence of breast cancer in the United States.1 While this reduction was due, in part, to a decline in the use of hormone replacement therapy, there was also a significant decline in screening mammography and clinical breast examinations among women 40 years of age and older.2 This is particularly concerning given the proven efficacy of screening mammography in improving early detection and survival in breast cancer patients, as demonstrated by 8 randomized controlled trials.3-12 Access to medical care, and particularly preventive screening, is a politically charged issue. Economically and socially disadvantaged populations have poorer access to quality care, often leading to suboptimal outcomes. African-American patients often are disadvantaged in terms of Presented at the Society of University Surgeons Annual Meeting, held in Huntington Beach, California on February 13–15, 2008. Accepted for publication May 22, 2008. Reprint requests: Anees B. Chagpar, 315 E. Broadway, Suite #312, Louisville, KY 40202. E-mail: anees.chagpar@nortonhealthcare. org. 0039-6060/$ - see front matter Ó 2008 Mosby, Inc. All rights reserved. doi:10.1016/j.surg.2008.05.006
education, income and insurance status. Previous studies have demonstrated a survival difference between Caucasian and African-American breast cancer patients, with some studies suggesting that these differences may be attributed in part to racial disparities in terms of mammographic screening. A number of national programs, such as the Breast and Cervical Cancer Early Detection Program and the subsequent Breast and Cervical Cancer Treatment Act of 2000, have provided resources to improve screening rates nationally, particularly in African-American patients. The current downward trend in screening mammography is concerning; and it is unclear as to whether this trend has affected both Caucasians and AfricanAmericans to the same extent. Such issues are critical in the implementation of future national screening programs, and will serve to inform health policy. The objective of this study was to assess racial disparities in the recent trend in mammographic screening rates in a populationbased study. METHODS Each year the National Center for Health Statistics (NCHS), Centers for Disease Control and Prevention conducts the National Health Interview Survey (NHIS). The NHIS has been conducted annually since its inception in 1957. It is a national SURGERY 467
468 Chagpar, Polk, and McMasters
population-based face-to-face survey which is designed to be representative of the American civilian non-institutionalized population. This survey consists of 2 main components: the ‘‘Basic Module,’’ containing basic health and demographic information, and ‘‘Supplements,’’ which relate to specific areas of interest. The Basic Module, which remains largely unchanged from year to year, consists of 3 components: the Family Core, the Sample Child Core, and the Sample Adult Core. The Family Core component collects information on everyone in the family, and its sample also serves as a sampling frame for additional integrated surveys, as needed. Information collected for all family members includes household composition and socio-demographic characteristics among other factors. From each family in the NHIS, 1 sample child (if any children under age 18 are present) and 1 sample adult are randomly selected, and information on each is collected with the Sample Child Core and the Sample Adult Core questionnaires. In 2000 and 2005, sample adults also completed a cancer supplement, which collected information regarding use of mammography and other cancer screening modalities. Nationally, the NHIS uses about 400 interviewers, trained and directed by health survey supervisors in the 12 U.S. Census Bureau Regional Offices. The interviewers receive thorough training on an annual basis in basic interviewing procedures and in the concepts and procedures unique to the NHIS. The NHIS is conducted using computer-assisted personal interviewing (CAPI). This method presents the questionnaire on computer screens to each interviewer and guides the interviewer through it, automatically routing the interviewer to appropriate questions based on answers to previous questions. Interviewers enter survey responses directly into the computer, and the CAPI program determines if the selected response is within an allowable range, checks it for consistency against other data collected during the interview, and saves the responses into a survey data file. This technology reduces the time required for transferring, processing, and releasing data, and ensures the accurate flow of the questionnaire. The survey sample is re-evaluated every 10 years in order to better reflect the changing U.S. population. The sample is chosen in such a way that each person in the population has a known non-zero probability of selection. These probabilities of selection, along with 9 adjustments for nonresponse and post-stratification, are reflected
Surgery September 2008
in the sample weights that are provided in the data files provided by the NHIS. These weights, which account for the multistage sample design to reflect the civilian noninstitutionalized population of the United States, are used for data analysis. In addition to the design and ratio adjustments, weights are further modified by adjusting them to the 2000 Census-based population estimates for sex, age, and race/ethnicity populations (post-stratification). Because of this complex sample design involving stratification, clustering, and multistage sampling, and the resulting adjusted sampling weights, statistical software that provides the capability of variance estimation and hypothesis testing for complex sample designs (e.g. Survey Data Analysis (SUDAAN)) is needed. In 2000, the NHIS surveyed 32,374 adults, representing a final response rate of 72.1%.13 Of these, 8774 Caucasian and 1623 African-American women over the age of 40 were surveyed, representing 51,709,917 Caucasian and 6,529,827 AfricanAmerican women in this age group in the US population. In 2005, 31,428 adults were surveyed, representing a final response rate of 69.0%.14 Of these, 8759 Caucasian and 1573 African-American women over the age of 40 were surveyed, representing 56,611,569 Caucasian and 7,627,337 African-American women in this age group in the US population. These women over the age of 40 were considered the cohort of interest for this study. Mammography screening rates of Caucasian and African-American women surveyed in 2000 and 2005 were compared using chi-square tests. For women who reported not having had a mammogram within the past 2 years, the reason for this non-compliance was compared between the 2 racial groups, in 2000 and 2005. Given that education level, insurance status, and income may confound the primary relationship of race on mammography screening rates, we performed a multivariate analysis using logistic regression to determine the independent effect of race controlling for these 3 factors on mammography rates in 2000 and 2005. Given the complicated sampling scheme used in the NHIS to make the survey nationally representative, population estimates were obtained by weighting each observation by the appropriate sample weights given by each survey. The sample weights account for the probabilities of selection, along with adjustments for non-response and post-stratification. All statistics were performed using SAS Version 9.1.3, and SUDAAN software.
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Table I. Sociodemographic features Proportion (%) of women over 40 years of age 2000
2005
Feature
Caucasian
AA
P-value
Caucasian
AA
P-value
Median age (yrs) Highest education achieved Less than high school High school / GED Some college Associate degree Bachelors degree Masters/Doctoral Annual household income < $20,000 $20,000–$75,000 >$75,000 Insurance status Not covered Medicaid Medicare Private
58.2
55.7
P < .0001 P = .0048
58.4
55.7
P < .0001 P = .0003
2.2 2.7 9.9 10.3 12.6 32.8
6.5 3.6 4.7 7.7 16.6 32.9
3.6 5.3 10.3 11.5 11.4 35.8
0 1.8 9.6 11.8 8.9 35.2
17.4 57.3 25.3
32.0 51.3 16.7
13.8 56.5 29.7
25.5 55.0 19.5
7.00 4.15 30.2 55.9
12.9 13.0 20.4 48.7
8.4 4.9 29.8 54.3
14.1 14.7 20.9 45.7
P < .0001
P < .0001
P < .0001
P < .0001
AA = African-American.
RESULTS Of the 10,994 women over the age of 40 surveyed in 2000, 8774 (84.4%) were Caucasian and 1623 (10.7%) were African-American. Of the 11,128 women over the age of 40 surveyed in 2005, 8759 (82.2%) were Caucasian and 1573 (11.1%) were African-American. Sociodemographic features of these groups are shown in Table I. Significant differences in educational level, insurance status, and income were seen in both 2000 and 2005 between Caucasian and African-American women. Overall, the rate of ever having had a mammogram declined from 80.8% in 2000 to 79.5% in 2005 (P < .0001), and the rate of having had a mammogram within the preceding 2 years declined from 68.5% in 2000 to 65.5% in 2005 (P = .0005). Univariate comparisons of mammographic screening rates between the Caucasian and African-American populations are shown in Table II. In each year, African-American women were less likely than Caucasian women to report ever having had a mammogram or having had a mammogram within the preceding 2 years. While a downward trend in mammography screening was seen in both populations, this achieved statistical significance only in the Caucasian population. A multivariate model controlling for education level, insurance status, and income, was performed to determine the independent effect of race on reporting ever having had a mammogram in 2000
and 2005. These results are shown in Table III. A second multivariate model controlling for education level, insurance status, and income, was performed to determine the independent effect of race on reporting having had a mammogram within the preceding 2 years in 2000 and 2005. These results are shown in Table IV. In all analyses, race was not a significant predictor of mammographic screening when sociodemographic factors were taken into consideration. Women who did not have a mammogram within the preceding 2 years were asked what the reason for this was. Uniformly, the main reason cited was that they simply ‘‘didn’t think about it.’’ The second most common reason, cited for both Caucasian and African-American women in 2005, was that their physician didn’t order a mammogram or didn’t say they needed one (13.5% and 13.4%, respectively). The proportion of women who claimed this was the reason they didn’t have a mammogram within the preceding 2 years increased from 2000 (12.5% and 9.6%, for Caucasian and African-American women, respectively). Cost remained a significant deterrent to mammographic screening for both Caucasian and African-American women in the 2005 survey with 10.3% of each of these populations indicating that this was the main reason they had not had a mammogram within the preceding 2 years. This proportion had increased for both populations from the 2000 survey in which 7.9% of Caucasians
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Table II. Univariate analysis of mammographic screening by race and year Proportion (%) women reporting having had a mammogram Ever
Caucasian AA P-value
Within the past 2 years
2000
2005
P-value
2000
2005
P-value
82.2 76.3 <.0001
81.0 74.0 <.0001
<.0001 .5082
69.8 64.4 <.0001
66.7 62.9 <.0001
.0006 .4998
Table III. Multivariate model of ever having had a mammogram 2000 Factor Race Caucasian AA Education < High school High school/GED Some college Associate degree Bachelors degree Masters/Doctoral Income < $20,000 $20,000–$75,000 >$75,000 Insurance status Not covered Medicaid Medicare Private
OR (95% CI)
2005 P-value
OR (95% CI)
.8448 1.00 1.07 (0.55 – 2.10)
.1107 1.00 0.59 (0.30 – 1.13)
.0121 1.00 6.06 1.39 2.11 1.66 2.61
(1.21 (0.38 (0.57 (0.40 (0.83
– – – – –
.7666 1.00 0.69 0.27 0.32 0.31 0.32
30.39) 5.15) 7.78) 6.96) 8.23)
(0.09 (0.04 (0.05 (0.04 (0.06
– – – – –
5.08) 1.80) 2.04) 2.18) 1.68)
.7129 1.00 1.29 (0.69 – 2.40) 1.00 (0.52 – 1.94)
.4376 1.00 1.56 (0.78 – 3.12) 0.99 (0.44 – 2.23)
.0898 1.00 1.99 (1.01 – 3.92) 1.66 (0.95 – 2.92) 2.66 (1.05 – 6.70)
and 8.1% of African-Americans cited cost as the main reason why they did not have a mammogram in the preceding 2 years. While cost was the third most common reason cited for not having had a mammogram within the preceding 2 years for African-American women surveyed in 2005, it was the fourth most common reason cited by Caucasian women. For Caucasian women in 2005, lack of time (i.e.; ‘‘I put it off’’ or ‘‘I didn’t get around to it’’) was the third most common reason cited for not having had a mammogram within the preceding 2 years (12.3% vs 7.8% for African-American women). This, too, increased from 2000, when the proportion of Caucasian and African-American women citing this reason for not having had a mammogram was 9.8% and 7.0%, respectively. DISCUSSION Mammographic screening across racial groups increased from 1987 to 2003.15 The proportion of women reporting having had a mammogram
P-value
<.0001 1.00 3.85 (1.81 – 8.17) 6.36 (3.07 – 13.17) 2.12 (0.81 – 5.55)
within the preceding 2 years increased from 30% in 1987 to 71% in 2003 for Caucasian women, and from 24% in 1987 to 70% in 2003 for African-American women.15 More recently, however, a reduction in mammographic screening has been noted in national studies.2,16 The racial differences in this trend have not been explored. Given the politically important issues of improving access to care in disadvantaged populations, and national programs designed to minimize disparities between Caucasian and African-American women with respect to screening mammography, this is of considerable interest. In this nationally representative, populationbased study, we found that African-American women were consistently less likely to report ever having had a mammogram or having had a mammogram in the preceding 2 years than Caucasian women. However, the absolute difference of women who reported having had a mammogram within the preceding 2 years between the 2 races
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Table IV. Multivariate model of having had a mammogram within preceding 2 years 2000 Factor Race Caucasian AA Education < High school High school/GED Some college Associate degree Bachelors degree Masters/Doctoral Income < $20,000 $20,000–$75,000 >$75,000 Insurance status Not covered Medicaid Medicare Private
OR (95% CI)
2005 P-value
OR (95% CI)
.2672 1.00 1.36 (0.79 – 2.35)
.6032 1.00 1.16 (0.66 – 2.06)
.0095 1.00 0.22 1.00 0.52 1.06 0.72
(0.05 (0.33 (0.17 (0.32 (0.27
– – – – –
.7538 1.00 1.24 1.17 2.06 1.52 1.02
0.94) 3.04) 1.60) 3.43) 1.92)
(0.24 (0.26 (0.49 (0.38 (0.26
– – – – –
6.43) 5.19) 8.76) 6.01) 3.95)
.8919 1.00 0.89 (0.55 – 1.45) 1.02 (0.57 – 1.83)
.6616 1.00 0.83 (0.46 – 1.51) 1.19 (0.60 – 2.37)
.0156 1.00 0.49 (0.27 – 0.91) 0.65 (0.36 – 1.17) 0.39 (0.18 – 0.84)
has diminished between 2000 and 2005 (5.4% vs 3.8%, respectively). Both racial groups have had a decline in mammographic screening between 2000 and 2005; however, this trend only reached statistical significance in Caucasian women. The absolute reduction in the proportion of Caucasian women who reported having had a mammogram within the preceding 2 years between 2000 and 2005 was 3.1%, while the absolute reduction in the proportion of African-American women who reported having had a mammogram within the preceding 2 years between 2000 and 2005 was 1.5%. A number of studies have found that AfricanAmerican women are less likely to adhere to mammographic screening guidelines.17-19 This may contribute, in part, to the more advanced presentation of breast cancer and worse survival rates in the African-American population.19,20 However, this effect does not seem to be driven primarily by race, but rather by the socioeconomic factors which correlate with minority race. We found that African-American women were significantly less likely to have mammographic screening than were Caucasian women in both 2000 and 2005. However, race was not an independent predictor of mammography screening on multivariate analysis controlling for education, insurance status, and income level. This implies that the apparent racial disparity in mammographic screening is mediated by socioeconomic factors that
P-value
.1031 1.00 0.45 (0.22 – 0.93) 0.66 (0.32 – 1.33) 0.38 (0.15 – 0.93)
often go along with race. This has been echoed by other studies, some of which demonstrated that once these socioeconomic variables are controlled, African-American women may, in fact, be more likely to be screened than Caucasian women.21,22 Still, the main reason for not having had a mammogram within the preceding 2 years is reported to be ‘‘not thinking about it,’’ regardless of race. ‘‘My doctor didn’t order it’’ was the second most common reason for not having had a mammogram within the preceding 2 years, regardless of race, in the 2005 survey. However, the third most common reason for not having had a mammogram within the preceding 2 years was cost for African-American women (10.3%) and time for Caucasian women (12.3%). These reported reasons for non-adherence to screening recommendations are of interest in engineering public health programs to enhance mammographic screening. The recent reduction in screening rates is of particular concern given the significant reduction in mortality from breast cancer associated with regular screening.23 The current study has a number of limitations. To begin with, as with many surveys, the NHIS did not have a 100% response rate. The response rates of 72.1% and 69.0% (in 2000 and 2005 respectively) are quite respectable for this type of national survey. Being derived from survey data, our conclusions are based entirely on self-report.
472 Chagpar, Polk, and McMasters
Although some studies have found self-report data to overestimate the true rate of mammography,15 others have found that this is a reliable measure for mammography.24,25 Regardless, any intrinsic bias related to the self-report nature of the NHIS survey should be evenly distributed between the 2 years and between the 2 racial groups. Therefore, the conclusions we reach on the basis of comparing like measures in this survey should be valid. The only concern may be if African-American women would systematically be more likely to overestimate their mammography usage in 2005 than in 2000. We have no reason to believe that this would necessarily be the case; however, this potential limitation should be noted. Furthermore, even if these data over-estimate mammography rates, the downward trend over time remains a matter of concern. If we accept the American Cancer Society’s statement that ‘‘until >90% of American women age >40 are receiving annual mammograms, the potential remains unrealized for a much more substantial reduction in breast cancer mortality,’’26 our finding that fewer than 70% of Caucasian and African-American women report having had a mammogram in the preceding 2 years leaves significant work to be done in improving screening.
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