Patterns of Mammography Use among Hispanic, American Indian, and Non-Hispanic White Women in New Mexico, 19941997
Frank D. Gilliland1,
Robert D. Rosenberg2,
William C. Hunt3,
Patricia Stauber3 and
Charles R. Key3,4
1 Department of Preventive Medicine and Norris Comprehensive Cancer Center, University of Southern California, Los Angeles, CA.
2 Department of Radiology, University of New Mexico, Albuquerque, NM.
3 New Mexico Tumor Registry, University of New Mexico, Albuquerque, NM.
4 Department of Pathology, University of New Mexico, Albuquerque, NM.
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ABSTRACT
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For screening efforts to maximally reduce mortality in the general population, a large proportion of women need to utilize mammography routinely. To investigate utilization of mammography in a community setting, the authors used population-based data collected by the New Mexico Mammography Project for residents of the Albuquerque, New Mexico, metropolitan area for the period 19941997. The authors computed screening rates and the proportion of women who routinely use mammography. The utilization of mammography was low. Only 50% of the women aged 5074 years were screened each year. Less than one third of women aged 4049 years or 75 years and older were screened annually. The percentage of women who routinely used mammography on an annual or biennial basis was low in all age groups, especially among Hispanics and American Indians. Women aged 5074 years had the highest percentage of routine annual mammography use, ranging from 30% in non-Hispanic Whites to 20% in Hispanics. Current utilization of mammography in community-based screening efforts is unlikely to achieve a potential 30% reduction in breast cancer mortality. Interventions are needed to increase the routine use of mammography. Am J Epidemiol 2000;152:4327.
Abbreviations:
NMMP; New Mexico Mammography Project
breast neoplasms; Hispanic Americans; Indians; North American; mammography
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INTRODUCTION
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The mortality, morbidity, and decrements in quality of life associated with breast cancer are important clinical and public health issues in the United States. Approximately 175,000 new cases of invasive breast cancer and 43,300 deaths from breast cancer are projected to have occurred in 1999 (1
). Efforts to reduce the burden of breast cancer have been focused largely on early detection and treatment. Mass screening mammography of women aged 5074 years is now widely accepted as efficacious and has been advocated by a number of different US professional organizations, including the American Cancer Society, the American College of Obstetricians and Gynecologists, the American College of Radiology, the American Academy of Family Practitioners, and the US Preventive Services Task Force.
Recommendations for screening mammograms have been based on the results of randomized controlled clinical trials and meta-analyses, which have consistently demonstrated a 2530 percent reduction in breast cancer mortality for the age group 5074 years (2




8
). Screening of women aged 4049 years was controversial until recently, when trials indicated a modest benefit for younger women (5
, 




15
).
Although the efficacy of screening in the trial setting is well documented, the effectiveness of mass screening as it occurs in a community setting has not been as extensively studied. Effectiveness is likely to depend upon a complex interaction of utilization, test performance, and practice patterns (15
, 16
). This study investigates a critical element for effectiveness, the pattern of utilization of mammography in a general community setting.
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MATERIALS AND METHODS
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Data on the use and outcomes of mammography are collected statewide by the New Mexico Mammography Project (NMMP), a member of the National Cancer Institute's Breast Cancer Surveillance Consortium (17
, 18
). The NMMP is a collaboration between radiology groups in New Mexico and the New Mexico Tumor Registry and involves the collection of computerized mammography data from radiology groups who read mammograms in New Mexico. All radiology groups in the Albuquerque, New Mexico, metropolitan area participate in the NMMP. Mammograms from mammography machines in nonradiologist offices are read by radiologists who contribute data to the NMMP. During the period of study, there were no other known fixed facilities performing mammography in the Albuquerque metropolitan area. Leakage of patients to facilities outside the catchment area is likely to be small, since the closest facilities are approximately 60 miles away. On the basis of these considerations, ascertainment of mammograms was nearly complete for women who reside in Albuquerque and the five surrounding counties that are served by these radiology groups.
The radiology groups submitted data on all mammograms that had been interpreted between January 1, 1994 and December 31, 1997. This analysis of utilization of mammography is restricted to female residents of Albuquerque and the five surrounding counties. The analysis is focused on women aged 3584 years. The younger women are unlikely to have received mammographic screening studies, and the benefits of screening have not been established for women older than aged 6974 years. We included those aged 7584 years because screening may be a reasonable choice for many women in this age group.
All five radiology groups submitted the name of the patient, date of birth, date of examination, and type and result of the mammogram. Other data items submitted by most groups included gender, ethnicity, specific recommendations for further studies, personal and family history of breast cancer, breast density, estrogen use, and symptoms. When race or ethnicity was not given, it was assigned by using the 1980 Census List of Spanish Surnames and a computer program, GUESS (Generally Useful Ethnic Search System). This method of race or ethnicity assignment has been documented and validated in the New Mexico population (19
21
).
All mammograms in the database were used to compute utilization rates, with the exceptions of additional views, short-term follow-up examinations, and 6-month follow-up examinations, which were counted as part of the preceding mammographic examination and not as separate examinations. We did not attempt to distinguish true screening examinations from diagnostic examinations. Symptomatic and asymptomatic as well as unilateral and bilateral mammograms were included.
Two primary measures of mammography utilization were computed: the screening rate, which is the fraction of the female population that receives a mammogram in a given time period, and the return rate, which is the fraction of women who return for their next mammogram within a specific time interval. The product of the screening rate and the return rate was computed as a measure of routine utilization of mammography in the population.
Average annual mammography screening rates were estimated by dividing the total number of mammograms for the 4-year period by the sum of the four yearly population estimates for 19941997 made by the US Census Bureau (22
). Only one mammogram per calendar year for each woman was counted. This rate can be interpreted as the average proportion of women in the population who received a mammogram in a single calendar year. Rates were computed by age (3549, 5074, and 7584 years) and by ethnic group (American Indian, Hispanic, and non-Hispanic White). To compute biennial screening rates, we divided the time period into two periods of 2-year duration, 19941995 and 19961997, counting only one mammogram per woman for each 2-year period. The population denominator was one-half the sum of the four yearly population estimates.
The proportion of women who returned for a subsequent mammogram within a specific interval of time was computed by using the Kaplan-Meier method for censored data. Follow-up was censored at December 31, 1997. When computing the annual return rate, we used an interval of 15 months to account for variation in community practice patterns. Similarly, for a biennial return rate we used 27 months. A woman could contribute more than one observation to these estimates if she had more than one mammogram in the 4-year period. Restricting the analysis to only one observation per woman did not substantially change the estimated return rates.
A measure of routine annual utilization of mammography was computed by multiplying the annual screening rate by the annual return rate. This product is an estimate of the proportion of women who had at least two mammograms in 2 consecutive years (plus 3 months). Similarly, a measure of routine biennial mammography use was computed as the product of the biennial screening rate and the biennial return rate.
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RESULTS
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Over the 4-year period, 19941997, 234,100 mammograms were performed on 120,048 women who resided in Albuquerque and the five surrounding counties. Sixty-four percent of the women who had mammograms were non-Hispanic White, 28 percent were Hispanic, and less than 3 percent were American Indian. Forty-six percent of the women were aged less than 50 years, 46 percent were aged 5074 years, and 7 percent were aged 75 years or older (table 1).
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TABLE 1. Number of women with at least one mammogram and total number of mammograms for five counties in New Mexico, 19941997
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Less than half of the population of women who are recommended to have yearly mammograms were screened each year (table 2). The annual mammography screening rate was 46 percent for women aged 5074 years, with the highest rate (49 percent) for non-Hispanic White women, followed by 40 percent for Hispanics, and 37 percent for American Indians. Mammography screening rates also varied by age. Approximately one third of the women aged 4049 and 7584 years are screened each year compared with almost half of the women aged 5074 years. This pattern of the highest screening rates for women aged 5074 years was apparent for both non-Hispanic White and Hispanic women. However, American Indian women had a different pattern of utilization, with the highest screening rates (37 percent) for women aged 7584 years. Biennial screening rates were more than 50 percent for most age and ethnic groups (64 percent for women aged 5074 years) and showed a pattern of variation similar to that of the annual rates.
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TABLE 2. Annual and biennial mammography screening rates per 100 women for five counties in New Mexico, 19941997
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Among women aged 5074 years, 82 percent returned for their next mammogram within 27 months, while only 58 percent returned for their next mammogram within 15 months (table 3). Age and ethnicity were again related to annual and biennial return rates. Women aged 5074 years and non-Hispanic White women had the highest return rates for both annual and biennial intervals. Younger women and American Indians had the lowest return rates. The difference in return rates between women aged 5074 years and those aged 7584 years was substantially less than the difference in annual and biennial screening rates.
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TABLE 3. Percent of women returning for the next mammogram within 15 and 27 months for five counties in New Mexico, 19941997
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The percentage of women who regularly used mammography on an annual basis was low in all age groups, especially among Hispanics and American Indians (figure 1). Women aged 5074 years had the highest percentage of annual routine mammography use, ranging from 29 percent in non-Hispanic Whites to 21 percent in Hispanics and 17 percent in American Indians. The percentage of American-Indian women who utilized mammograms annually increased from 12 to 22 percent over the age range 5074 years, and in the age group 7074 years, their utilization exceeded that of Hispanic women. The overall proportion of young women who annually utilized mammography was substantially lower than that of women aged 5074 years. Among women aged 4549 years, the percentage of utilizers was approximately half of that for women aged 5074 years. A sharp decline in routine utilizers was apparent for women aged 75 years or older in each of the ethnic groups. The percentage of women who utilized mammography on a biennial basis was substantially higher than the those for annual utilization (52 vs. 27 percent for women aged 5074 years) (figure 2). The patterns of variation by age and ethnic group were the same as those described for annual utilization.

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FIGURE 2. Biennial mammography use (percent of women) for five counties in New Mexico, NMMP, 19941997.
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DISCUSSION
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We found that the utilization of mammography in our population-based study was low. The percentage of women who routinely used mammography on an annual basis was low in all age groups. We estimated that less than one third of women aged 5074 years, the age group for which annual mammography is uniformly recommended, were routinely screened on an annual basis. Among younger women, the percentage routinely utilizing mammography was half that of women aged 5074 years. Because the efficacy of mammography in the younger age group appears to depend on the interval between examinations, this low rate of routine annual utilization indicates that any mortality reduction in young women may be small (12
, 13
). A sharp decline in routine utilization was also apparent for women aged 75 years or older in each of the ethnic groups. Although biennial utilization rates were higher than annual rates, they were substantially lower than would be desired on the basis of current recommendations.
Initial screening mammograms may detect prevalent cases that are more advanced than are cases detected by subsequent mammograms and are, therefore, less likely to be curable with existing modalities (17
). The effectiveness of regular screening depends on the relation of screening interval, tumor growth rate, rate of progression of breast cancer, and other host factors (12
, 13
). Studies of tumor doubling time suggest that an annual screening interval may be necessary to achieve the maximum benefit of mammography as assessed by reduction in mortality, especially in women aged 50 years or younger (12
, 13
). However, in older women, an 18- or 24-month interval may be as efficacious as an annual interval. On the basis of this study, it appears that routine mammography screening in the community setting is conducted more often on a biennial rather than on an annual basis in the current New Mexico preventive care delivery system. Whether annual use is necessary to maximally reduce mortality in all age groups of women is an open question.
The patterns of utilization of mammography have several implications for breast cancer screening programs and interventions designed to increase utilization. Breast cancer screening has been vigorously implemented for women over age 40 years in American Indian and Hispanic communities by the New Mexico Department of Health, the Indian Health Service, and tribal governments in collaboration with a national Centers for Disease Control and Prevention screening program (23
). The assessment of population coverage of these programs has largely relied on surveillance systems based on self-reports of mammography use. For example, in a telephone survey of American-Indian residents in rural New Mexico, 76 percent of the women over age 40 years reported ever having a mammogram, and a high proportion of women (60 percent) reported following annual screening recommendations (23
). However, our annual screening rates of 37 and 40 percent, respectively, among American-Indian and Hispanic women over age 50 years are lower than estimates based on the results of the telephone survey. It is probable that the higher estimates based on self-report are due to "telescoping" of the time interval between mammograms, a fact that suggests caution be used in the interpretation of data from public health surveillance systems based on self-reported utilization patterns (23
25
). Comparison of estimates of utilization developed from other data with the NMMP estimates may provide useful insights into the strengths and weaknesses of the current public health surveillance system for mammography.
In this study, the proportion of women who returned within a year was much greater than the proportion of the population who were screened each year, indicating that some women have periodic mammograms while others forego mammography. Age and ethnic differences in return rates were substantially less than the age and ethnic differences in the proportion screened each year. This suggests that factors related to ethnicity and age influence the initial choice of screening but are less important for predicting whether utilization will occur on a regular basis. Increasing utilization of mammography to the level needed to achieve a 2530 percent reduction in mortality may require distinct intervention strategies for different age and ethnic groups. For women who use mammography on a less than optimal interval, interventions could profitably focus on reducing the time between mammograms. For women who never use mammography, interventions should focus on reducing barriers to initial use for each ethnic and age group. The barriers of cost, availability, and access have already been substantially lowered by public health programs in New Mexico, especially for minority and low-income groups. The fact that utilization in the state has remained low suggests the existence of other important barriers to both initial and routine use of mammography. Research is needed to identify these barriers and develop intervention strategies that effectively reduce them.
Our investigation has a number of strengths as well as some limitations. We collected population-based counts of mammograms directly from all facilities in the five-county region including and surrounding Albuquerque. A consideration of the geography of the region, the distribution of mammography facilities within the region, and the NMMP's statewide mammography surveillance system suggest that the ascertainment of mammograms was nearly complete for this region during the period 19941997. When ethnicity was not available from mammography records, we assigned it by using validated methods developed by the New Mexico Tumor Registry, which has more than 25 years of experience in establishing population denominators and estimating ethnic-specific cancer rates and mortality rates in New Mexico (26
). Our estimates of screening rates include mammograms performed on both symptomatic and asymptomatic women. The choice to include both sets of mammograms was made because it is often impossible to define the reason for each examination in the current preventive care system and because screening also occurs in women with breast symptoms. If a bias is introduced by the inclusion of both symptomatic and asymptomatic mammograms, estimates of screening will be artifactually high.
Estimating routine utilization of mammography in the community setting presented a number of methodological challenges. We developed a novel method for estimating the routine utilization of mammography by combining estimates of population screening rates and the interval between mammograms. Although we investigated a number of alternative methods for estimating routine use of screening mammography, we chose a method that combines estimates of the annual screening rate (the proportion of the population screened each year) with the annual return rate (the proportion of the population returning within a year). These two rates measure different, but related, aspects of mammography utilization. They can be estimated on the same set of data, as we have done, or can be estimated using different sets of data and different methods. These properties may make our method attractive for public health surveillance, evaluation, and community practice audits.
Our study is limited by our inability to identify women who migrate into or out of the catchment area of the NMMP. The ability to link mammograms performed on the same woman at different facilities may be imperfect, which would lower the rate of routine utilization but increase the screening rate. Migration could also produce an artifactually low estimate of routine utilization. However, because migration is low for a 1- or 2-year period in these age groups, a substantial bias from migration is unlikely for annual or biennial utilization rates. Although American-Indian women may seek mammograms at widely dispersed facilities, our estimates are unlikely to be substantially low because we collected data on most mammograms among American-Indian women in New Mexico.
In conclusion, mammography screening and routine utilization rates in the Albuquerque metropolitan area of New Mexico were much lower in women of all ethnic and age groups than that necessary to achieve a 2530 percent reduction in breast cancer mortality. Further research is needed to identify determinants of initial and routine mammography use, such as physician recommendations, confusion about these recommendations, age and ethnic group differences in the concept of disease, and acculturation factors.
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ACKNOWLEDGMENTS
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Supported by National Institutes of Health grants NO1 CN 05228 and 1 UO1 CA69976 01.
Rita Elliot and Ann Harris provided editorial assistance.
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NOTES
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Reprint requests to Dr. Frank Gilliland, Department of Preventive Medicine, University of Southern California School of Medicine, 1540 Alcazar Street, CHP 236, Los Angeles, CA 90033.
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Received for publication April 22, 1999.
Accepted for publication October 11, 1999.