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DOI: 10.1148/radiol.2242011370
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(Radiology 2002;224:555-559.)
© RSNA, 2002

Breast Imaging

Clinical Breast Examination Practices among Women Undergoing Screening Mammography1

Katharine M. McGreevy, MPA, Lisa F. Baron, MD and David G. Hoel, PhD

1 From the Departments of Biometry and Epidemiology (K.M.M., D.G.H.) and Radiology (L.F.B.), Medical University of South Carolina, 135 Cannon St, Suite 303, Charleston, SC 29425. From the 2001 RSNA scientific assembly. Received August 13, 2001; revision requested October 9; revision received November 13; accepted January 7, 2002. Address correspondence to K.M.M. (e-mail: mcgreekm@musc.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To determine the proportion of women who underwent clinical breast examination (CBE) within 12 months before undergoing screening mammography and to examine which factors, if any, were associated with having undergone CBE within 12 months before screening mammography.

MATERIALS AND METHODS: A cross-sectional study of 1,135 women presenting for screening mammography was conducted with a self-administered questionnaire. Data were collected regarding sociodemographic information, health care provider information, breast self-examination practices, and CBE history. Data were analyzed with the {chi}2 test of independence.

RESULTS: One hundred forty (38.5%) of 364 nonwhite women and 366 (57.4%) of 638 white women reported having undergone CBE 12 months before screening mammography. This association between race and CBE was statistically significant before (P < .001) and after adjusting for education, age, and type of referring physician (P < .001). There was a statistically significant association between undergoing CBE within 12 months and age (P < .001), type of referring physician (P < .001), and education level (P < .001). Health insurance status was associated with having undergone CBE within the past 12 months, but it was not a statistically significant association after controlling for race.

CONCLUSION: The proportion of women who undergo comprehensive breast cancer screening differs by race, education level, and type of referring physician.

© RSNA, 2002

Index terms: Breast radiography, 00.11 • Cancer screening, 00.30 • Epidemiology


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Breast cancer is one of the leading causes of mortality and is the most commonly diagnosed non–skin-related malignancy among women in the United States (1,2). More than 40,000 women die of breast cancer each year, and more than 180,000 women receive a diagnosis of the disease annually (1). Early detection and timely treatment of breast cancer can have a favorable influence on breast cancer mortality (3). To increase the early detection of breast cancer, the National Cancer Institute, the American Cancer Society, the American Medical Association, and the American College of Radiology recommend annual clinical breast examination (CBE) for women over the age of 40 years as one component of routine breast cancer screening (4–7).

CBE and screening mammography are complementary screening modalities, and each evaluation provides separate and particular sources of information for breast cancer detection (8). An analysis of data from the National Breast and Cervical Cancer Early Detection Program indicates that approximately 5% of the cancers reported in their data set were found only at CBE and were not detected on a screening mammogram (9). Results of randomized trials of breast cancer screening indicate that the sensitivity of the combination of CBE and screening mammography is greater than the sensitivity of screening mammography alone because CBE enables detection of cancers that are not visible on screening mammograms (10). The percentage of cancers detected at CBE but not detected at screening mammography in these randomized trials ranges from 3% to 45% (10–12).

Despite the endorsement of annual CBE in the guidelines of several professional organizations and the increased sensitivity derived from combining this screening modality with screening mammography, previous research has indicated that many women are not undergoing annual CBE as part of routine preventive health care services (13,14). Researchers at the National Cancer Institute’s Breast Cancer Screening Consortium compared breast cancer screening rates among women 65–74 years of age in 1987–1988 and in 1991 and found that as mammography use increased over this period, the use of CBE as a screening modality decreased (14). Investigators in a study conducted at Boston University Medical Center in 1996 found that 24% of women who underwent screening mammography did not undergo CBE within 12 months before or 18 months after screening mammography (13).

Data from the 1992 Behavioral Risk Factor Surveillance System (BRFSS) of the Centers for Disease Control indicated that approximately 38% of women had undergone both CBE and mammography in the year preceding the interview and that the percentage of women reporting having undergone either or both examinations during the preceding year increased with years of education and income but decreased with age (15). Data from the 1997 BRFSS indicated that many women who participate in initial breast cancer screening do not continue to undergo regular screening (3). In 1997, 80% of the surveyed women reported having ever undergone both mammography and CBE, while 65% reported that they had undergone both screenings within the past 2 years (3). The BRFSS researchers called for continued surveillance of the percentage of women who undergo regular breast cancer screening (3).

The aim of this study was to determine the proportion of women who had undergone CBE within 12 months prior to screening mammography and to examine which factors, if any, were associated with having undergone CBE within 12 months prior to screening mammography.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A cross-sectional study of 1,135 women undergoing screening mammography at the Medical University of South Carolina was conducted between August 2000 and March 2001. This is an urban facility that serves individuals from three surrounding counties, with a total population of approximately 553,000. A self-administered questionnaire was given to all women before they underwent screening mammography. Data were collected regarding sociodemographic factors (including age, race, highest education level completed, and insurance status), family history of breast cancer, health care provider information (including type and sex of referring physician), CBE practices (had they undergone CBE, and, if so, date of last CBE), and breast self-examination practices. This study was approved by the institutional review board. Informed consent from the patients was implicitly obtained when they agreed to complete the survey.

The {chi}2 test of independence was used to analyze associations between each of the factors and having undergone CBE within 12 months prior to screening mammography. The Cochran-Mantel Haenszel test of conditional independence was used to test associations between variables and having undergone CBE within 12 months when it was necessary to control for other variables. The Breslow-Day test was used to assess homogeneity across strata. The Cochran-Armitage trend test was used to test for trends with ordinal variables. Statistical analyses were conducted with SAS software, version 8 (SAS Institute, Cary, NC).

Missing data were handled through interpolation. If a woman did not provide the month and year of her last CBE (and did not indicate that she had never undergone CBE), her data were not included in the analysis of time since last CBE. If a woman indicated the year of her last CBE but did not give the month, and the time since her last CBE was more than 1 year, her CBE was assigned the month of June. If a woman indicated that the year of her last CBE was the same year as her screening mammographic examination but did not provide the month, her CBE was assigned the median of the difference between the month of screening mammography and January.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Of the 1,135 completed surveys, 118 were excluded from the analysis. Of these 118 surveys, 58 were excluded because the respondents did not provide any information regarding their last CBE. An additional 60 were excluded because these women were younger than 40 years at the time of screening mammography, and we were interested in determining adherence to the American Cancer Society, National Cancer Institute, American Medical Association, and American College of Radiology guidelines regarding screening with CBE, all of which recommend annual CBE after the age of 40 years.

The mean age of the remaining 1,017 women at the time of screening mammography was 53 years. Approximately 64% of the study population was white, as indicated in Table 1. Fifty-two percent of the women had obtained at least a college degree, and the majority of women had health insurance. Other characteristics of the study population are reported in Table 1. The total numbers of women reporting each characteristic are also listed in Table 1.


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  		TABLE 1. Characteristics of Study Population (n = 1,017)

 
The odds ratios (ORs) of having undergone CBE within 12 months before screening mammography for race, family history, age, type of referring physician, and sex of referring physician are presented in Table 2. Of the 1,017 women reporting, 50.2% indicated they had undergone CBE within the past 12 months. Of the 364 nonwhite women in our study, 38.5% reported that they had undergone CBE within 12 months before undergoing screening mammography; of the 638 white women, 57.4% reported that they had undergone CBE within 12 months before undergoing screening mammography; this association between race and CBE was statistically significant before and after adjusting for education, age, and type of referring physician. There was a statistically significant association between having never undergone CBE and race, with 6% of nonwhite women and 2.5% of white women reporting that they had never undergone CBE (P = .005).


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  		TABLE 2. ORs for Associations between CBE within 12 Months and Race, Family History, Age, and Type and Sex of Referring Physician

 
Older women were less likely to report having undergone CBE within 12 months (P < .001), with a statistically significant decreasing trend (P < .001). Women were more likely to report having undergone CBE if they had been referred by an obstetrician/gynecologist than if they had been referred by a family doctor, internist, or surgeon (P < .001). The sex of the referring physician was not associated with reporting a CBE within the past 12 months (P = .19). A family history of breast cancer was not associated with reporting CBE within the past 12 months (P = .72).

Among those in our study population who reported their health insurance status, 583 (92.0%) of the 634 white women and 281 (78.7%) of the 357 nonwhite women had health insurance. Health insurance status was associated with reporting having undergone CBE within the past 12 months (P < .005); however, after controlling for race, the association was elevated but no longer statistically significant, as indicated in Table 3. Women with lower education levels were less likely to report having undergone CBE within the past 12 months; this association remained significant after controlling for race (P < .001).


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  		TABLE 3. Cochran-Mantel Haenszel ORs for the Association between CBE within 12 Months and Insurance Status and Education Level, Controlling for Race

 
The duration since last CBE at the time of screening mammography is presented in Table 4. Thirty-two percent of the 638 white women and 20% of the 364 nonwhite women reported that they had undergone CBE within 3 months before screening mammography. Three percent of white women and 6% of nonwhite women reported that they had never undergone CBE.


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  		TABLE 4. Time Since Last CBE by Race

 
Data from women who reported their breast self-examination practices for the year preceding screening mammography are presented in Table 5. Of the 1,008 women of all races, 37% reported that they had performed monthly breast self-examination during the past year. Thirty-two percent of the 635 white women and 42% of the 359 nonwhite women reported that they had performed monthly breast self-examination. Sixty-six percent of white women and 71% of nonwhite women indicated that they had performed breast self-examination at least every 3 months. Ten percent of white women and 6% of nonwhite women reported that they had never performed breast self-examination.


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  		TABLE 5. Frequency of Breast Self-Examination in Past Year by Race

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this study, approximately 50% of women undergoing screening mammography reported that they had not undergone CBE within the previous 12 months. This indicates that many women are not undergoing annual CBE as part of routine breast cancer screening as recommended by the National Cancer Institute, the American Cancer Society, the American Medical Association, and the American College of Radiology. Furthermore, nonwhite, less educated, and older women are less likely to report having undergone CBE 12 months before undergoing screening mammography. Women with a family history of breast cancer are not more likely to undergo comprehensive breast cancer screening, as recommended by these national guidelines.

Our finding that nonwhite women are less likely to report having undergone annual CBE is supported by the finding in a previous study of women over the age of 70 that older black women are less likely than older white women to report having undergone CBE within the past 2 years (16). One previous study did not find an association between race and having undergone CBE 12 months before or 18 months after screening mammography (13). One possible explanation is that this study involved 100 women and thus may have lacked adequate power to detect a statistically significant difference. Our finding that insurance status is not associated with reporting having undergone CBE within 12 months is consistent with the findings of this previous study (13).

The decrease in the percentage of women who reported having undergone CBE as age increases is supported by the 1992 BRFSS finding that women in older age groups are less likely to undergo CBE (15). This finding is unfortunate, because older women may greatly benefit from CBE. Screening CBE may be especially useful in older women because fatty changes in breast composition make lump detection easier (10,17). Furthermore, previous research indicates that older women do not accept mammography as readily as do younger women (10,18). Therefore, some older women may be willing to undergo only CBE as a form of breast cancer screening. A previous study did not find an association between age and having undergone CBE 12 months before or 18 months after screening mammography (13). As discussed earlier, this study had a small sample size and may have lacked power to detect this association.

Our findings suggest that women who are referred for screening mammography by an obstetrician/gynecologist are more likely to report having undergone CBE within 12 months previously than are women who were referred by a family doctor, internist, or surgeon. In our study, the sex of the referring physician was not associated with women reporting that they had undergone CBE within 12 months. This conflicts with a previous report that indicated that male physicians were more likely to omit CBE and depend solely on mammography for breast cancer screening (13).

In our analysis, women with a family history of breast cancer were not more likely than women without a family history to report having undergone CBE within the past year. Because a family history of breast cancer increases the risk of breast cancer, early detection strategies are recommended for women with a family history of breast cancer (18). Our results suggest that women with a family history of breast cancer may not be undergoing comprehensive breast cancer screening.

The increase in the percentage of women who reported having undergone CBE within 12 months as education level increased is supported by the 1992 BRFSS findings (15). Our results suggest this trend has remained consistent over the past 8 years. The 1999 BRFSS findings also indicated that women with higher education levels were more likely to participate in breast cancer screening than women with lower education levels (3).

These results suggest that many physicians who refer women for screening mammography are not performing CBE as part of routine breast cancer screening. Previous research has suggested that as the use of screening mammography increases, CBE may be being omitted rather than being used in combination with mammography. Our results provide more recent evidence that women are not undergoing annual CBE.

Screening mammography is a radiologic examination performed to detect unsuspected breast cancer at an early stage in asymptomatic women (19). One implication of women not undergoing CBE before undergoing screening mammography (on an annual basis) is that the radiologists interpreting the screening mammograms may be assuming the women are asymptomatic. Because many women may not be undergoing annual CBE before undergoing screening mammography, it is possible that patients who would be assessed with diagnostic mammography on the basis of abnormal CBE results are undergoing less intensive screening mammography.

In conclusion, physicians referring women for screening mammography need to adhere to national guidelines by performing annual CBE. In particular, physicians need to focus on performing CBE in nonwhite, less educated, and older women. Radiologists interpreting screening mammograms should be aware that many women have not been screened with CBE and hence may not be asymptomatic.

We believe the strengths of our study include a large sample size with adequate power to detect associations between the factors we examined and the outcome of CBE 12 months before screening mammography. This mammography facility is at a major hospital, and the results apply to women throughout the region. Our sample included a racial distribution that is representative of our region. A potential limitation of our study is that it may not be valid to generalize these results to women outside the southeastern region. Furthermore, our sample is not representative of minority women other than blacks.


   FOOTNOTES
 
Abbreviations: BRFSS = Behavioral Risk Factor Surveillance System, CBE = clinical breast examination, OR = odds ratio

Author contributions: Guarantors of integrity of entire study, L.F.B., K.M.M.; study concepts, D.G.H., L.F.B., K.M.M.; study design, K.M.M.; literature research, K.M.M.; clinical studies, L.F.B., K.M.M.; data acquisition, K.M.M.; data analysis/interpretation, D.G.H., K.M.M., L.F.B.; statistical analysis, K.M.M.; manuscript preparation, L.F.B., D.G.H., K.M.M.; manuscript definition of intellectual content, L.F.B., K.M.M., D.G.H.; manuscript editing, L.F.B., D.G.H.; manuscript revision/review and final version approval, L.F.B., K.M.M., D.G.H.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Nass SJ, Henderson C, Lashof JC. Mammography and beyond: developing technologies for the early detection of breast cancer Washington, DC: National Academy, 2001.
  2. National Cancer Institute, DCCPS Surveillance Research Program Cancer Statistics Branch. Surveillance, epidemiology, and end results (SEER) program public-use data (1973–1998) Bethesda, Md: National Cancer Institute, 2001.
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