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Three-Year Prospective Adherence to Three Breast Cancer Screening Modalities
27, 781–786 (1998) PM980357
PREVENTIVE MEDICINE ARTICLE NO.
Three-Year Prospective Adherence to Three Breast Cancer Screening Modalities1 Laura J. Solomon, Ph.D.,*,†,2 Ruth M. Mickey, Ph.D.,†,‡ C. J. Rairikar, M.A.,‡ John K. Worden, Ph.D.,†,§ and Brian S. Flynn, Sc.D.†,§ *Department of Psychology, ‡Biometry Facility, §Office of Health Promotion Research and Department of Family Practice, and † Vermont Cancer Center, University of Vermont, Burlington, Vermont 05405
Background. This study prospectively examined rates of adherence to mammography, clinical breast examination (CBE), and breast self-examination (BSE) in a cohort of women over 3 years to determine whether participation in BSE influenced participation in the other two screening modalities. Methods. Women ages 51 and older (n 5 450) who attended a small group educational session to learn BSE and to hear about CBE and mammography guidelines were assessed annually by telephone for 3 consecutive years to determine their subsequent breast cancer screening behavior. Results. Annual CBE and mammography screening are highly positively associated. Regular performance of BSE has a modest positive association with both CBE and mammography adherence over time. Conclusions. Women who perform BSE regularly over time may be more likely to adhere to the other breast cancer screening guidelines. q1998 American Health Foundation and Academic Press
Key Words: breast neoplasms; mammography; breast self-examination; mass screening.
INTRODUCTION
Regular adherence to breast cancer screening is currently the best hope for early detection of breast cancer. Consensus exists within the scientific community on the merits of annual screening mammograms and clinical breast examination (CBE) for women ages 50 and older [1], while the role of breast self-examination (BSE) is more controversial [2–6]. Yet most researchers and 1 This research was supported by Grants CA-46456 and CA-73010 from the National Cancer Institute. The contents of this article are solely the responsibility of the authors and do not necessarily represent the official views of the National Cancer Institute. 2 To whom correspondence and reprint requests should be addressed at the Department of Psychology, Dewey Hall, University of Vermont, Burlington, VT 05405. Fax: (802) 656-8783. E-mail: [email protected].
practitioners agree that rates of repeated participation in the three screening modalities among women 50 and older are lower than desired [7,8]. Several studies have examined retrospectively mammography participation rates among various samples of women [9–13]. Most of these studies relied on retrospective reports over several years to determine screening adherence, making them potentially subject to faulty recall. Prospective studies that identify a cohort of women initially and then follow these women over time hold greater promise for understanding actual screening behavior and factors that predict adherence to screening [9]. Most large prospective studies of adherence to breast cancer screening have been intervention trials designed to examine the efficacy of mammography and/or CBE. These studies, which repeatedly prompted screening participation, found that participation rates were high initially and tended to drop off with repeated screenings. For example, the HIP study [14] found that 60% of women invited to attend annual mammography and CBE screenings for 4 consecutive years actually did so. The Edinburgh trial found a decline in mammography and CBE participation from 61 to 53% over 3 years [15], while Tabar and colleagues [16] in Sweden observed a decrease in attendance from 90 to 82% in the first three rounds of mammography screening. In the Utrecht Project [17] attendance at invited mammography and CBE screenings declined from 72 to 42% over 4 years. Scaf-Klomp and colleagues [18] followed a cohort of Dutch women ages 50–69 for 17 years to determine adherence to invitations to obtain a mammogram every 2 years. Results revealed that regular participation remained higher among women who began screening mammograms earlier (ages 50–53) compared with women who began having mammograms at a later age. Most of the above studies either looked only at mammography participation or examined participation in
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0091-7435/98 $25.00 Copyright q 1998 by American Health Foundation and Academic Press All rights of reproduction in any form reserved.
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SOLOMON ET AL.
mammography and CBE as a packaged screening, occurring at the same medical visit. Therefore, it is not possible from these studies to determine the impact of a woman’s participation in one screening modality on her likelihood of participating in another. Furthermore, very few studies have examined prospectively screening participation rates over several years in all three breast cancer screening modalities: mammography, CBE, and BSE. Only the Canadian National Breast Screening Study [19,20] observed rates of participation in the three screening methods over 5 years among a subset of women 50 to 59 randomized into certain experimental conditions. Some of the women were rescreened annually for BSE competence, but all completed annual selfadministered questionnaires assessing BSE frequency. In all groups, there was a significant increase in the proportion of women reporting BSE 12 or more times in the past year, shifting from 20% in Year 1 to between 50 and 65% in Year 5. However, among women who inconsistently attended CBE screenings compared with consistent attendees, rates of monthly BSE were significantly lower at all time points. Adherence to mammography and CBE ranged from 90% in Year 2 to 87% in Year 5, with only 2 to 3% of the women who obtained a CBE refusing to receive a mammogram. These screening behaviors were heavily prompted within the context of the study, and mammography and CBE were linked for women in the combined condition, making it difficult to determine whether adherence to one influenced adherence to the other. The current study explores the relationships among all three screening modalities in a cohort of women ages 51 and older over 3 years to determine patterns of adherence among the screening behaviors. Unlike many of the prior studies, CBE, BSE, and mammography participation over time was free to vary as a function of naturally occurring influences in the environment. Beyond an initial small group educational session when all participants were trained to do BSE and told of the guidelines for mammography and CBE, no further efforts were made in this study to prompt mammography and CBE screening. Thus, this is the first study to look prospectively at adherence to all three breast cancer screening modalities to examine how adherence to one may influence adherence to the others. More specifically, it is possible that promotion of BSE could be detrimental to the goal of early detection of breast cancer because some women may feel that BSE is an acceptable substitute for mammography or CBE. This study addresses the question whether participation in BSE adversely impacts participation in the other two screening modalities. In light of the controversy regarding the efficacy of BSE, this question is worthy of investigation.
METHODS
Participants Subjects eligible for this study were 591 women ages 51 and older who attended one of a series of communitybased, small group education sessions designed to promote breast cancer screening in Lee County, Florida, in the early 1990s and who completed a telephone interview about their breast screening practices 1 year later. Women were recruited through worksites, organizations, clubs, churches, and neighborhoods. Of the eligible women, 450 (76%) became participants in this study by completing two additional annual telephone interviews. All participants were English-speaking volunteers with no personal history of breast cancer who were trained in BSE and provided with CBE and mammography screening guidelines in the educational session and who received the three yearly telephone interviews to determine their screening activity. The study was approved by the University of Vermont’s Institutional Review Board. The small group educational sessions were 1 h in length, ranged in size from 3 to 30 women (x 5 9.4; SD 5 5.0), and were held in community centers, churches, worksites, civic clubs, and women’s homes. Fourteen women with health or teaching background were trained by project staff to facilitate the group sessions in pairs. In the sessions, BSE technique was modeled and practiced using silicone breast models, CBE and mammography guidelines were discussed, and a 5-min videotape showed what it is like to get a mammogram. For a full description of these training sessions, see Solomon and colleagues [21]. As part of a larger study on BSE maintenance, women were randomized by groups into different BSE maintenance conditions; however, for the purposes of this study we have collapsed across these BSE maintenance conditions to look at the relationships among BSE, CBE, and mammography screening practices over time. After the small group educational session, there were no further attempts within the context of this study to prompt the participants to obtain annual CBEs or mammograms. Assessments Telephone assessments were conducted by an experienced female interviewer who was trained by the principal investigator and who contacted the women 1 year (11 to 13 months), 2 years (23 to 25 months), and 3 years (35 to 37 months) following the small group educational session. Interviews took about 10 min to complete. Each year questions assessed BSE frequency (number of times performed BSE in past 6 months; “regular” BSE was defined as having performed BSE four or more times in the past 6 months), CBE participation (month and year she had her most recent clinical breast exam
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performed by a doctor or nurse), and mammography participation (month and year she had her most recent mammogram). To examine screening behavior over time, we created an adherence variable for each screening modality consisting of three levels: (a) regular adherence (meeting screening criteria for regular BSE or annual CBE or annual mammography each of the 3 years), (b) inconsistent adherence (meeting screening criteria for regular BSE or annual CBE or annual mammography 1 or 2 of the 3 years), and (c) nonadherence (not meeting the screening criteria for regular BSE or annual CBE or annual mammography any of the 3 years). Demographic information (age, education, race, and family history of breast cancer) was collected at the small group education session. At the 3-year interview only, we assessed family income and whether her doctor recommended that she get a mammogram within the past year. Data Analysis PROC GLM and PROC FREQ procedures in SAS [22] were used to examine the demographic characteristics of participants and nonparticipants. The PROC FREQ procedure was also used to examine the rates of participation in the different screening modalities and levels of adherence. We used Cochran’s Q test to examine change in participation rates for each screening modality over time. The g statistic was used to investigate trends among the different levels of adherence to the screening modalities because the levels formed ordered categories. Demographic characteristics among participants by the levels of adherence to different screening modalities were examined using PROC GLM and PROC FREQ procedures. Multiple comparisons were performed using Tukey’s test for continuous measures and using simultaneous test procedures for categorical measures [23]. We addressed the problem of homogeneity of small groups through the use of the statistical software SUDAAN [24]. There were no large design effects (0.9– 1.1), and the results were similar to those obtained from SAS; therefore, only results using SAS are presented. RESULTS
Participants were compared with nonparticipants on demographic information. Participants compared with nonparticipants were significantly younger (M 5 63.5 years versus M 5 65.4 years, respectively; P , .001) and more educated (M 5 13.1 years versus M 5 12.6 years, respectively; P , .001). Both groups were predominantly Caucasian (over 90%), with a comparable family history of breast cancer (27.1% versus 22% among participants and nonparticipants, respectively). Table 1 presents the rates of participation in each screening method each year for all participants. Both CBE and mammography screening showed high and
TABLE 1 Participation Rates for Each Screening Modality at Each Year
Year 1 Year 2 Year 3 Cochran’s Q
% Regular BSE
% CBE in past year
% Mammography in past year
63.0 57.2 54.6 14.3*
76.9 77.8 81.2 2.7
64.3 67.3 65.9 1.7
* P , 0.01.
steady participation rates each year (over 75% participation in CBE and over 60% participation in mammography); however, for BSE, adherence changed over time (P , 0.01). We explored the patterns among the screening modalities to determine whether level of adherence across the 3 years to one screening method was associated with level of adherence across the 3 years to the other screening methods. Table 2 summarizes the relationships among the different levels of adherence. The g statistic was used because the different levels of adherence represent ordered categories. There appears to be modest, but significant relationships between the levels of adherence to BSE and the levels of adherence to CBE and mammography (the confidence intervals TABLE 2 Patterns in Levels of Adherence among the Screening Modalities across the 3 Years BSE adherence CBE adherence
Regular (n 5 175)
Inconsistent (n 5 159)
Regular (%) 69.1 57.9 Inconsistent (%) 26.9 34.6 Nonadherent (%) 2.9 4.4 g 5 0.26; 95% confidence interval (0.11, 0.41)
None (n 5 98) 46.9 36.7 9.2
BSE adherence Mammography adherence
Regular (n 5 175)
Inconsistent (n 5 159)
Regular (%) 46.3 42.1 Inconsistent (%) 41.7 44.1 Nonadherent (%) 12.0 12.0 g 5 0.16; 95% confidence interval (0.02, 0.29)
None (n 5 98) 32.7 45.9 20.4
CBE adherence Mammography adherence
Regular (n 5 266)
Inconsistent (n 5 145)
Regular (%) 62.0 13.1 Inconsistent (%) 32.0 70.3 Nonadherent (%) 5.6 15.2 g 5 0.79; 95% confidence interval (0.71, 0.86)
None (n 5 22) 0.0 13.6 81.8
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do not include zero). In each case, greater adherence to BSE is associated with greater adherence to CBE and mammography. The strongest relationship, however, lies between CBE and mammography. The positive g statistic indicates a trend of higher adherence to CBE being strongly associated with higher adherence to mammography screening. We also examined levels of adherence to CBE and mammography in combination as a single indicator in relation to adherence to BSE because annual CBE and mammography screening is the current recommendation for women over age 50. Not surprisingly, we found that greater adherence to
BSE is associated with greater adherence to the combined indicator [g 5 0.22; 95% confidence interval (0.10, 0.35)]. Table 3 presents the demographic information among the participants for the different levels of adherence to each of the screening modalities. For levels of adherence to BSE, we found no significant differences for any of the demographic characteristics. However, for levels of adherence to CBE and mammography, significant differences were found on age and income, but not on education or family history of breast cancer. Multiple comparisons revealed that participants who adhered
TABLE 3 Demographic Characteristics of Participants at Different Levels of Adherence to Each Screening Modality across the 3 Years BSE adherence Regular Characteristics M age M education % household income Less than $15,000 $15,000–30,000 $30,000 or more % Family history of breast cancer
Inconsistent
None
Mean (SD) or %
n
Mean (SD) or %
n
Mean (SD) or %
n
66.0 (7.8) 13.4 (2.5)
175 173
67.0 (8.5) 13.3 (2.5)
159 158
65.6 (8.8) 13.8 (2.2)
98 98
11.3 38.8 50.0 21.4
9 31 40 21
14.8 39.4 45.8 18.9
21 56 65 33
17.9 40.7 41.4 14.1
25 57 58 22 CBE adherence
Regular Characteristics M age* M education % household income** Less than $15,000 $15,000–30,000 $30,000 or more % Family history of breast cancer
Inconsistent
None
Mean (SD) or %
n
Mean (SD) or %
n
Mean (SD) or %
n
65.4 (7.9) 13.6 (2.5)
266 266
66.6 (8.2) 13.0 (2.5)
145 143
69.4 (9.4) 13.3 (2.2)
22 22
11.2 39.3 49.6 18.6
25 88 111 49
21.7 38.3 40.0 15.2
33.3 47.6 19.1 22.7
7 10 4 5
26 46 48 22
Mammography adherence Regular Characteristics M age*** M education % household income*** Less than $15,000 $15,000–30,000 $30,000 or more % Family history of breast cancer * P, 0.05. ** P, 0.01. *** P, 0.005.
Inconsistent
None
Mean (SD) or %
n
Mean (SD) or %
n
Mean (SD) or %
n
65.1 (8.1) 13.7 (2.5)
186 186
66.5 (7.9) 13.3 (2.5)
197 195
69.0 (9.2) 12.8 (2.7)
61 60
32.7 40.4 26.9 18.0
17 21 14 11
7.7 38.5 53.9 17.8
12 60 84 33
18.1 39.8 42.2 17.9
30 66 70 35
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ADHERENCE TO BREAST CANCER SCREENING
to regular CBE or mammography were significantly younger and had a higher household income than those who did not adhere to annual screening. DISCUSSION
Controversy remains regarding the efficacy of BSE in reducing breast cancer mortality; however, this study addresses the question whether regular performance of BSE among women 51 years and older actually interferes with their participation in annual CBE or mammography screening. Our findings reveal that adherence to regular BSE is associated with a modest increase in the likelihood that older women will adhere to CBE and mammography screening guidelines. Thus, performance of BSE as a health behavior does not substitute for other breast cancer screening activities; instead, it appears that women who perform regular BSE are also more likely to participate in annual CBE and mammography screening over time. Not surprisingly, CBE and mammography participation are highly positively associated over time. This relationship is likely driven by the impact of a physician’s recommendation to get a mammogram, as the physician is often the provider performing the woman’s CBE. Our data from Year 3 revealed a significant association between physician recommendation and mammography participation (odds ratio 5 2.04; CI, 1.35– 3.08), a finding not unique to our study, as physician recommendation is one of the best predictors of mammography screening found in the existing literature [11,12,25,26]. When we examined the demographic characteristics of women as a function of level of adherence to the screening modalities, we observed differences in age and household income for levels of adherence to CBE and mammography. Women obtaining annual CBEs or annual mammograms were younger and had higher household incomes than women not adhering to those screening guidelines. These findings are consistent with observations from the breast cancer screening literature [7,10,11,13]. However, we found no differences in demographic characteristics for level of adherence to BSE, suggesting that in this sample of women BSE adherence was independent of age, income, education, or family history of breast cancer. Several limitations of this study should be noted. First, the subjects were a select group of women who voluntarily participated in a small group education program for breast cancer screening and then received annual telephone contacts for 3 years. Most of these women were non-Hispanic Caucasians with enough interest in the topic to come to a 1-h session. These restrictions would seem to dampen the generalizability of our findings. However, data from a cross-sectional study
looking at African-American women found no relationship between regular BSE performance and annual participation in CBE [27]. At the very least, this suggests that BSE does not interfere with CBE participation in diverse samples of women, although confirmation awaits further research. Second, comparisons between the women who completed all the telephone assessments and the women who did not revealed that participants in our study were significantly younger and more highly educated than nonparticipants. However, the clinical significance of these differences seems minimal, as the difference in age was less than 2 years and the difference in education was only half a year. Finally, data on mammography participation, like those on CBE and BSE, were based on self-reports. Results from several validity studies comparing women’s reports of mammography use to actual mammography records reveal 82 to 94% confirmation of self-report within the past year across diverse samples of women [28–30]. The fact that the longest recall period within our study was 1 year, and only 6 months for BSE, lends confidence to the accuracy of our self-report findings. In conclusion, despite the limitations of a restricted, homogeneous sample, we found the practice of BSE to be modestly positively associated with participation in annual CBE and annual mammography screening in women 51 years and older. These findings should alleviate some of the concerns of critics of BSE who worry that promotion of the practice will hinder participation in other breast cancer screening activities. REFERENCES 1. American Cancer Society. Cancer facts and figures. New York: Am. Cancer Soc., 1996. 2. Foster RS, Worden JK, Costanza MC, Solomon LJ. Clinical breast examination and breast self-examination. Cancer 1992;69 Suppl:1992–8. 3. Gastrin G, Miller AB, To T, et al. Incidence and mortality from breast cancer in the Mama Program for Breast Screening in Finland, 1973–1986. Cancer 1994;73:2168–74. 4. O’ Malley MS, Fletcher SW. Screening for breast cancer with breast self-examination: a critical review. JAMA 1987;257: 2197–203. 5. Newcomb PA, Weiss NS, Storer BE, et al. Breast self-examination in relation to the occurrence of advanced breast cancer. J Natl Cancer Inst 1991;83:260–5. 6. Thomas DB, Gao DL, Self SG, et al. Randomized trial of breast self-examination in Shanghai: methodology and preliminary results. J Natl Cancer Inst 1997;89:355–65. 7. Rimer BK. Mammography use in the U.S.: trends and the impact of interventions. Ann Behav Med 1994;16:317–26. 8. Zapka JG, Hosmer D, Costanza ME, Harris DR, Stoddard A. Changes in mammography use: economic, need, and service factors. Am J Public Health 1992;82:1345–51. 9. Bastani R, Maxwell AE, Bradford C. Cross-sectional versus prospective predictors of screening mammography. Cancer Epidemiol Biomarkers Prev 1996;5:845–8.
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10. Lee JRJ, Vogel VG. Who uses screening mammography regularly? Cancer Epidemiol Biomarkers Prev 1995;4:901–6. 11. Lerman C, Rimer B, Trock B, Balshiem A, Engstrom PF. Factors associated with repeat adherence to breast cancer screening. Prev Med 1990;19:279–90. 12. Rimer BK, Lerman C, Trock B, King E, Engstrom PF. Why do some women get regular mammograms? Am J Prev Med 1991;7:69–74. 13. Zapka JG, Stoddard A, Maul L, Costanza ME. Interval adherence to mammography screening guidelines. Med Care 1991;29: 697–707. 14. Fink R, Shapiro S, Roester R. Impact of efforts to increase participation in repetitive screenings for early breast cancer detection. Am J Public Health 1972;3:328–37. 15. Roberts MM, Alexander FE, Anderson TJ, et al. Edinburgh trial of screening for breast cancer: mortality at seven years. Lancet 1990;335:241–6. 16. Tabar L, Fagerberg G, Duffy SW, Day NE. The Swedish twocounty trial of mammographic screening for breast cancer recent results and calculation of benefit. Epidemiol Community Health 1989;43:107–14. 17. Collette JHA, Day NE, Rombach JJ, deWaard F. Evaluation of screening for breast cancer in a non-randomized study (The Dom Project) by means of a case–control study. Lancet 1984;1:1224–6. 18. Scaf-Klomp W, Van Sonderen FLP, Stewart R, Van Dijck JAAM, Van den Heuvel WJA. Compliance after 17 years of breast cancer screening. J Med Screening 1995;2:195–9. 19. Baines CJ, To T. Changes in breast self-examination behavior achieved by 89,835 participants in the Canadian National Breast Screening Study. Cancer 1990;66:570–6.
20. Miller AB, Baines CJ, To T, Wall C. Canadian National Breast Screening Study. 2. Breast cancer detection and death rates among women aged 50 to 59 years. Can Med Assoc J 1992; 147:1477–88. 21. Solomon LJ, Flynn BS, Worden JK, et al. Assessment of selfreward strategies for maintenance of breast self-examination. J Behav Med 1998;21:83–102. 22. SAS Institute, Inc. SAS/STAT guide for personal computers, version 6. Cary (NC): SAS Inst., 1987. 23. Gabriel KS. Simultaneous test procedures for multiple comparisons on categorical data. J Am Stat Assoc 1966;61:1081–96. 24. Shah BV, Barnwell BG, Bieler GS. SUDAAN user’s manual, release 7.0. Research Triangle Park (NC): Research Triangle Inst., 1996. 25. Fox SA, Murata PJ, Stein JA. The impact of physician compliance on screening mammography for older women. Arch Intern Med 1991;151:50–6. 26. Howe HL. Repeat mammography among women over 50 years of age. Am J Prev Med 1992;8:182–5. 27. Mickey RM, Durski J, Worden JK, Danigelis NL. Breast cancer screening and associated factors for low-income African-American women. Prev Med 1995;24:467–76. 28. King ES, Rimer BK, Trock B, Balshem A, Engstrom P. How valid are mammography self-reports? Am J Public Health 1990; 80:1386–8. 29. Etzi S, Lane DS, Grimson R. The use of mammography vans by low-income women: the accuracy of self-reports. Am J Public Health 1994;84:107–9. 30. 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.
PREVENTIVE MEDICINE ARTICLE NO.
Three-Year Prospective Adherence to Three Breast Cancer Screening Modalities1 Laura J. Solomon, Ph.D.,*,†,2 Ruth M. Mickey, Ph.D.,†,‡ C. J. Rairikar, M.A.,‡ John K. Worden, Ph.D.,†,§ and Brian S. Flynn, Sc.D.†,§ *Department of Psychology, ‡Biometry Facility, §Office of Health Promotion Research and Department of Family Practice, and † Vermont Cancer Center, University of Vermont, Burlington, Vermont 05405
Background. This study prospectively examined rates of adherence to mammography, clinical breast examination (CBE), and breast self-examination (BSE) in a cohort of women over 3 years to determine whether participation in BSE influenced participation in the other two screening modalities. Methods. Women ages 51 and older (n 5 450) who attended a small group educational session to learn BSE and to hear about CBE and mammography guidelines were assessed annually by telephone for 3 consecutive years to determine their subsequent breast cancer screening behavior. Results. Annual CBE and mammography screening are highly positively associated. Regular performance of BSE has a modest positive association with both CBE and mammography adherence over time. Conclusions. Women who perform BSE regularly over time may be more likely to adhere to the other breast cancer screening guidelines. q1998 American Health Foundation and Academic Press
Key Words: breast neoplasms; mammography; breast self-examination; mass screening.
INTRODUCTION
Regular adherence to breast cancer screening is currently the best hope for early detection of breast cancer. Consensus exists within the scientific community on the merits of annual screening mammograms and clinical breast examination (CBE) for women ages 50 and older [1], while the role of breast self-examination (BSE) is more controversial [2–6]. Yet most researchers and 1 This research was supported by Grants CA-46456 and CA-73010 from the National Cancer Institute. The contents of this article are solely the responsibility of the authors and do not necessarily represent the official views of the National Cancer Institute. 2 To whom correspondence and reprint requests should be addressed at the Department of Psychology, Dewey Hall, University of Vermont, Burlington, VT 05405. Fax: (802) 656-8783. E-mail: [email protected].
practitioners agree that rates of repeated participation in the three screening modalities among women 50 and older are lower than desired [7,8]. Several studies have examined retrospectively mammography participation rates among various samples of women [9–13]. Most of these studies relied on retrospective reports over several years to determine screening adherence, making them potentially subject to faulty recall. Prospective studies that identify a cohort of women initially and then follow these women over time hold greater promise for understanding actual screening behavior and factors that predict adherence to screening [9]. Most large prospective studies of adherence to breast cancer screening have been intervention trials designed to examine the efficacy of mammography and/or CBE. These studies, which repeatedly prompted screening participation, found that participation rates were high initially and tended to drop off with repeated screenings. For example, the HIP study [14] found that 60% of women invited to attend annual mammography and CBE screenings for 4 consecutive years actually did so. The Edinburgh trial found a decline in mammography and CBE participation from 61 to 53% over 3 years [15], while Tabar and colleagues [16] in Sweden observed a decrease in attendance from 90 to 82% in the first three rounds of mammography screening. In the Utrecht Project [17] attendance at invited mammography and CBE screenings declined from 72 to 42% over 4 years. Scaf-Klomp and colleagues [18] followed a cohort of Dutch women ages 50–69 for 17 years to determine adherence to invitations to obtain a mammogram every 2 years. Results revealed that regular participation remained higher among women who began screening mammograms earlier (ages 50–53) compared with women who began having mammograms at a later age. Most of the above studies either looked only at mammography participation or examined participation in
781
0091-7435/98 $25.00 Copyright q 1998 by American Health Foundation and Academic Press All rights of reproduction in any form reserved.
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SOLOMON ET AL.
mammography and CBE as a packaged screening, occurring at the same medical visit. Therefore, it is not possible from these studies to determine the impact of a woman’s participation in one screening modality on her likelihood of participating in another. Furthermore, very few studies have examined prospectively screening participation rates over several years in all three breast cancer screening modalities: mammography, CBE, and BSE. Only the Canadian National Breast Screening Study [19,20] observed rates of participation in the three screening methods over 5 years among a subset of women 50 to 59 randomized into certain experimental conditions. Some of the women were rescreened annually for BSE competence, but all completed annual selfadministered questionnaires assessing BSE frequency. In all groups, there was a significant increase in the proportion of women reporting BSE 12 or more times in the past year, shifting from 20% in Year 1 to between 50 and 65% in Year 5. However, among women who inconsistently attended CBE screenings compared with consistent attendees, rates of monthly BSE were significantly lower at all time points. Adherence to mammography and CBE ranged from 90% in Year 2 to 87% in Year 5, with only 2 to 3% of the women who obtained a CBE refusing to receive a mammogram. These screening behaviors were heavily prompted within the context of the study, and mammography and CBE were linked for women in the combined condition, making it difficult to determine whether adherence to one influenced adherence to the other. The current study explores the relationships among all three screening modalities in a cohort of women ages 51 and older over 3 years to determine patterns of adherence among the screening behaviors. Unlike many of the prior studies, CBE, BSE, and mammography participation over time was free to vary as a function of naturally occurring influences in the environment. Beyond an initial small group educational session when all participants were trained to do BSE and told of the guidelines for mammography and CBE, no further efforts were made in this study to prompt mammography and CBE screening. Thus, this is the first study to look prospectively at adherence to all three breast cancer screening modalities to examine how adherence to one may influence adherence to the others. More specifically, it is possible that promotion of BSE could be detrimental to the goal of early detection of breast cancer because some women may feel that BSE is an acceptable substitute for mammography or CBE. This study addresses the question whether participation in BSE adversely impacts participation in the other two screening modalities. In light of the controversy regarding the efficacy of BSE, this question is worthy of investigation.
METHODS
Participants Subjects eligible for this study were 591 women ages 51 and older who attended one of a series of communitybased, small group education sessions designed to promote breast cancer screening in Lee County, Florida, in the early 1990s and who completed a telephone interview about their breast screening practices 1 year later. Women were recruited through worksites, organizations, clubs, churches, and neighborhoods. Of the eligible women, 450 (76%) became participants in this study by completing two additional annual telephone interviews. All participants were English-speaking volunteers with no personal history of breast cancer who were trained in BSE and provided with CBE and mammography screening guidelines in the educational session and who received the three yearly telephone interviews to determine their screening activity. The study was approved by the University of Vermont’s Institutional Review Board. The small group educational sessions were 1 h in length, ranged in size from 3 to 30 women (x 5 9.4; SD 5 5.0), and were held in community centers, churches, worksites, civic clubs, and women’s homes. Fourteen women with health or teaching background were trained by project staff to facilitate the group sessions in pairs. In the sessions, BSE technique was modeled and practiced using silicone breast models, CBE and mammography guidelines were discussed, and a 5-min videotape showed what it is like to get a mammogram. For a full description of these training sessions, see Solomon and colleagues [21]. As part of a larger study on BSE maintenance, women were randomized by groups into different BSE maintenance conditions; however, for the purposes of this study we have collapsed across these BSE maintenance conditions to look at the relationships among BSE, CBE, and mammography screening practices over time. After the small group educational session, there were no further attempts within the context of this study to prompt the participants to obtain annual CBEs or mammograms. Assessments Telephone assessments were conducted by an experienced female interviewer who was trained by the principal investigator and who contacted the women 1 year (11 to 13 months), 2 years (23 to 25 months), and 3 years (35 to 37 months) following the small group educational session. Interviews took about 10 min to complete. Each year questions assessed BSE frequency (number of times performed BSE in past 6 months; “regular” BSE was defined as having performed BSE four or more times in the past 6 months), CBE participation (month and year she had her most recent clinical breast exam
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performed by a doctor or nurse), and mammography participation (month and year she had her most recent mammogram). To examine screening behavior over time, we created an adherence variable for each screening modality consisting of three levels: (a) regular adherence (meeting screening criteria for regular BSE or annual CBE or annual mammography each of the 3 years), (b) inconsistent adherence (meeting screening criteria for regular BSE or annual CBE or annual mammography 1 or 2 of the 3 years), and (c) nonadherence (not meeting the screening criteria for regular BSE or annual CBE or annual mammography any of the 3 years). Demographic information (age, education, race, and family history of breast cancer) was collected at the small group education session. At the 3-year interview only, we assessed family income and whether her doctor recommended that she get a mammogram within the past year. Data Analysis PROC GLM and PROC FREQ procedures in SAS [22] were used to examine the demographic characteristics of participants and nonparticipants. The PROC FREQ procedure was also used to examine the rates of participation in the different screening modalities and levels of adherence. We used Cochran’s Q test to examine change in participation rates for each screening modality over time. The g statistic was used to investigate trends among the different levels of adherence to the screening modalities because the levels formed ordered categories. Demographic characteristics among participants by the levels of adherence to different screening modalities were examined using PROC GLM and PROC FREQ procedures. Multiple comparisons were performed using Tukey’s test for continuous measures and using simultaneous test procedures for categorical measures [23]. We addressed the problem of homogeneity of small groups through the use of the statistical software SUDAAN [24]. There were no large design effects (0.9– 1.1), and the results were similar to those obtained from SAS; therefore, only results using SAS are presented. RESULTS
Participants were compared with nonparticipants on demographic information. Participants compared with nonparticipants were significantly younger (M 5 63.5 years versus M 5 65.4 years, respectively; P , .001) and more educated (M 5 13.1 years versus M 5 12.6 years, respectively; P , .001). Both groups were predominantly Caucasian (over 90%), with a comparable family history of breast cancer (27.1% versus 22% among participants and nonparticipants, respectively). Table 1 presents the rates of participation in each screening method each year for all participants. Both CBE and mammography screening showed high and
TABLE 1 Participation Rates for Each Screening Modality at Each Year
Year 1 Year 2 Year 3 Cochran’s Q
% Regular BSE
% CBE in past year
% Mammography in past year
63.0 57.2 54.6 14.3*
76.9 77.8 81.2 2.7
64.3 67.3 65.9 1.7
* P , 0.01.
steady participation rates each year (over 75% participation in CBE and over 60% participation in mammography); however, for BSE, adherence changed over time (P , 0.01). We explored the patterns among the screening modalities to determine whether level of adherence across the 3 years to one screening method was associated with level of adherence across the 3 years to the other screening methods. Table 2 summarizes the relationships among the different levels of adherence. The g statistic was used because the different levels of adherence represent ordered categories. There appears to be modest, but significant relationships between the levels of adherence to BSE and the levels of adherence to CBE and mammography (the confidence intervals TABLE 2 Patterns in Levels of Adherence among the Screening Modalities across the 3 Years BSE adherence CBE adherence
Regular (n 5 175)
Inconsistent (n 5 159)
Regular (%) 69.1 57.9 Inconsistent (%) 26.9 34.6 Nonadherent (%) 2.9 4.4 g 5 0.26; 95% confidence interval (0.11, 0.41)
None (n 5 98) 46.9 36.7 9.2
BSE adherence Mammography adherence
Regular (n 5 175)
Inconsistent (n 5 159)
Regular (%) 46.3 42.1 Inconsistent (%) 41.7 44.1 Nonadherent (%) 12.0 12.0 g 5 0.16; 95% confidence interval (0.02, 0.29)
None (n 5 98) 32.7 45.9 20.4
CBE adherence Mammography adherence
Regular (n 5 266)
Inconsistent (n 5 145)
Regular (%) 62.0 13.1 Inconsistent (%) 32.0 70.3 Nonadherent (%) 5.6 15.2 g 5 0.79; 95% confidence interval (0.71, 0.86)
None (n 5 22) 0.0 13.6 81.8
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do not include zero). In each case, greater adherence to BSE is associated with greater adherence to CBE and mammography. The strongest relationship, however, lies between CBE and mammography. The positive g statistic indicates a trend of higher adherence to CBE being strongly associated with higher adherence to mammography screening. We also examined levels of adherence to CBE and mammography in combination as a single indicator in relation to adherence to BSE because annual CBE and mammography screening is the current recommendation for women over age 50. Not surprisingly, we found that greater adherence to
BSE is associated with greater adherence to the combined indicator [g 5 0.22; 95% confidence interval (0.10, 0.35)]. Table 3 presents the demographic information among the participants for the different levels of adherence to each of the screening modalities. For levels of adherence to BSE, we found no significant differences for any of the demographic characteristics. However, for levels of adherence to CBE and mammography, significant differences were found on age and income, but not on education or family history of breast cancer. Multiple comparisons revealed that participants who adhered
TABLE 3 Demographic Characteristics of Participants at Different Levels of Adherence to Each Screening Modality across the 3 Years BSE adherence Regular Characteristics M age M education % household income Less than $15,000 $15,000–30,000 $30,000 or more % Family history of breast cancer
Inconsistent
None
Mean (SD) or %
n
Mean (SD) or %
n
Mean (SD) or %
n
66.0 (7.8) 13.4 (2.5)
175 173
67.0 (8.5) 13.3 (2.5)
159 158
65.6 (8.8) 13.8 (2.2)
98 98
11.3 38.8 50.0 21.4
9 31 40 21
14.8 39.4 45.8 18.9
21 56 65 33
17.9 40.7 41.4 14.1
25 57 58 22 CBE adherence
Regular Characteristics M age* M education % household income** Less than $15,000 $15,000–30,000 $30,000 or more % Family history of breast cancer
Inconsistent
None
Mean (SD) or %
n
Mean (SD) or %
n
Mean (SD) or %
n
65.4 (7.9) 13.6 (2.5)
266 266
66.6 (8.2) 13.0 (2.5)
145 143
69.4 (9.4) 13.3 (2.2)
22 22
11.2 39.3 49.6 18.6
25 88 111 49
21.7 38.3 40.0 15.2
33.3 47.6 19.1 22.7
7 10 4 5
26 46 48 22
Mammography adherence Regular Characteristics M age*** M education % household income*** Less than $15,000 $15,000–30,000 $30,000 or more % Family history of breast cancer * P, 0.05. ** P, 0.01. *** P, 0.005.
Inconsistent
None
Mean (SD) or %
n
Mean (SD) or %
n
Mean (SD) or %
n
65.1 (8.1) 13.7 (2.5)
186 186
66.5 (7.9) 13.3 (2.5)
197 195
69.0 (9.2) 12.8 (2.7)
61 60
32.7 40.4 26.9 18.0
17 21 14 11
7.7 38.5 53.9 17.8
12 60 84 33
18.1 39.8 42.2 17.9
30 66 70 35
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ADHERENCE TO BREAST CANCER SCREENING
to regular CBE or mammography were significantly younger and had a higher household income than those who did not adhere to annual screening. DISCUSSION
Controversy remains regarding the efficacy of BSE in reducing breast cancer mortality; however, this study addresses the question whether regular performance of BSE among women 51 years and older actually interferes with their participation in annual CBE or mammography screening. Our findings reveal that adherence to regular BSE is associated with a modest increase in the likelihood that older women will adhere to CBE and mammography screening guidelines. Thus, performance of BSE as a health behavior does not substitute for other breast cancer screening activities; instead, it appears that women who perform regular BSE are also more likely to participate in annual CBE and mammography screening over time. Not surprisingly, CBE and mammography participation are highly positively associated over time. This relationship is likely driven by the impact of a physician’s recommendation to get a mammogram, as the physician is often the provider performing the woman’s CBE. Our data from Year 3 revealed a significant association between physician recommendation and mammography participation (odds ratio 5 2.04; CI, 1.35– 3.08), a finding not unique to our study, as physician recommendation is one of the best predictors of mammography screening found in the existing literature [11,12,25,26]. When we examined the demographic characteristics of women as a function of level of adherence to the screening modalities, we observed differences in age and household income for levels of adherence to CBE and mammography. Women obtaining annual CBEs or annual mammograms were younger and had higher household incomes than women not adhering to those screening guidelines. These findings are consistent with observations from the breast cancer screening literature [7,10,11,13]. However, we found no differences in demographic characteristics for level of adherence to BSE, suggesting that in this sample of women BSE adherence was independent of age, income, education, or family history of breast cancer. Several limitations of this study should be noted. First, the subjects were a select group of women who voluntarily participated in a small group education program for breast cancer screening and then received annual telephone contacts for 3 years. Most of these women were non-Hispanic Caucasians with enough interest in the topic to come to a 1-h session. These restrictions would seem to dampen the generalizability of our findings. However, data from a cross-sectional study
looking at African-American women found no relationship between regular BSE performance and annual participation in CBE [27]. At the very least, this suggests that BSE does not interfere with CBE participation in diverse samples of women, although confirmation awaits further research. Second, comparisons between the women who completed all the telephone assessments and the women who did not revealed that participants in our study were significantly younger and more highly educated than nonparticipants. However, the clinical significance of these differences seems minimal, as the difference in age was less than 2 years and the difference in education was only half a year. Finally, data on mammography participation, like those on CBE and BSE, were based on self-reports. Results from several validity studies comparing women’s reports of mammography use to actual mammography records reveal 82 to 94% confirmation of self-report within the past year across diverse samples of women [28–30]. The fact that the longest recall period within our study was 1 year, and only 6 months for BSE, lends confidence to the accuracy of our self-report findings. In conclusion, despite the limitations of a restricted, homogeneous sample, we found the practice of BSE to be modestly positively associated with participation in annual CBE and annual mammography screening in women 51 years and older. These findings should alleviate some of the concerns of critics of BSE who worry that promotion of the practice will hinder participation in other breast cancer screening activities. REFERENCES 1. American Cancer Society. Cancer facts and figures. New York: Am. Cancer Soc., 1996. 2. Foster RS, Worden JK, Costanza MC, Solomon LJ. Clinical breast examination and breast self-examination. Cancer 1992;69 Suppl:1992–8. 3. Gastrin G, Miller AB, To T, et al. Incidence and mortality from breast cancer in the Mama Program for Breast Screening in Finland, 1973–1986. Cancer 1994;73:2168–74. 4. O’ Malley MS, Fletcher SW. Screening for breast cancer with breast self-examination: a critical review. JAMA 1987;257: 2197–203. 5. Newcomb PA, Weiss NS, Storer BE, et al. Breast self-examination in relation to the occurrence of advanced breast cancer. J Natl Cancer Inst 1991;83:260–5. 6. Thomas DB, Gao DL, Self SG, et al. Randomized trial of breast self-examination in Shanghai: methodology and preliminary results. J Natl Cancer Inst 1997;89:355–65. 7. Rimer BK. Mammography use in the U.S.: trends and the impact of interventions. Ann Behav Med 1994;16:317–26. 8. Zapka JG, Hosmer D, Costanza ME, Harris DR, Stoddard A. Changes in mammography use: economic, need, and service factors. Am J Public Health 1992;82:1345–51. 9. Bastani R, Maxwell AE, Bradford C. Cross-sectional versus prospective predictors of screening mammography. Cancer Epidemiol Biomarkers Prev 1996;5:845–8.
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