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Screening Mammography: Do Women Prefer a Higher Recall Rate Given the Possibility of Earlier Detection of Cancer?¹

¹ From the Department of Radiology, University of Pittsburgh Medical Center, 300 Halket St, Imaging Research, Suite 4200, Pittsburgh, PA 15213. Received May 20, 2005; revision requested July 18; revision received August 3; final version accepted September 1. Address correspondence to D.G. (e-mail: gurd{at}upmc.edu).

	ABSTRACT

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Purpose: To prospectively survey women undergoing screening mammography to assess their attitudes toward and preference for the level of recall rates given the possibility that an increase in recall rates may result in earlier detection of cancer.

Materials and Methods: This HIPAA-compliant survey was performed with an institutional review board–approved protocol. Women who arrived for their routine screening mammographic examination from November 2004 to March 2005 were informed before they consented to participate. The distribution of responses for each survey question was summarized, and proportions for the entire group and different subgroups were computed. The z score statistic was used to assess significant differences between subgroups.

Results: Fifteen hundred seventy anonymized questionnaires were collected; 1171 (75%) were from women between 40 and 59 years of age. Of 1528 respondents, 1486 (97%) believed that a false-positive result would not deter them from continuing with regular screening, and most would have been willing to be recalled more often for either a noninvasive (86% [1308 of 1519 respondents]) or an invasive (82% [1248 of 1515 respondents]) procedure if it might increase the chance of detecting a cancer (if present) earlier. Compared with respondents undergoing their initial screening mammographic examination, women who had undergone at least one prior screening examination reported that they were more likely to continue with screening if they had received a previous false-positive result (P = .02). Women younger than 60 years and those previously recalled were more willing to be called back more often for a noninvasive or, when indicated, an invasive procedure (P < .05).

Conclusion: A substantial fraction of women in this study would have preferred the inconvenience of and anxiety associated with a higher recall rate if it resulted in the possibility of detecting breast cancer earlier.

© RSNA, 2006

	INTRODUCTION

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Mammography is considered to be a critically important examination for early detection of breast cancer and is presently the only examination specifically approved by the U.S. Food and Drug Administration to screen for breast cancer in asymptomatic women with unknown risk levels (1). Screening mammography has advanced to an extent that its efficacy in the detection of early breast cancer is by and large recognized and accepted around the world (2). Unfortunately, it is not 100% accurate. It has been estimated that approximately 77.8%–95% of breast cancers are detected with the use of screening mammography (3–6). A cancer may be missed at mammography for several reasons, including but not limited to the following: (a) The cancer is not visible in the image either because of dense tissue or because it is in an unexpected (or "difficult") location, (b) the cancer is subtle and the radiologist does not recognize it against the background structure, and (c) the radiologist sees the cancer but decides its appearance is similar to that of a commonly seen benign finding. Conversely, tissue that is in fact normal or a benign finding may be interpreted as suspicious for a possible cancer, and, as a result, a fraction of women who do not have cancer will be recalled (ie, called back after the screening mammographic examination to undergo additional procedures, such as the acquisition of additional mammographic views, ultrasonography, magnetic resonance imaging, and sometimes, ultimately, needle or surgical biopsy).

Published clinical practice guidelines for radiologists recommend keeping the percentage of women recalled after screening mammography for additional evaluation (the recall rate) at or below 10% to keep costs down and limit anxiety among women (7,8). However, reducing recall rates could have a direct effect on the early detection of breast cancer in that detection of some cancers may be delayed with a decrease in recall rates (9,10). Additionally, it has been documented that recall rates vary greatly among radiologists (11–14). Therefore, it is not clear that we should universally institute a clinical practice in which radiologists are advised to uniformly reduce their recall rates.

It has been documented that women want to be included in the decision-making process for medical tests and want to be directly involved in their health care (15). With this in mind, women may want to choose whether or not they would prefer the inconvenience of a higher recall rate and the associated implications, such as time spent, cost, anxiety, and uncertainty, if it could be demonstrated that the result of the inconvenience would be a chance to detect cancer earlier if it is present. Given the fact that mammography is not a perfect procedure and is not likely to become one, the need to involve women in the decision-making process concerning their own health may be obvious to some yet is frequently not met. We found only three small studies in which women were asked about their feelings regarding the relationship between recall rates, detection rates, and their own preferences (16–18). Thus, the purpose of our study was to prospectively survey women undergoing screening mammography to assess their attitudes toward and preferences for the level of recall rates given the possibility that an increase in recall rates may result in earlier detection of cancer.

	MATERIALS AND METHODS

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Participants
From November 2004 to March 2005, at our main facility and at three of our satellite breast imaging clinics (Magee Womancare Centers, located in Monroeville, Pleasant Hills, and Bethel Park, Pa), where a large number of screening mammographic examinations are performed, we conducted a survey of women's preferences regarding the possible trade-offs between recall and earlier detection. Throughout our practice, the mean age of our screened population is 50.1 years ± 11.2 (standard deviation), our overall recall rate is approximately 11.2%, and the screening-attributable cancer detection rate is 3.5 per 1000 screening examinations. The survey was open for different lengths of time at different sites, was conducted according to an institutional review board–approved protocol, and was compliant with the Health Insurance Portability and Accountability Act. More than one author in consensus was involved in the survey design and/or the data analysis. The originally proposed survey was modified slightly in response to comments from external reviewers and institutional review board members.

Women who arrived for a routine screening mammographic examination at one of the participating facilities were invited to take part in the survey. All eligible women were offered a questionnaire at the time of their arrival and were informed that completion of the questionnaire was entirely voluntary and that their responses would be anonymous. The Appendix contains the survey's introductory paragraph, which explains some of the issues that were being addressed with the survey. However, we recognized that the issues covered are not always simple concepts, and women who consented to participate were instructed to complete the questionnaire to the best of their ability. There was no immediate opportunity for women to ask for help in either understanding or answering a specific question.

Questionnaire
The survey consisted of a two-part questionnaire. Data concerning demographic characteristics, personal and family history of breast cancer, and whether women had previously undergone screening mammography were addressed in Part I of the questionnaire. Part II consisted of questions regarding knowledge and beliefs about mammography, perception of breast cancer risk, attitude about being recalled, and preferences regarding the possibility of an increased chance of being recalled (for additional evaluations either noninvasive or invasive) if by being recalled one might increase the chance of a breast cancer being detected earlier. The last two questions in Part II of the questionnaire (those pertaining to recall preference) were prefaced by brief introductory statements.

For example, question 6 read as follows:

Please read the following statement before you answer the question. The average chance of finding a cancer as a result of screening is approximately 1 out of every 300 patients and to find these cancers approximately 10% of these women are being recalled for additional tests. Question 6: I would be willing to take the chance of being called back more often (for example 15% of the time instead of 10%) for a second noninvasive procedure (such as additional mammogram views or breast ultrasound) if doing so might increase the chance (for example 1 out of 200 instead of 1 out of 300) that if I have cancer it might be detected earlier.

Response choices were (a) strongly disagree, (b) disagree, (c) not sure about it, (d) agree, and (e) strongly agree.

Data Entry and Statistical Analysis
All surveys, which were anonymous with regard to both patient information and facility location, were returned to our laboratory and entered into a database in which responses (and nonresponses) were recorded for each question. We summarized the distribution of responses for each question and computed proportions. For the purpose of analysis, we combined the responses for questions 1, 6, and 7 in Part II of the questionnaire into two categories, as shown in the Figure. The z score statistic with the Yates correction for continuity was used to determine whether there was a significant difference between the proportion of women who would agree to be recalled for a noninvasive procedure and the proportion of those who would agree to be recalled for an invasive procedure (questions 6 and 7) (19).

View larger version (67K): [in this window] [in a new window] [Download PPT slide]   Part II of survey and responses: participant knowledge, beliefs, preferences, and attitudes. No.* = number of participants. Owing to the fact that not all participants responded to all questions, the total number of participants in a given category may be fewer than 1570 (range of rate of nonresponse to a given question, 3%–7%).

	RESULTS

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Questionnaire Part I
A total of 1570 women responded to our survey during the period it was open. The majority of women who responded to the survey (Table 1) were relatively young (1171 of 1563 women were aged 40–59 years), were white (1512 of 1561 women), had at least some college education (1180 of 1560 women), had an annual household income of $35 000 or greater (1268 of 1465 women), reported having no personal history of breast cancer (1538 of 1560 women), did not have a first-degree relative who had or had had breast cancer (1282 of 1562), and had undergone at least one previous screening mammographic examination (1479 of 1561 women). The majority of women who responded (1269 of 1561) had undergone three or more prior mammographic examinations. Additionally, approximately half of the women (679 of 1412) reported that they had been recalled previously. Of the women who reported that they had been recalled previously, 21% (144 of 679) reported that they had undergone an invasive procedure.

Comparisons
Women who had undergone at least one prior screening mammographic examination were more likely than women who were undergoing their initial screening examination to continue with screening if they had experienced a previous recall that resulted in a negative interpretation (P = .02) (Table 2). However, there were no significant differences between women undergoing their initial screening examination and those who had undergone prior screening examinations in terms of the preference for being called back more often for a noninvasive (P = .25) or an invasive (P = .47) procedure if such a recall resulted in an increased chance for earlier detection. Women who had previously been recalled differed significantly from those who had never been recalled in that they were more willing to be called back more often for a noninvasive (P = .003) or an invasive (P = .03) procedure; however, these two groups did not differ in their belief that a false-positive result would not deter them from continuing with their annual screening examination (P = .53). Women with and those without a family history of breast cancer were similar in terms of the likelihood that they would continue to undergo screening examinations (P = .81) and in agreeing to be called back more often for a noninvasive (P = .54) or an invasive (P = .20) procedure. When we compared women younger than 60 years of age with those who were 60 years of age or older, we found no significant differences in their likelihood of continuing screening and their agreeing to be called back for an invasive procedure (P = .54 and P = .15, respectively). However, these two subgroups did differ in agreeing to be called back for a noninvasive procedure (P = .009) in that women younger than 60 years were more willing to be called back for the noninvasive procedure given a possible increase in the rate of detecting cancer (if present) earlier.

	DISCUSSION

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In our study we specifically asked women if they would prefer a higher recall rate if it meant that the chance for earlier cancer detection, if cancer was present, could possibly increase. Overall, we found that women who responded overwhelmingly preferred this trade-off. In addition, this particular preference was quite general to all subgroups—namely, those women who had undergone previous screening mammographic examinations and those who were undergoing their first screening mammographic examination. We also found no difference between women with a family history of breast cancer and women without a family history of breast cancer with respect to this preference. Interestingly, women who had been recalled for additional studies on at least one occasion were more likely to prefer being called back more often for this very purpose, and the overwhelming preference for higher recall rates remained in those who had had previously undergone an invasive procedure.

The results of our study agree with the results of previous studies in that most women are likely to continue with annual screening even if they have experienced recalls for ultimately negative findings (16–18,20,21). We also found that women who had undergone screening examinations in the past were more likely to continue with annual screening than those who had not undergone a previous screening examination. Our results were similar to those reported by Nekhlyudov et al (16) and Silverman et al (17) in that, of women surveyed or interviewed regarding screening mammography, most viewed themselves as having the same likelihood of breast cancer being detected at screening mammography as that of other, similar women. In our study, a smaller fraction (28%) of women overestimated the sensitivity of mammography as compared with the fraction of women (32%–52%) who reportedly overestimated its sensitivity in other studies (22,23). However, in our study, women did overestimate the chance of finding breast cancer at one screening mammographic examination. This overestimation may be the result of women failing to understand clearly the survey question and/or the belief that the risk during one screening mammographic examination is of the same magnitude as a lifetime risk. This issue is an important one and warrants further investigation because it suggests that we may not be doing as good a job as we should in explaining the difference between lifetime risk and the risk of having a cancer detected during a single annual mammographic examination.

Our study had several limitations. First, there was clearly a self-selection bias. The majority of the participants (respondents) were younger than 60 years, were white, had a higher annual income, were educated, had previously undergone screening mammography, and were fairly knowledgeable regarding recall rates and the sensitivity of mammography. Minority women, along with women with less education, lower income, and no history of screening, were underrepresented. Minority women were underrepresented (3.14%) in the participating group largely owing to the specific locations where the survey was implemented. Therefore, our results may not be generalizable to the screening population (all asymptomatic women) as a whole. However, our sample does reflect the population that is more likely to participate in periodic screening.

Second, almost half of the women had been recalled previously. Although this is not unique to screening programs such as ours, in which the majority of participants have undergone several previous mammographic examinations, it may limit the generalizability of our observations. Third, our study may have entailed a nonresponse bias. We do not know how many women chose not to respond to our survey; therefore, we do not know the characteristics of these nonrespondents. Fourth, the wording and style used in the questionnaire could be criticized for either clarity or content; however, from the few personal comments we received from several participants, we assume that the primary goal of subjectively assessing attitudes and preferences was largely achieved. Fifth, the way the survey was conducted—namely, the fact that it was open to all comers at the specific sites during a certain period and active personal solicitation was not performed—may have resulted in a decrease in the overall fraction of respondents and a bias toward the subset of women who were more interested in the specific issues covered in the survey. Last, although we believe this survey was relatively short, we did have questions that were left unanswered. Our highest nonresponse rate for a given question was 10%.

Despite these limitations, we believe that a large fraction of women who actively participate in routine screening mammography would prefer a higher recall rate if it resulted in even a small increase in the probability of earlier breast cancer detection.

	APPENDIX

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The introduction statement to the survey is reproduced below:

Many women are called back for additional tests after their screening mammogram because the radiologist (the doctor that interprets the mammograms) sees a questionable abnormality that needs to be investigated to determine if it could be a breast cancer. In most cases when the woman is recalled for additional tests (sometimes only additional mammogram views are needed, but often breast ultrasound, and less often needle biopsy are needed), the final diagnosis of those additional tests is "No Cancer." In less than 5% of women recalled for additional tests, a breast cancer will be found. If radiologists were to increase the number of women called back for additional tests, only a very small number of additional cancers may be found. This means an even smaller percent of women recalled will be found to have cancer while a greater percent of women recalled will have been inconvenienced only to be told that they do not have breast cancer. However, any additional cancer will have been found 1 year earlier. Radiologists have to decide at what suspicion level the "small" chance of finding a cancer outweighs the burdens of time, cost and anxiety that recalling the woman for additional tests will involve. The benefit of recalling a larger number of women for additional tests, by including patients that radiologists believe have only a small chance of actually having breast cancer, will be for only the additional small number of women whose cancer is detected. Most of these women recalled for less suspicious findings on the screening mammogram will be normal. In this survey, we are asking women who come for yearly breast cancer screening what they think about these issues.

	ADVANCE IN KNOWLEDGE

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• Many women actively participating in screening mammography would prefer a higher recall rate, along with the associated anxiety and inconvenience, if it resulted in even a small increase in the chance that if they had a cancer it would be detected earlier.
  

	ACKNOWLEDGMENTS

 
The authors thank Justin Lazaroff for his diligent and tireless work on this project.

	FOOTNOTES

 
Author contributions: Guarantor of integrity of entire study, M.A.G.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, J.L.K., A.H.K.; clinical studies, J.H.S., V.J.C., C.S.C.; statistical analysis, A.H.K.; and manuscript editing, all authors

Authors stated no financial relationship to disclose.

	References

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