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Breast Imaging |
1 From the School of Medicine, Department of Radiology (K.K.L.) and the Department of Human and Community Development (J.O., R.A.P.), University of California, Davis, 4860 Y St, Ste 3100, Sacramento, CA 95817. Received January 14, 2000; revision requested February 28; final revision received June 7; accepted July 14. Supported in part by the Breast Cancer Fund of the State of California through the Breast Cancer Research Program of the University of California (grant 1KB-0134). Address correspondence to K.K.L. (e-mail: kklindfors@ucdavis.edu).
| ABSTRACT |
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MATERIALS AND METHODS: A retrospective survey was mailed to women with false-positive screening mammograms that had proved negative or benign at diagnostic imaging. The women were divided into (a) those who had undergone diagnostic imaging during the same appointment as their screening examination and (b) those who had returned at a later date for work-up. The survey included questions about stress that was related to the screening and diagnostic experiences, how subjects had been notified about screening results, and their breast health histories.
RESULTS: From the group that had undergone immediate work-up (n = 100), 50 eligible surveys were received; 71 were received from women who had undergone later work-ups (n = 176). The self-reported overall stress was significantly greater (P = .027) in the group recalled for subsequent diagnostic imaging. Among all respondents, stress from a false-positive screening result was greatest in women younger than 50 years of age with a positive first-degree family history of breast cancer.
CONCLUSION: Providing immediate on-site diagnostic evaluation can reduce the stress of a false-positive screening mammogram.
Index terms: Breast Breast neoplasms, diagnosis, 00.30 Breast radiography, 00.11
| INTRODUCTION |
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Many women experience psychologic distress after an abnormal screening mammogram, even when subsequent diagnostic imaging and/or biopsy yields a benign result (37). Little is known, however, about the factors that influence the perceived level of stress. Some authors (2,8) have suggested that the use of on-site radiologists, who can perform immediate diagnostic imaging work-ups so that women do not have to return for follow-up testing, might reduce the anxiety associated with false-positive screening mammograms. Because this theory has not, to our knowledge, been empirically investigated, we conducted a retrospective survey to evaluate the effect of immediate diagnostic imaging on the stress experienced by women who have false-positive results, as compared with that experienced by women who are recalled for later work-up. A secondary aim of this survey was to identify other factors that might predict anxiety among women with abnormal screening examination findings.
| MATERIALS AND METHODS |
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An anonymous questionnaire (Appendix) was mailed to each subject within 6 weeks after the completion of diagnostic imaging. Demographic information and information about family history of breast carcinoma were ascertained. Women were asked about their screening history, which included whether they had ever had a false-positive screening mammogram or undergone breast biopsy. The surveys included questions about stress that was related to both the screening and diagnostic imaging experiences. Stress was assessed by using a five-point Likert-type scale: A rating of 1 meant "not stressful at all"; 2, "mildly stressful"; 3, "moderately stressful"; 4, "very stressful"; and 5, "extremely stressful." Subjects were asked how and when they had been notified about the screening results and how long the interval between screening and diagnostic imaging had been. They were also asked whether, when told of the need for further testing, they had been given any information regarding the likelihood that the mammographic abnormality represented carcinoma; women who had had such a discussion were asked to recall what had been said.
A brief assessment of dispositional optimism (10), the general tendency to expect positive outcomes in life, was included in the questionnaire so that its potential effect on recalled stress could be evaluated in both groups. This was done to ensure that there was no psychologic bias when women who had undergone immediate work-up were compared with those who had undergone subsequent imaging. Stress was also correlated with optimism in the entire study population.
Respondents were asked to also indicate whether they believed that their feelings, attitudes, or breast health practices had changed as a result of their experience and to comment in their own words about the nature of such changes.
Survey results were analyzed by performing a series of one-way analyses of variance. The dependent variable was overall stress that was associated with the diagnostic experience, from the time that the screening mammogram result had been received until the diagnostic imaging results had been communicated. The stress experienced by the group that had undergone immediate diagnostic examination was compared with that experienced by the group that had undergone later examination.
The educational background, marital status, ethnicity, and annual income levels of the immediate and later work-up groups were compared by performing
2 bivariate contingency table analyses, with a P value of .05, to rule out biases that could have resulted from differences in demographic variables between the groups. The numbers of women with a family history of breast cancer also were compared, as were the numbers of women who had undergone diagnostic work-up for previous false-positive mammograms or had a history of previous breast biopsy. The mean ages of the women in each group were compared by performing the Student t test. Finally, all of these demographic and health history variables were examined separately for their possible effect on the outcome measure of stress by performing one-way analyses of variance.
The influence of patient-provider communication on stress was assessed in the group that had undergone later imaging by examining who (radiologist, primary care provider, other) had notified the subject and what, if anything, had been said about the probability that the mammographic abnormality actually represented breast cancer. Within the later work-up group, responses were analyzed by performing one-way analyses of variance to determine whether the method of communication (ie, mail, telephone, or in person) or interval between screening and receipt of results had influenced stress.
Patient responses to whether their feelings and attitudes about breast health and disease would, in the future, change their breast health practices were examined to determine whether more women in one group reported such changes. Among those who reported such changes, comments were categorized into several general themes; descriptive trends in the types of changes were sought.
| RESULTS |
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The 121 women in the study ranged in age from 30 to 91 years (mean age, 54 years). More than 79% (94 of 117) had at least some college education. In the study sample, 11% (13 of 116) were single or had never been married, 60% (70 of 116) were married, 18% (21 of 116) were separated or had been divorced, 9% (11 of 116) had been widowed, and 1% (one of 116) had reported "other" marital status. Annual household income had been reported in $10,000 increments; 40% (44 of 110) of study participants had an income of $49,000 or less. Of the respondents, 79% (89 of 113) were white, 8% (nine of 113) were Hispanic, 6% (seven of 113) were African American, 7% (eight of 113) had reported another ethnicity, and 7% (eight of 121) did not state their ethnicity. With respect to these demographic variables, there were no significant differences between the group that had undergone immediate work-up and the group that had undergone subsequent imaging.
All women had been asked to rate the stress of the overall experience from the time they had received the screening mammography results until they had received the follow-up examination results. Women who had undergone immediate diagnostic work-up experienced significantly less stress than did those who had undergone later diagnostic imaging evaluation (P = .027). The mean overall stress rating in the group that had undergone immediate work-up was 2.30 on a scale of 1 ("not stressful at all") to 5 ("extremely stressful"). In the group that had returned for subsequent diagnostic imaging, the mean stress rating was 2.79. Both means were in the mild to moderately stressful range (Fig 1).
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To test the possibility that group differences in stress might have been influenced by group differences in dispositional optimism, an analysis of variance of optimism in the diagnostic groups was performed. There was no significant difference in the dispositional optimism between the group that had undergone immediate diagnostic evaluation and the group that had undergone later imaging (P = .097).
The overall stress of the experience in the group that had undergone diagnostic procedures later did not vary significantly with the amount of time that had elapsed between screening and diagnosis (P = .23). Follow-up tests had been completed within 2 weeks of screening for 33% (22 of 66) of these subjects and within 4 weeks for 80% (53 of 66).
Because it may not be possible or preferable to offer immediate diagnostic imaging to all patients with abnormal screening mammograms, other predictors of stress were sought for the survey population as a whole. Education, income, ethnicity, marital status, and dispositional optimism had no significant effect on the stress experienced by women; however, age did have a significant effect (P = .037) on stress (Fig 2). Age and stress were negatively correlated; thus, younger women experienced significantly greater overall stress from a false-positive mammogram than did older women (P = .037). The stress among younger women was not due to inexperience with recalls for diagnostic imaging; there were no significant differences in the number of women who had experienced prior false-positive screenings when analyzed in accordance with decade of life (P = .836).
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Among those women who had undergone later evaluation of an abnormal screening mammogram, 72% (47 of 65) had been advised by telephone of the need to return for subsequent imaging; 11% (seven of 65) had been notified by mail, 9% (six of 65) had been notified in person, and 3% (two of 65) did not remember how they were notified. Sixty-eight percent (46 of 68) had received the results of their screening examination within 1 week after screening. A majority of women had been advised of their screening results by their referring physicians; 36% (25 of 70) had reported that they had been advised by nonphysicians (eg, nurses, receptionists). The overall stress of the breast imaging experience was not significantly associated with who had notified the woman of her results, how those results had been communicated, or the amount of time that had elapsed between the screening examination and the receipt of its results.
When notified of the need for further imaging to clarify an abnormal screening result, most women had not been given any information regarding the probability that the abnormality represented breast cancer; 16% (18 of 114) of the total study population (11% [five of 46] in the immediate work-up group and 19% [13 of 68] in the delayed work-up group) reported having had such a discussion. In all cases in which such a discussion had ensued, subjects reported having been told that the probability of breast cancer was "very low" or that the abnormality was "highly unlikely" to be breast cancer. The overall stress of the diagnostic imaging experience was, however, significantly greater (P = .045) among women who had reported a discussion of the likelihood that the abnormality would result in a diagnosis of breast carcinoma, even though they had been told that this was very unlikely. The mean stress rating in the group that had reported a discussion of the probability of malignancy was 3.11; in the group that had not reported such a discussion, the mean stress rating was 2.51.
In response to the question about whether their feelings or attitudes about breast health and disease had changed as a result of their false-positive screening experience, 40% (44 of 109) indicated that there had been a change. There was no significant difference in affirmative answers between the group that had undergone immediate work-up and the group that had returned for later evaluation (P = .559). When subjects were asked whether they believed their breast health practices would change in the future as a result of their experience, 63% (71 of 112) of the women responded that their health practices would not change, whereas 37% (41 of 112) indicated possible changes. Again, the responses did not differ significantly between groups (P = .131). Women were also invited to respond to open-ended questions about the nature of any perceived changes in feelings, attitudes, or behavior. General themes emerged from a review of these comments and included (a) an enhanced sense of vulnerability to breast cancer, (b) an appreciation of the importance of breast cancer screening, and (c) the intent to become more vigilant about screening in the future; however, too few written comments were provided overall to conduct meaningful quantitative analyses or compare content between the comments of those in the immediate and the later work-up groups.
| DISCUSSION |
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Women in both the immediate and later work-up groups reported their breast imaging experience as mildly to moderately stressful on the average. However, the distribution of reported stress levels in each group showed that the highest percentage of women in the delayed work-up group (33% [23 of 70]) reported "moderate" levels of stress, whereas the highest proportion of women in the immediate work-up group (38% [19 of 50]) reported their experience as only "a little" stressful. Moreover, the proportion of women who reported their experience as "very" stressful was more than twice as high in the later work-up group (17% [12 of 70]), as compared with that in the immediate work-up group (8% [four of 50]). Because the observed difference in mean stress levels could not be attributed to group differences in family breast cancer history, prior screening history, dispositional optimism, or any of the sociodemographic characteristics measured in this study, this difference likely reflected the differential effects of the timing of the diagnostic imaging examination. A reduction in stress appeared to be a function of the immediate work-up because there were no significant differences in stress as a function of the length of time to diagnosis within the group that had returned for later evaluation; stress did not appear to increase in a linear fashion with increased time to final diagnostic disposition.
This survey was completed prior to the implementation of the final regulations of the Mammography Quality Standards Act (MQSA); hence, most of the women who had undergone a later diagnostic evaluation had been notified with a telephone call from their provider of the need to return for additional work-up. Few women had been notified by mail. Stress was not related to the method of notification, although the number of respondents who had received letters was small. Today, all women are notified of their results by mail in accordance with MQSA regulations; for women who need further assessment, letters are sometimes preceded by a telephone call from their health care provider, although this practice may be declining. Further study is necessary to determine whether the changes in patient notification will affect the level of anxiety experienced by women who undergo mammographic screening.
Batch reading of screening mammograms has been promoted as a method to reduce costs (1113); however, later interpretation has additional benefits. Screening mammography is performed in asymptomatic women, most of whom will have normal findings. For the interpreting radiologist, finding the rare early breast cancer on these mammograms requires intense concentration; the pressure of a waiting patient can reduce the radiologists ability to focus on the images. Later reporting of screening mammograms also allows for consensus double reading, which may improve sensitivity (14) and diminish callbacks (15). Results of a recent survey showed that women would prefer later interpretation of their screening mammograms if it meant that double reading would be performed (16). Dissemination of information regarding the benefits of later interpretation may increase patient acceptance, although it is not likely that the stress of a recall for diagnostic examination will be affected.
Education about the low probability that a recall for diagnostic imaging will ultimately yield a diagnosis of cancer should reduce anxiety; however, in this study, women who had had any type of discussion regarding this issue experienced higher stress levels. This may indicate that education on screening outcomes, which include false-positive results, should receive more general public attention at times when women are less focused on their own individual health.
Younger women in this study found false-positive screening mammograms to be more stressful than did older women. These findings are consistent with those of other studies (17,18) in which age was found to be related to an emotional response to breast health issues, with younger women having greater distress. It is likely that there are developmental and situational reasons for the anxiety experienced by younger women. First, a breast cancer diagnosis might be considered a more untimely event in the life of a younger woman, who might have children at home or be establishing a career. Second, younger women are new to the screening population and have had greater exposure to the recent widespread energetic campaigning and public education regarding breast cancer, risk factors, and the importance of screening. Whereas these efforts have improved adherence to screening guidelines, they have also resulted in a falsely high sense of vulnerability among younger women (19). It is also possible that, although there were no differences according to decade of life in the number of women who had themselves received prior false-positive screening results, in the current study, older women knew more other women who have experienced recalls with subsequent negative diagnoses, and this could allay their anxiety.
To reduce patient anxiety, some breast imaging practices may desire to perform immediate on-site diagnostic imaging for abnormal screening results in those women most likely to experience distress. In this survey, women younger than 50 years with a positive first-degree family history of breast cancer experienced significantly greater stress than did all others. Women with a personal history of breast cancer were excluded from the current study; it is unknown whether they, too, might benefit emotionally from immediate interpretation and diagnostic imaging.
In their open-ended comments regarding whether their feelings or attitudes about breast health practices had changed as a result of their false-positive mammogram experience, none of the respondents who provided comments indicated that they would discontinue screening. A number of women reported an increased sense of vulnerability to breast cancer. Some mentioned that they intended to become more vigilant about maintaining a regular schedule of mammography and breast self-examination. A self-selection bias among the women who participated in this study cannot be excluded; perhaps women who chose not to respond represented a population whose experiences deterred them from future screening. However, the comments obtained from this sample are consistent with findings from other research studies (17,20,21).
A possible source of bias in this retrospective study was the unequal questionnaire response rates; in the group that had undergone immediate work-up, there was a 50% response rate (50 of 100 women), as compared with a 40% response rate (71 of 176 women) in the group that had undergone later diagnostic evaluation. The differential response rates did not reflect differences in sociodemographic characteristics between the groups but might have been due to other confounding factors. For example, it is possible that, among women who had returned for later diagnostic evaluation, there were fewer respondents because some women had not wished to revisit a stressful experience. Because the questionnaire was answered anonymously, it was not possible to further assess the reasons for nonresponse.
Only those women with false-positive screening mammograms that had subsequently been shown at diagnostic evaluation to be negative or demonstrate unequivocally benign findings (BI-RADS category 1 or 2) (9) were considered in this study. Because the major focus was to evaluate the effect of immediate versus later work-up in women with false-positive screenings, women with probably benign findings who had undergone short-interval follow-up examinations and those who subsequently had benign biopsies were excluded; the potential anxiety surrounding those procedures would likely have confounded our ability to assess the effect of the timing of diagnostic imaging.
The results of this survey show that performing immediate diagnostic imaging can reduce the stress of a false-positive mammogram; they also show that women younger than 50 years with a positive first-degree family history of breast cancer feel the greatest distress after receiving a false-positive screening result. However, patient anxiety is not the only consideration in deciding whether to offer on-site screening interpretation with immediate diagnostic evaluation; the lower cost and potential for improved sensitivity of mammography with later interpretation also must be taken into account. These issues deserve further study so that there is empiric information to aid practices in balancing competing interests so that they may deliver the highest quality of care.
| APPENDIX |
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Study of Womens Mammography Experiences
Directions: Please answer the questions below about your experience of having a mammogram within the past month that required follow-up tests. It will be most helpful if you answer all of the questions that apply to your experience; any additional information or comments about your experience will be read and appreciated by our research team. Please return this questionnaire in the enclosed, postage-paid envelope within the next 10 days. It is not necessary to put your name or any identifying information on either this questionnaire, or the return envelope. Thank you for your help with this study.
I was informed in person
I was notified on the telephone
I was notified by mail
Not sure, or dont remember
Immediately after the mammogram, at the same appointment
Later on the same day as my mammogram
Within a few days of having the mammogram
About a week after the mammogram
More than a week after the mammogram
Not sure, or dont remember
Doctor where the mammogram was done (radiologist)
My own doctor (primary care or family practice doctor)
A surgeon
Not sure, or dont remember
Other (please explain)
Not stressful at all
Mildly stressful
Moderately stressful
Very stressful
Extremely stressful
Additional X-rays
Ultrasound (sonogram)
Biopsy
Other (please explain)
Dont remember
Same day
Within one week
12 weeks later
23 weeks later
34 weeks later
4 or more weeks later
Not sure, or dont remember
Other (please explain)
Doctor where the follow-up tests were done (radiologist)
My own doctor (primary care or family practice doctor)
Not sure, or dont remember
Other (please explain)
Yes
No
Not sure, or dont remember
Not worried at all
A little worried
Moderately worried
Very worried
Extremely worried
Not stressful at all
A little stressful
Moderately stressful
Very stressful
Extremely stressful
Not stressful at all
A little stressful
Moderately stressful
Very stressful
Extremely stressful
Not stressful at all
A little stressful
Moderately stressful
Very stressful
Extremely stressful
No, my feelings and attitudes did not change as a result of my experience.
Yes, I believe my feelings or attitudes changed in the following way(s): (Please describe in your own words)
No, my breast health behavior did not change as a result of my experience.
Yes, I believe my breast health behavior changed in the following way(s): (Please describe in your own words)
years
8th grade
Some high school
High school graduate
Some college
College graduate
Some graduate or professional school
Graduate or professional degree
Single/never married
Married and living with spouse
Separated/divorced
Widowed
Other:
Less than $20,000
$20,000 $29,999
$30,000 $39,999
$40,000 $49,000
$50,000 $59,999
$60,000 $69,999
$70,000 or above
Yes
No
Not sure, or dont remember
Yes
No
Not sure, or dont remember
Needle biopsy
Surgical biopsy
Not sure
Yes
No
Not sure/dont know
Yes
No
Not sure/dont know
In addition, subjects completed a questionnaire on their outlook on life (Fig A1).
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| FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, K.K.L.; study concepts, K.K.L.; study design, K.K.L., J.O., R.A.P.; definition of intellectual content, K.K.L.; literature research, K.K.L., J.O.; clinical studies, K.K.L., J.O.; data acquisition, K.K.L.; data analysis, K.K.L., J.O., R.A.P.; statistical analysis, J.O., R.A.P.; manuscript preparation, K.K.L.; manuscript editing, K.K.L., J.O., R.A.P.; manuscript review, K.K.L., J.O.
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