Hafslund, Bjorg MSc; Espehaug, Birgitte PhD; Nortvedt, Monica W. PhD
Organized mammography screening has become part of routine healthcare in Norway and has been offered to every woman aged 50 to 69 years since 2005. Mammography screening targets apparently healthy women, and ensuring that the screening does more good than harm is therefore important. Moreover, women invited for screening should be fully informed of both the benefits and negative effects.1 One such potential negative effect is adverse mental effects. Many authors have highlighted the potential negative mental effects of screening and recall after screening for those with positive results in screening that turn out to be false-positive and those who get a cancer mammae diagnosis.2–8
Some prospective studies on routine screening have reported an increased short-term effect as anxiety among the women recalled for what turn out to be false-positive results.2,4,6 Increased anxiety has also been found 2 to 3 months after screening,2,3,5,8,9 and this was statistically significant in 2 studies.5,8 A study in Sweden found a contradictory result at 3 months, with less anxiety, although this was not statistically significant.6 Furthermore, less anxiety (but not statistically significant) was reported2,7,8 as a long-term effect at 6 to 12 months after screening.
False-positive results have not been conclusively linked to increased depression. Follow-up studies have found increased depression both at 2 to 3 months2,3,8 and 6 to 12 months after screening,2,8 but the last reports were not statistically significant. Jatoi et al5 found significantly more depression, but the time for assessment varied. A follow-up study by Gibson et al10 also found increased depression among nonwhites. In contrast, less depression has been found at 2 to 3 months,6,9 and Lampic et al6 found significantly less depression. Lampic et al7 found significantly less depression 12 months after screening. Other studies of mental effects look for mental distress,3,11 symptoms of global distress,9 or worry and intrusive thoughts.2,9,12
One prospective cohort study found worse health-related quality of life (HRQOL) after receiving a false-positive mammogram,13 but only single questions were used. Being recalled for further examination after screening reduced women’s HRQOL for some months, but they reported the same HRQOL as women with negative screening results at 6 months after screening. Bonomi et al14 obtained HRQOL values associated with mammography screening for use in cost-effectiveness analysis. Women rated how clinical scenarios affected HRQOL, rating receiving a false-positive diagnosis as 48.5 points in a possible range of 0 to 100.
Many previous studies have focused on anxiety or worry. The mental variables for mammography screening are fragmented, and the findings are discrepant. In many cases, the psychological approaches to mammography screening are being hampered by the lack of adequate instrumentation and are presented as single questions or subscales. Very few studies have focused on depression and mammography screening, and no study has assessed changes in HRQOL using a validated measure, although several authors have recommended this.14,15
The lifetime risk for a woman having a false-positive screening outcome is 21% in Norway if she participates biannually in 10 screening rounds from 50 to 69 years of age.16 Kalager et al17 reported that mammography screening has reduced the mortality rate from breast cancer to 10% in Norway instead of the approximately 30% expected. Lower mortality from breast cancer and the ongoing discussion of overdiagnosis in mammography screening1 underlines the importance of high quality in the screening program. Furthermore, women today inform themselves through the Internet and mass media and will ask for updated evidence. Because the screening program includes many women, any negative and positive screening effects should be highlighted. Finally, new screening methods such as digital mammography may increase the sensitivity of mammograms. This might lead to more false-positive screening outcomes.18,19
Our study was intended to extend the literature as follows: (1) we have conducted a longitudinal study that includes both general measures of HRQOL and mental effects; (2) assess HRQOL, anxiety, and depression within the same study, which allows for an evaluation of the impact of HRQOL, anxiety, and depression on organized screening.
In Norway, organized mammography screening is in line with public health policy, and the Ministry of Health and Care Services has initiated a research-based evaluation of the program, which is administered by the Research Council of Norway.20 A national expert and counseling group is set to monitor, among several issues, women’s experience of organized mammography screening.21 However, one topic not investigated/not well understood is women’s health status and well-being as recalled after ordinary screening, and this study was carried out for that purpose. Discrepancies found on mental effects on recall and further follow-ups recommend well-designed studies to facilitate health policy decisions regarding screening.
The overall aim was to examine the association between false-positive mammography results and changes in anxiety and depression among the women recalled because of findings in the mammogram and any changes in their HRQOL. The specific research questions were as follows: (1) Do women report any changes in anxiety and depression before screening, at recall, and at follow-up 3 and 6 months later? (2) Do women report any changes in HRQOL before screening, at recall, and in follow-up until 6 months later? These findings were compared with those from a matched group of women with negative results (control group) participating in the same screening cohort.
A descriptive longitudinal study design was used. Health-related quality of life, anxiety, and depression were measured among women recalled because of false-positive or positive results after organized screening; the measures were at recall and at 3 and 6 months later and a baseline measurement before screening (Figure). The recalled participants were recalled because of a positive mammogram, which could be benign or malignant findings, or suspect findings, which turned out to be either negative (no cancer) or positive (cancer), or they were recalled because of technical reasons that ordinary need a new mammography. Short-term consequences of false-positive mammography are up to 3 months after being recalled for further examinations. Long-term effect of recall was measured 6 months after the recall.
Figure. Flow diagram...Image Tools
Participants and Procedures
Of the cohort of 7801 women attending screening, 4249 women completed the questionnaire before screening. Altogether, 246 women of the screening cohort were recalled for further examination in Hordaland and Sogn and Fjordane Counties, Norway. The data were collected from 2007 until early 2008. The recalled participants were asked to take part in the coming data collection because of the study design. The flow of participants throughout the study is illustrated in the Figure. The recall visit occurred within approximately 2 weeks after screening. The follow-up procedures performed were new mammograms, ultrasound, or biopsy (either fine-needle aspiration biopsy or open biopsy). Our sample was not specified as to the follow-up procedure.
Before screening, the study cohort received the questionnaire and information on the study design and the purpose of the study and that participation was voluntary. The researcher sent the questionnaires to the participants’ home address before screening and at 3 and 6 months after screening. For data collection at recall, the researcher sent the questionnaires along with the recall letter by the breast diagnostic centers. The respondents returned the questionnaire to the radiographers when attending before screening and at recall and in a prepaid envelope to the researcher at 3 and 6 months. Because of the study design, no reminders were sent for the data collection before screening and at recall, but in the other cases, a reminder was sent 2 weeks later to nonrespondents. If still not returned, the participant was assumed to have withdrawn from the study.
Of the participants with negative results, 229 were asked to complete the questionnaire 6 months after screening. The control group was matched to the participants for age and geographical location before screening.
The Short-Form 36 (SF-36) Health Survey and the Hospital Anxiety and Depression Scale (HADS) were used. Ware and Sherbourne22 developed the SF-36, and Zigmond and Snaith23 developed the HADS. The background questions included such sociodemographic characteristics as level of formal education (lower-secondary school [9 years], upper-secondary school [12 years], or college or university [≥15 years]), occupation (senior vs junior position), number of children, and smoking status (smoker vs nonsmoker). The Norwegian Cancer Registry supplied information about age and place of residence.
SF-36 HEALTH SURVEY
Generic health measures such as the SF-36 assess health concepts that represent subjective health, also called HRQOL,24 and the HRQOL outcomes are known to be most directly affected by any health interventions.25 It contains 36 questions covering 8 health domains or that can be summarized into 2 higher-order clusters summary scores.26 The 8 SF-36 scales are physical functioning, role-physical, bodily pain, and general health, which comprise the physical summary score; and vitality, social functioning, role-emotional, and mental health, which comprise the mental summary score. The possible scores range from 0 to 100, a high score indicating better health status.26 For respondents missing 1 or more responses on SF-36, the missing values were imputed according to the guidelines of Ware and Kosinski.26 Missing substitution was performed to calculate the score for dimensions when less than 50% of the questions were unanswered. If a respondent was missing any SF-36 scale, the component scale score was set to missing.26 Cronbach α for internal consistency was .88 in this study. The Norwegian acute version 2 of the SF-36 scale standard version was used for this study. The SF-36 has been translated, validated, and tested cross-culturally among Norwegians.27
HOSPITAL ANXIETY AND DEPRESSION SCALE
Based on extensive reviews from more than 700 published studies using HADS, Bjelland et al28 concluded that HADS performs well in assessing the symptom severity and caseness of anxiety disorders and depression in, for example, primary care patients and the general population. Hospital Anxiety and Depression Scale has 2 subscales, each containing 7 items calculating anxiety (HADS anxiety) and depression (HADS depression) subscale scores. Each item is scored from 0 to 3, and the maximum score is 21 for both anxiety and depression. For respondents missing 1 to 2 items on HADS anxiety or HADS depression, the missing values were replaced by the mean of the completed item scores. This was done by multiplying the score by 7/5 if 5 of the 7 questions were answered and by 7/6 if 6 questions were answered. Higher scores on the scales indicated higher levels of anxiety and depression. Caseness is usually defined by a score of 8 or greater, and this was also done here. This cutoff level has been shown to optimally balance sensitivity and specificity on receiver operating characteristic curves.28 Cronbach α for internal consistency was .76 in this study.
The Regional Ethics Committee approved our study (approval no. 143.06), as did the Norwegian Social Science Data Services in accordance with the stated terms (approval no. 15226).
Descriptive analysis was performed among women with false-positive and negative results, with percentages reported for categorical data and means and SDs for continuous data; χ2 tests with estimated Φ and Cramer’s V correlations and independent-sample t tests were conducted to evaluate demographic differences in the 2 groups. Linear mixed-effects model analyses were performed to compare anxiety, depression, and SF-36 scores before screening with scores at recall and at 3 and 6 months after screening for the false-positive group and with those 6 months after screening for the negative group. The test results for group differences could be established for scores before screening and 6 months after screening. Level of education and occupation, smoking status, age (continuous), and number of children (continuous) were included in the model as fixed factors. The estimated regression coefficients were reported with 95% confidence intervals and 2-sided P values. P < .05 were considered statistically significant. All statistical analysis was conducted using IBM PASW Statistics 18 (IBM Corporation 2010, Armonk, New York).
Altogether, 246 recalled women were sent the questionnaire before the recall date, and 141 women who were positive or false-positive returned the questionnaire (response rate, 57%) (Figure). Four questionnaires were not completed. Of the women recalled, 128 had false-positive results, and 13 were positive results. At the data collection 3 months after screening, the 128 women with false-positive results were sent the questionnaire, and 91 women completed it (response rate, 71%). Two questionnaires were returned with the addressee unknown. At 6 months after screening, 77 women returned the questionnaire (response rate of 85% compared with 3 months after screening). Four questionnaires were returned with the addressee unknown.
Altogether, 195 control subjects completed the questionnaire 6 months after screening (response rate, 85%). One questionnaire was returned with the addressee unknown.
The 13 women with a positive diagnosis were excluded from further study (mean age, 61 [SD, 5.1] years). The 128 women with false-positive results had a mean age of 58 (SD, 5.8) years before screening, and the control group was similar (mean age, 58 [SD, 5.5] years) before screening and neither significant difference within age groups (Table 1). The women with false-positive results did not differ significantly from the control group in education, occupation, number of children, and smoking before screening (Table 1).
Short- and Long-term Effects
The mean anxiety score for the women with false-positive results increased from 3.9 (SD, 3.1) before screening to 4.6 (SD, 3.7) at recall and was statistically significant (P = .04) after adjusting for education, occupation, number of children, and smoking (Table 2). Within the false-positive group, 23 women (18%) had an anxiety score of 8 or greater. Questions 3 and 11 were those questions where women with false-positive results scored highest on HADS anxiety at recall. In question 3, “I get a sort of frightened feeling as if something awful is about to happen,” 17 women (13.3%) scored very bad and bad, and in question 11 (“I feel restless as I have to be on the move”), 26 women (20.3%) scored very much and much. No long-term effect was seen, as the anxiety score was 4.3 (SD, 3.4) at 3 months after screening and declined to 4.1 (SD, 3.2) at 6 months. There was no statistically significant difference to the control group before screening (P = .47) and 6 months after (P = .81).
The mean depression score among women with false-positive results was 2.6 (SD, 2.2) before screening and increased at recall (mean, 2.9 [SD, 3.0]) at 3 months after screening (mean 3.1 [SD, 2.9) and at 6 months (mean, 3.2 [SD, 2.9]). No significant differences were found within the false-positive group after adjusting for education, occupation, number of children, and smoking (Table 2). Among women with false-positive results, 9 (12%) had depression scores of 8 or greater 6 months after screening, 5 (9%) more than before screening. In question 8 (“I feel as if I am slowed down”), 11 women (8.6%) with false-positive result diagnosed negative answered very often or almost the whole time.
Women with false-positive results had a statistically significant higher depression score than control subjects at 6 months after screening (P = .045). The control group had similar depression scores before screening and at 6 months after screening (mean, 2.4 [SD, 2.6]).
HEALTH-RELATED QUALITY OF LIFE
The SF-36 scores on mental health declined statistically significantly among the women with false-positive results from before screening until recall (P = .03). Especially the questions “Have you felt calm and peaceful?” and “Have you been a happy person?” were scored lower at recall than before screening. Social functioning and role-emotional scores were also noticeably lower at recall (2.7 vs 3.7 points) (not shown). Nevertheless, all 8 dimensions of SF-36 declined from before screening until 6 months after screening (not shown).
The SF-36 scores did not differ between women with false-positive results and control subjects before screening, but 6 months after screening, they differed not only within the general health (P = .02) and mental health (P = .03) dimensions (Table 2) but also in role-physical (P = .05) and role–emotional (P = .01) (not shown).
The control subjects scored higher on vitality (P = .02) and mental health (P = .05) (Table 2) at 6 months after screening.
Women recalled for further examination after mammography screening had significantly higher anxiety at recall than before screening, but no evidence indicated statistically significantly increased long-term anxiety. Depression increased from before screening until 6 months after screening, but this increase was not statistically significant. Compared with the control group, depression was statistically significant higher for the women with false-positive results at 6 months after screening (P = .045). Health-related quality of life as general health (P = .02) and mental health (P = .03) was significantly lower in the false-positive group than in the control group.
Anxiety and Depression
The significant findings of increased anxiety at recall support findings in other European countries.2,6,8 Being recalled after mammography screening is stressful for many women, and in our sample, 23 women (18%) had a clinically significant level of anxiety at recall. Higher anxiety was scored on questions about what might happen in the future and if feeling restless. The level of anxiety decreased, and no significant evidence of anxiety was found in the follow-up. Higher anxiety from before screening to 3 months after screening has also been found elsewhere,2,3 but in our study, similar to a study in Finland,2 anxiety decreased at 6 months after screening and was at the same level as before screening.
The depression emerging among women with false-positive results from before screening to 6 months after screening seen in our study has been found elsewhere,2 but contradictory results have also been seen.7 An increase in the proportion with depression of 9 percentage points from before screening until 6 months later is substantial, and the women with false-positive result, which turned out to be diagnosed negative, scored higher on the question, “I feel as if I am slowed down.” Aro et al2 found increased intrusive thoughts among women with false-positive results, who might feel they are less healthy because of the recall, and this causes the depression. Those with false-positive and negative results differed statistically significantly in depression 6 months after screening, with women with false-positive results scoring 0.8 points higher. To our knowledge, no other researcher has documented significant differences between people with false-positive and negative results.
Health-Related Quality of Life
The statistically significant decline in mental health at recall measured by SF-36 indicates negative effects on women’s HRQOL. Some women scored lower on questions about feeling calm and peaceful and question about being happy. The women with false-positive results declined in SF-36 social functioning and role-emotional. Being recalled after mammography screening seems to interrupt their social life, and they are forced to reduce time spent in daily work and activities. In general, the time from being recalled until getting a negative diagnosis is no more than 4 weeks, but many women can have difficulty in coping with the reported reactions such as worse mental health during these weeks.
The women with false-positive results did not differ statistically significantly in HRQOL, but the scores in all dimensions of SF-36 were lower at 6 months after screening than before screening. The HRQOL dimensions general health and mental health differed statistically significantly between people with false-positive and negative results at 6 months after screening. The lower scores 6 months after screening and statistically significant difference between people with false-positive and negative results underline the need to examine more closely any effects of screening on HRQOL. Nevertheless, the findings were not clinically significant. The women with negative results had better vitality and mental health 6 months after screening than before screening. An explanation for these findings could be that the women with negative results confirmed being healthy and were relieved by having normal mammograms. However, this did not happen for the women with false-positive results when they got their final negative result.
Implications for Practice
Depression as a long-term effect of mammography screening and negative effects on HRQOL might have public health consequences. Some women scored higher on “I feel as if I am slowed down,” which might indicate they lost energy. It might affect screening behavior, as the women who are most depressed and who have lower HRQOL might not attend screening in the next screening round. This means that information should be disseminated even better than it is today and should be more individually tailored. Better information is required on theprevalence of false-positive results during screening and information on the time needed for clear diagnostic results after recall. Digital mammography and its high resolution might increase the number of false-positive results and confirm the need for good information.
To guarantee high-quality screening services, however, the time from screening until recall should be as short as possible, and the waiting time until the diagnosis is confirmed should be brief. Organized screening might more easily provide information warning about possible false-positive findings in the invitation for screening. Well-informed women attending screening ask for evidence and updated information and act appropriately on such information. Being aware of improving the quality of information leaflets and Web pages on mammography screening is very important in every organized mammography screening throughout the world.
Strengths and Limitations
The strength of our study was the longitudinal study design measuring anxiety, depression, and HRQOL in the same study cohort before screening, at recall, and in follow-up until 6 months after screening. This design, measuring anxiety, depression, and HRQOL before screening, at recall, and at 3 and 6 months after screening, has not been found elsewhere. Aro et al2 had a similar design but did not measure HRQOL and did not measure at recall, and the sample was composed of women 50 years old. We also used a questionnaire validated among Norwegians, and concurrent findings in HADS and mental health strengthen the findings. The sample size was also fairly high.
The limitations in our study could be the low response rate, especially before screening, but in accordance with the study design, no reminders were sent before screening or at recall. We suggest that women with anxiety and depression in general and women with lower HRQOL tend to respond to questionnaires less often. They were probably less representative in our study. The respondents in this study were representative for the women attending screening in Norway and women recalled for what turn out to be false-positive results. A limitation was that specific information on the follow-up procedures for mammography, ultrasound, or biopsy could have provided more information for the study.
Depression arising 6 months after screening and the worsening HRQOL reflect a not fully understood sense of the effects of being recalled in organized screening. The long-term effects of false-positive results in mammography screening should be closely examined. Our study confirmed that HRQOL and especially mental health and general health should be highlighted more. An interesting result was the discrepancy in mental health and general health between people with false-positive and negative results at 6 months after screening.
The benefits of mammography screening are far greater than the negative aspects. Nevertheless, efforts should be made to minimize anxiety at recall and the increase in depression and reduction in HRQOL after screening. This can be achieved by improving the communication and information throughout the screening procedure, particularly during the process of further examination, and by ensuring that both primary and secondary healthcare services provide support and reassurance for these women. Women’s HRQOL, anxiety, and depression are even more important than ever before, given the high resolution of the digital equipment and increased false-positive findings in mammography.
The HRQOL results for vitality and mental health among women with negative results at 6 months after screening might get the women with negative results to recommend the program to others rather than the opposite.
1. Gtzsche Peter C, Nielsen M. Screening for breast cancer with mammography. Cochrane Database of Systematic Reviews. Chichester, UK: John Wiley & Sons, Ltd; 2009.
2. Aro AR, Pilvikki Absetz S, van Elderen TM, van der Ploeg E, van der Kamp LJ. False-positive findings in mammography screening induces short-term distress - breast cancer-specific concern prevails longer. Eur J Cancer. 2000; 36 (9): 1089–1097.
3. Barton MB, Morley DS, Moore S, et al.. Decreasing women’s anxieties after abnormal mammograms: a controlled trial. J Natl Cancer Inst. 2004; 96 (7): 529–538.
4. Ekeberg Ø, Skjauff H, Kåresen R. Screening for breast cancer is associated with a low degree of psychological distress. Breast. 2001; 10 (1): 20–24.
5. Jatoi I, Zhu K, Shah M, Lawrence W. Psychological distress in U.S. women who have experienced false-positive mammograms. Breast Cancer Res Treat. 2006; 100 (2): 191–200.
6. Lampic C, Thurfjell E, Bergh J, Sjoden PO. Short- and long-term anxiety and depression in women recalled after breast cancer screening. Eur J Cancer. 2001; 37 (4): 463–469.
7. Lampic C, Thurfjell E, Sjoden PO. The influence of a false-positive mammogram on a woman’s subsequent behaviour for detecting breast cancer. Eur J Cancer. 2003; 39 (12): 1730–1737.
8. Scaf-Klomp W, Sanderman R, van de Wiel HB, Otter R, van den Heuvel WJ. Distressed or relieved? Psychological side effects of breast cancer screening in the Netherlands. J Epidemiol Community Health. 1997; 51 (6): 705–710.
9. Sandin B, Chorot P, Valiente RM, Lostao L, Santed MA. Adverse psychological effects in women attending a second-stage breast cancer screening. J Psychosom Res. 2002; 52 (5): 303–309.
10. Gibson CJ, Weiss J, Goodrich M, Onega T. False-positive mammography and depressed mood in a screening population: findings from the New Hampshire Mammography Network. J Public Health. 2009; 31 (4): 554–560.
11. Meystre-Agustoni G, Paccaud F, Jeannin A, Dubois-Arber F. Anxiety in a cohort of Swiss women participating in a mammographic screening programme. J Med Screen. 2001; 8 (4): 213–219.
12. Lipkus IM, Halabi S, Strigo TS, Rimer BK. The impact of abnormal mammograms on psychosocial outcomes and subsequent screening. Psychooncology. 2000; 9 (5): 402–410.
13. Gram IT, Lund E, Se S. Quality of life following a false positive mammogram. Br J Cancer. 1990; 62: 1018–1022.
14. Bonomi AE, Boudreau DM, Fishman PA, et al.. Quality of life valuations of mammography screening. Qual Life Res. 2008; 17 (5): 801–814.
15. Johnston K, Brown J, Gerard K, O’Hanlon M, Morton A. Valuing temporary and chronic health states associated with breast screening. Soc Sci Med. 1998; 47 (2): 213–222.
16. Hofvind S, Thoresen S, Tretli S. The cumulative risk of a false-positive recall in the Norwegian Breast Cancer Screening Program. Cancer. 2004; 101 (7): 1501–1507.
17. Kalager M, Zelen M, Langmark F, Adami H-O. Effect of screening mammography on breast-cancer mortality in Norway. N Engl J Med. 2010; 363 (13): 1203–1210.
18. Skaane P. Studies comparing screen-film mammography and full-field digital mammography in breast cancer screening: updated review. Acta Radiol. 2009; 50 (1): 3–14.
19. Skaane P, Hofvind S, Skjennald A. Randomized trial of screen-film versus full-field digital mammography with soft-copy reading in population-based screening program: follow-up and final results of Oslo II study. Radiology. 2007; 244 (3): 708–717.
22. Ware J, Sherbourne C. The MOS 36-item Short-Form Health Survey (SF-36). Med Care. 1992; 30 (6): 473–483.
23. Zigmond AS, Snaith RP. The Hospital Anxiety and Depression Scale. Acta Psychiatr Scand. 1983; 67 (6): 361–370.
24. Alonso J, Ferrer M, Gandek B, et al.. Health-related quality of life associated with chronic conditions in eight countries: results from the International Quality of Life Assessment (IQOLA) Project. Qual Life Res. 2004; 13 (2): 283–298.
25. Ware JE, Kosinski M. Interpreting SF-36 summary health measures: a response. Qual Life Res. 2001; 10 (5): 405–413. discussion 15–20.
26. Ware JE, Kosinski M. SF-36 Physical & Mental Health Summary Scales: A Manual for Users of Version 1. 2nd ed. Lincoln, RI: QualityMetric Incorporated; 2005.
27. Loge JH, Kaasa S. Short Form 36 (SF-36) Health Survey: normative data from the general Norwegian population. Scand J Soc Med. 1998; 26 (4): 250–258.
28. Bjelland I, Dahl AA, Haug TT, Neckelmann D. The validity of the Hospital Anxiety and Depression Scale. An updated literature review. J Psychosom Res. 2002; 52 (2): 69–77.
© 2012 Lippincott Williams & Wilkins, Inc.