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What Is the Psychological Impact of Mammographic Screening on Younger Women With a Family History of Breast Cancer? Findings From a Prospective Cohort Study by the PIMMS Management Group

Sally Tyndel, Joan Austoker, Bethan J. Henderson, Kate Brain, Clare Bankhead, Alison Clements, Eila K. Watson

From the Cancer Research UK, Primary Care Education Research Group, Division of Public Health, Primary Health Care, University of Oxford, Oxford; Institute of Medical & Social Care Research, Ardudwy, Normal Site, University of Wales, Bangor, Bangor, Gwynedd; and Institute of Medical Genetics, School of Medicine, Cardiff University, Heath Park, Cardiff, United Kingdom

Address reprint requests to Joan Austoker, PhD, Division of Public Health, Primary Health Care, University of Oxford, Old Road, Headington, Oxford OX3 7LF, United Kingdom; e-mail: joan.austoker{at}dphpc.ox.ac.uk

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
Purpose: Studies are underway to establish the clinical effectiveness of annual mammographic screening in women younger than 50 years with a family history of breast cancer. This study investigated both the positive and negative psychological effects of screening on these women.

Patients and Methods: Women who received an immediate all-clear result after mammography (n = 1,174) and women who were recalled for additional tests before receiving an all-clear result (false positive; n = 112) completed questionnaires: 1 month before mammography, and 1 and 6 months after receiving final results. The questionnaires included measures of cancer worry, psychological consequences, and perceived benefits of breast screening.

Results: Women who received an immediate all-clear result experienced a decrease in cancer worry and negative psychological consequences immediately after the result, whereas women who were recalled for additional tests did not. By 6 months this cancer-specific distress had reduced significantly in both groups. Changes in levels of distress were significantly different between the two groups, but in absolute terms the differences were not large. Recalled women reported significantly greater positive psychological consequences of screening immediately after the result, and were also more positive about the benefits of screening compared with women who received an immediate all-clear result.

Conclusion: For women receiving an immediate all-clear result, participating in annual mammographic screening is psychologically beneficial. Furthermore, women who are recalled for additional tests do not appear to be harmed by screening: these women's positive views about mammography suggest that they view any distress caused by recall as an acceptable part of screening.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
Breast cancer is the most common cancer in women in the United States and United Kingdom.^1,2 Having a family history of breast cancer (FHBC) is one of the strongest risk factors for developing the disease.³ Guidelines recommend regular mammographic screening from age 40 years for women with an FHBC,^4,5 although it is not yet known whether the benefits of regular screening for these women outweigh the harms.

For all women, one of the harms associated with having a mammogram is a false-positive screen resulting in additional imaging and biopsies.^6,7 A recent systematic review of women in routine screening programs concluded that those who are recalled for additional tests experience significant anxiety in the short term and possibly long term.⁸ Given that the cumulative rate of having a false-positive screen for all women age 40 to 49 years ranges from 23% to 56%,^7,9 potentially large numbers of women with an FHBC could receive a false-positive result.

Studies have found elevated levels of cancer-specific distress in women with an FHBC,^10,11 although this group of women does not appear to experience increased levels of general psychological morbidity^12,13 Risk factors for distress include age,¹⁴ education level,¹⁵ cancer experiences within the family,¹⁶ and risk perception.¹⁷ Given the greater cancer worry in women with an FHBC, it is possible they may be particularly adversely affected by a false-positive result. Previous studies have investigated the psychological impact of screening in women with an FHBC, but are hampered by their small sample sizes and study designs.¹⁸

This is the first large, prospective cohort study to examine both the positive and negative psychological impact of mammographic screening in women younger than age 50 who have regular screening because of an FHBC. We wished to test the hypothesis that in both the short and longer term, women who receive an immediate all-clear result gain psychological benefit from screening, whereas women who are recalled for additional tests before an all-clear result experience increased cancer-specific distress.

	PATIENTS AND METHODS

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Participants
Women were invited to join the study if they were age 35 to 49 years and were already participating in (or had just been accepted onto) a 12- to 18-month screening program after assessment by specialist clinics as being at moderate or high risk of familial breast cancer. Women with a previous diagnosis of breast cancer or a family history of ovarian cancer only were excluded.

Participating clinics followed similar protocols. Women were referred to specialist family history/breast/genetics clinics by family physicians or hospital consultants. All referred women completed a family history questionnaire that was used to assess risk. Assessment into a moderate-risk category (lifetime risk of 17% to 30%) or high-risk category (lifetime risk of > 30%) was in broad agreement with United Kingdom National Institutes of Health and Clinical Excellence guidance.⁵ Women in both the moderate- and high-risk categories were offered regular mammograms and were counseled by a health professional from the specialist clinics. In addition, women at high-risk were offered specialist genetic counseling and could also be offered genetic testing or risk-reducing surgery.

This study was granted approval by London Multicenter Research Ethics Committee.

Procedures
Twenty-one centers throughout the United Kingdom participated in the study. Eligible women were identified by centers and sent questionnaires approximately 1 month before the scheduled mammogram appointment (T1). Where possible, centers sent a reminder to nonresponders at 2 weeks. At T1, 2,321 (62%) women completed the questionnaire and returned it directly to the research team, who sent out follow-up questionnaires approximately 1 (T2) and 6 months (T3) after women had received their final screening result. Nonresponders were sent one reminder at 2 weeks. At T2, 1,593 (80%) eligible women completed the questionnaire. Two hundred eight women who received an all-clear result were not sent follow-up questionnaires; initially, it was estimated that we only needed to follow up a random sample of one in three of the all-clear women. This decision was later revised to ensure we attained our target sample size. At T3, 1,436 (73%) eligible women completed the questionnaire. At T2 and T3, women were excluded if they completed the questionnaire more than 2 months or more than 8 months, respectively, after receipt of results, did not attend for a mammogram, or had a cancer diagnosis (Fig 1).

View larger version (37K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Response to questionnaires. T1, 1 month before screening; T2, 1 month after final screening; T3, 6 months after final screening.

Measures
The main study outcome, breast cancer–specific distress, was measured by the Revised Cancer Worries Scale (CWS-R)^19-21and the PCQ.²²

The six-item CWS-R assesses the frequency of concerns about developing cancer and the impact of these concerns on mood and daily functioning. It has been widely used and validated in populations at increased risk of cancer.^23-25 Women were asked questions such as, "How often do you worry about developing breast cancer?" At T1 and T3, the questions related to the previous month; at T2, questions related to the period since receiving their final result. Items are scored from 1 (not at all or rarely) to 4 (almost all of the time), and summed for a total score (range, 6 to 24; T1, = .84; T2, = .82; T3, = .80).

The PCQ measures negative (12 items) and positive (10 items) psychological consequences of breast screening in terms of emotional, physical, and social functioning. The negative PCQ, which has been widely used and validated in studies of routine breast screening programs,^22,26,27 was administered at all three time points, with the same time anchor points as reported for the CWS-R. Women were asked questions such as, "As a result of thoughts about breast cancer, have you had trouble sleeping?" Items are scored from 0 (not at all) to 3 (quite a lot of the time). In previous studies the negative PCQ has been analyzed using subtotals,²² but also by using total scores.²⁶ In the current study, factor analysis revealed one scale and the PCQ was summed for a total negative score (T1, = .94; T2, = .95; T3, = .94), with a range of 0 to 36.

Secondary outcome measures were positive psychological consequences and perceived benefits of screening. The positive section of the PCQ was designed to be used after receipt of screening results,²² and was therefore administered at T2 and T3. Women were asked questions such as, "Have your experiences of breast screening (mammography) caused you to feel more hopeful about the future?" Positive items are summed for a total positive score (T2, = .91; T3, = .91), with a range of 0 to 30. After receiving their results, women were also asked whether their attitude about the benefits of breast screening had changed since their last visit. Response options were 1 (I now feel more positive), 2 (I feel the same), or 3 (I feel less positive). Data were dichotomized into two categories (I feel more positive and I feel the same/less positive), given that less than 1% of women felt less positive about screening.

Demographic information was collected at T1 and included age, marital status, race, educational level, and whether participants had biologic children. Screening clinics provided information on risk level (moderate or high), and whether this was the participants' first screen on the family history screening program. Data about previous mammograms and recall, details about the women's family history (deceased relatives, relatives currently receiving treatment for breast cancer), and time since they first realized that they were at increased risk of developing breast cancer (up to 1 year ago or > 1 year ago) were obtained from participants. Women were also asked to rate their perceived risk of developing breast cancer in their lifetime. Responses were collapsed into four categories: 1, no chance/unlikely; 2, likely; 3, highly likely/definitely; and 4, do not know.

Statistical Analysis
Characteristics of the two groups were compared using the ² test for categoric variables, with Yates continuity correction where appropriate. Age was compared using Mann-Whitney U test. Scores on the dependent variables (CWS-R, PCQ) were treated as continuous variables and paired-samples t tests were used for within-group comparisons of T1 versus T2 and T2 versus T3.

The negative psychological effect of recall at follow-up was examined using a random-effects linear regression model, with clinic center as the index variable and the between-group difference scores (calculated from T1-T2 and T2-T3) as the dependent variables. Covariates were included to adjust for scores on the psychological questionnaires at the relevant baselines (T1 or T2) and to control for potentially important variables. These variables were included based on significant prescreening differences between the recall and all-clear groups (Table 1) and background variables that were considered to be important potential predictors of cancer-specific distress (Table 2). Checks were made for any correlations between covariates, and preliminary analyses were performed to ensure that the assumptions required for regression were not violated. Given that the change scores on the PCQ were negatively skewed, a preliminary analysis was done using the Mann-Whitney U test to compare the effect of recall/all-clear result on the changes in negative psychological consequences. The data were then transformed using log 10 (score + 1).

	RESULTS

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For the purpose of this analysis, the 1,286 women who completed all three questionnaires were divided into two groups. The all-clear group (n = 1,174) consisted of women given an immediate all-clear result. The recall group (n = 112) consisted of women recalled for additional tests as a result of the mammogram. Additional tests were one or more of the following: additional mammogram, ultrasound, clinical breast examination, fine-needle aspiration, core biopsy, or surgery to remove a benign tumor.

As listed in Table 1, the participant characteristics measured at T1 showed that women in the recall group were significantly more likely to be at high risk (P = .036) and to have biologic children (P = .027). Women in the recall group also had higher psychological scores prescreening on both main outcome measures (Fig 2).

View larger version (13K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 2. Mean scores on (A) Cancer Worry Scale (CWS) and (B) negative Psychological Consequences Questionnaire (PCQ) for recall and all-clear groups (with 95% CI).

Positive Psychological Impact
Table 4 shows the effect of recall on the positive PCQ at both follow-up time points. The recalled women had significantly higher scores at T2 compared with women with an all-clear result, but this difference had dissipated at the 6-month follow-up. Similarly, a higher proportion of women in the recalled group reported feeling more positive about the benefits of screening than women with an initial all-clear result after mammography. This difference between the groups persisted at 6 months.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
This study assessed both the positive and negative psychological impact of screening on women younger than age 50 years with an FHBC. It is interesting, and contrary to our expectations, that women who received a false-positive result did not show a statistically significant increase in cancer worry or negative psychological consequences after receiving their results. This differs from studies of women in the general population undergoing routine breast screening who have consistently reported significant adverse psychological consequences associated with a false-positive result 1 to 6 months after recall.^15,26,28-30 One possible explanation is that women with an FHBC have different expectations of screening. Whereas women participating in routine screening have an expectation that screening will reassure them that "everything is all right,"³¹ and hence recall for additional tests challenges their health expectations,²⁹ this may not be the case for women with an FHBC.

There were significant differences in magnitude of change for cancer worry and negative psychological consequences between women who received an immediate all-clear result and recalled women. However, the differences were small. The negative PCQ, which has been designed specifically to detect consequences of screening mammography, measured a mean change at T2 that could only be equated to a response of "rarely" instead of "not at all" to one of 12 questions. However, even small changes in cancer worry or negative psychological consequences may be important within the context of an already heightened anxiety. The levels of cancer worry found in this study are similar to those reported in other studies in similar populations,^11,23,24 and are higher than those found in a general-population sample (CWS-R mean = 8.9, SD = 2.0).¹¹ However, neither of the measures used in the study are clinical measures, and it has been suggested that when there are no clinical case thresholds available, measures of breast cancer worry in women with FHBC may simply be reflecting understandable concerns about risk status.^11,13

It has been reported that women with an FHBC place a high value on access to regular mammography,^32,33 and once offered the opportunity, are highly motivated to attend.³⁴ To add to the understanding of the psychological impact of mammography on women with an FHBC, we also measured positive psychological consequences. Women who were recalled reported significantly more positive psychological consequences after receiving their results than the all-clear group, although there was no difference between the groups at 6 months. Furthermore, similar to a study of routine mammography,³⁵ being recalled for additional tests apparently enhanced women's belief in the benefits of screening. When women were asked if their attitude toward screening had changed after receipt of results, the women who were recalled were significantly more positive about the benefits of screening—an attitude that still remained at 6 months. One explanation may be relief at the positive outcome of the recall, particularly if they had expected the worst before screening because of their increased risk.³⁶ This pattern of results suggests that women with an FHBC who are recalled for additional tests place great faith in mammography screening despite their experiences.

This study had several strengths compared with previous studies that have reported on this topic. The study was large and recruited women throughout the United Kingdom, from family history clinics that were operating in a broadly similar fashion, and according to United Kingdom National Institutes of Health and Clinical Excellence guidance on the management of women with an FHBC. The study also benefited from being prospective in nature, enabling us to account for differences in levels of cancer-specific distress that existed before screening. A limitation associated with conducting a prospective cohort study using postal questionnaires is the potential bias resulting from loss to follow-up, although sensitivity analysis indicated this was unlikely to affect the findings of this study. However, it is possible that nonresponders at baseline were either a much more distressed group or conversely a much less distressed group, which would limit the generalizability of our findings. Generalizability is limited further because of the site of the study (United Kingdom only), restricted age range, and lack of racial diversity of the participants. It would also have enhanced understanding of the course of the psychological impact if the recalled women had completed an additional questionnaire during the recall period. However, given the mode of operation of the clinics, this was not feasible. Finally, although the measures asked women to reflect on cancer-specific distress in the previous 4 weeks, it is possible that anticipation of screening increased levels of distress at the time the prescreening questionnaire was completed.

The efficacy of screening in women younger than age 50 years with an FHBC has not been proven and is currently being investigated by a large multicenter study in the United Kingdom.³⁷ However, the indications are promising,^38,39 and the results from the current study suggest that participating in annual mammography screening is psychologically beneficial to the majority of women who receive an immediate all-clear result. Furthermore, although the majority of women who are recalled for additional tests do not experience the immediate reduction in cancer-specific distress seen in the all-clear group, their positive views about mammographic screening would suggest they view any distress caused by recall as an acceptable part of screening. Nonetheless, the high scores reported by some individuals on the questionnaires suggest it is still important to identify subgroups of vulnerable women who may be especially prone to adverse emotional responses to screening.

	AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
The author(s) indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
Conception and design: Sally Tyndel, Bethan J. Henderson, Kate Brain, Clare Bankhead, Alison Clements, Joan Austoker, Eila K. Watson

Collection and assembly of data: Sally Tyndel

Data analysis and interpretation: Sally Tyndel, Bethan J. Henderson, Kate Brain, Clare Bankhead, Alison Clements, Eila K. Watson

Manuscript writing: Sally Tyndel, Bethan J. Henderson, Kate Brain, Clare Bankhead, Alison Clements, Joan Austoker, Eila K. Watson

Final approval of manuscript: Sally Tyndel, Bethan J. Henderson, Kate Brain, Clare Bankhead, Alison Clements, Joan Austoker, Eila K. Watson

	Appendix

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The following collaborating centers participated in this study: Nottingham City Hospital, Withington Hospital, Manchester; Breast Test Wales –North, South East, and South West; Wales, Medical Genetics –North, South East, and South West; Southend Hospital; Elizabeth Garrett Anderson Hospital, London; Countess of Chester; Frenchay Hospital, Bristol; Royal Hospital Haslar, Portsmouth; Royal Liverpool University Hospital; Royal Cornwall Hospital; Ninewells Hospital, Dundee; City and Sandwells Hospital, Birmingham; Mayday University Hospital, Croydon; Derby City Hospital; Royal Marsden, London; University Hospitals Coventry and Warwickshire. This study would not have been possible without the enthusiasm of a multidisciplinary team of doctors, nurses, administrative and secretarial staff based in these centers.

	ACKNOWLEDGMENTS

 
We thank all of the patients who took the time to complete our questionnaire; the collaborating centers for their help; Rafael Perera and Pat Yudkin for statistical advice; and Jenny Hood for administrative assistance. This article was written on behalf of the PIMMS Management Group including: Stephen Duffy, Wolfson College of Preventive Medicine, London; Gareth Evans, Dept of Clinical Genetics, St Mary's Hospital, Manchester; Hilary Fielder, Screening Services, Velindre NHS Trust, Wales; Jonathon Gray, Institute of Medical Genetics, University Hospital Wales; James Mackay, Institute of Child Health, London; and Douglas Macmillan, Professorial Unit of Surgery, University of Nottingham, United Kingdom.

	NOTES

 
Supported by Grant No. C73A2916 from Cancer Research UK.

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
1. American Cancer Society: Cancer Facts and Figures for 2006. http://www.cancer.org/docroot/STT/stt_0_2006.asp?sitearea=STT&level=1

2. Office of National Statistics: Office of National Statistics. Breast Cancer: Incidence rises while deaths continue to fall. http://www.statistics.gov.uk/cci/nugget_print.asp?ID=575

3. Emery J, Lucassen A, Murphy M: Common hereditary cancers and implications for primary care. Lancet 358:56-63, 2001[CrossRef][Medline]

4. US Preventative Services Task Force: Screening for breast cancer: Recommendations and rationale. Ann Intern Med 137:344-346, 2002[Abstract/Free Full Text]

5. McIntosh A, Shaw C, Evans G, et al: Clinical Guidelines and Evidence Review for The Classification and Care of Women at Risk of Familial Breast Cancer. London, United Kingdom, National Collaborating Centre for Primary Care/University of Sheffield, 2004

6. Djulbegovic B, Lyman GH: Screening mammography at 40-49 years: Regret or no regret? Lancet 368:2035-2037, 2006[CrossRef][Medline]

7. Moss SM, Cuckle H, Evans A, et al: Effect of mammographic screening from age 40 years on breast cancer mortality at 10 years' follow-up: A randomised controlled trial. Lancet 368:2053-2060, 2006[CrossRef][Medline]

8. Brett J, Bankhead C, Henderson B, et al: The psychological impact of mammographic screening: A systematic review. Psychooncology 14:917-938, 2005[CrossRef][Medline]

9. Elmore JG, Barton MB, Moceri VM, et al: Ten-year risk of false positive screening mammograms and clinical breast examinations. N Engl J Med 338:1089-1096, 1998[Abstract/Free Full Text]

10. Brain K, Gray J, Norman P, et al: Randomized trial of a specialist genetic assessment service for familial breast cancer. J Natl Cancer Inst 92:1345-1351, 2000[Abstract/Free Full Text]

11. Rees G, Fry A, Cull A, et al: Illness perceptions and distress in women at increased risk of breast cancer. Psychol Health 19:749-765, 2004[CrossRef]

12. Butow P, Meiser B, Price M, et al: Psychological morbidity in women at increased risk of developing breast cancer: A controlled study. Psychooncology 14:195-203, 2005

13. Coyne JC, Benazon NR, Gaba CG, et al: Distress and psychiatric morbidity among women from high-risk breast and ovarian cancer families. J Consult Clin Psychol 68:864-874, 2000[CrossRef][Medline]

14. Cull A, Anderson ED, Campbell S, et al: The impact of genetic counselling about breast cancer risk on women's risk perceptions and levels of distress. Br J Cancer 79:501-508, 1999[CrossRef][Medline]

15. Olsson P, Armelius K, Nordahl G, et al: Women with false positive screening mammograms: How do they cope? J Med Screen 6:89-93, 1999[Abstract/Free Full Text]

16. van Dooren S, Seynaeve C, Rijnsburger AJ, et al: The impact of having relatives affected with breast cancer on psychological distress in women at increased risk for hereditary breast cancer. Breast Cancer Res Treat 89:75-80, 2005[CrossRef][Medline]

17. Hopwood P: Breast cancer risk perception: What do we know and understand? Breast Cancer Res 2:387-391, 2000[CrossRef][Medline]

18. Watson EK, Henderson BJ, Brett J, et al: The psychological impact of mammographic screening on women with a family history of breast cancer: A systematic review. Psychooncology 14:939-948, 2005[CrossRef][Medline]

19. Lerman C, Trock B, Rimer BK, et al: Psychological and behavioral implications of abnormal mammograms. Ann Intern Med 114:657-661, 1991[Medline]

20. Lerman C, Trock B, Rimer BK, et al: Psychological side effects of breast cancer screening. Health Psychol 10:259-267, 1991[CrossRef][Medline]

21. Watson M, Duvivier V, Wade-Walsh M, et al: Family history of breast cancer: What do women understand and recall about their genetic risk? J Med Genet 35:731-738, 1998[Abstract/Free Full Text]

22. Cockburn J, De Luise T, Hurley S, et al: Development and validation of the PCQ: A questionnaire to measure the psychological consequences of screening mammography. Soc Sci Med 34:1129-1134, 1992[CrossRef][Medline]

23. Brain K, Norman P, Gray J, et al: A randomized trial of specialist genetic assessment: Psychological impact on women at different levels of familial breast cancer risk. Br J Cancer 86:233-238, 2002[CrossRef][Medline]

24. Fry A, Cull A, Appleton S, et al: A randomised controlled trial of breast cancer genetics services in South East Scotland: Psychological impact. Br J Cancer 89:653-659, 2003[CrossRef][Medline]

25. Hopwood P, Shenton A, Lalloo F, et al: Risk perception and cancer worry: An exploratory study of the impact of genetic risk counselling in women with a family history of breast cancer. J Med Genet 38:139, 2001[Free Full Text]

26. Ong G, Austoker J, Brett J: Breast screening: Adverse psychological consequences one month after placing women on early recall because of a diagnostic uncertainty—A multicentre study. J Med Screen 4:158-168, 1997[Medline]

27. Brett J, Austoker J: Women who are recalled for further investigation for breast screening: Psychological consequences 3 years after recall and factors affecting re-attendance. J Public Health Med 23:292-300, 2001[Abstract/Free Full Text]

28. Absetz P, Aro AR, Sutton SR: Experience with breast cancer, pre-screening perceived susceptibility and the psychological impact of screening. Psychooncology 12:305-318, 2003[CrossRef][Medline]

29. Brett J, Austoker J, Ong G: Do women who undergo further investigation for breast screening suffer adverse psychological consequences? A multi-centre follow-up study comparing different breast screening result groups five months after their last breast screening appointment. J Public Health Med 20:396-403, 1998[Abstract/Free Full Text]

30. 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 39:1730-1737, 2003[CrossRef][Medline]

31. Webster P, Austoker J: Women's knowledge about breast cancer risk and their views of the purpose and implications of breast screening: A questionnaire survey. J Public Health 28:197-202, 2006[CrossRef]

32. Young D, McLeish L, Sullivan F, et al: Familial breast cancer: Management of lower risk referrals. Br J Cancer 95:974-978, 2006[CrossRef][Medline]

33. Murabito JM, Evans JC, Larson MG, et al: Family breast cancer history and mammography: Framingham Offspring Study. Am J Epidemiol 154:916-923, 2001[Abstract/Free Full Text]

34. Lalloo F, Boggis CR, Evans DG, et al: Screening by mammography, women with a family history of breast cancer. Eur J Cancer 34:937-940, 1998[CrossRef][Medline]

35. Lipkus IM, Halabi S, Strigo TS, et al: The impact of abnormal mammograms on psychosocial outcomes and subsequent screening. Psychooncology 9:402-410, 2000[CrossRef][Medline]

36. Chalmers K, Thomson K: Coming to terms with the risk of breast cancer: Perceptions of women with primary relatives with breast cancer. Qual Health Res 6:256-282, 1996[Abstract/Free Full Text]

37. The FH01 Management Committee SCaC: The challenge of evaluating annual mammography screening for young women with a family history of breast cancer. J Med Screen 13:177-182, 2006[Medline]

38. Gui GPH, Kadayaprath G, Darhouse N, et al: Clinical outcome and service implications of screening women at increased breast cancer risk from a family history. Eur J Surg Oncol 32:719-724, 2006[CrossRef][Medline]

39. Maurice A, Evans DG, Shenton A, et al: Screening younger women with a family history of breast cancer: Does early detection improve outcome? Eur J Cancer 42:1385-1390, 2006[CrossRef][Medline]

Submitted January 31, 2007; accepted June 14, 2007.

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