False-positive findings in mammography screening induces short-term distress — breast cancer-specific concern prevails longer

European Journal of Cancer 36 (2000) 1089±1097

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False-positive ®ndings in mammography screening induces shortterm distress Ð breast cancer-speci®c concern prevails longer A.R. Aro a,*, S. Pilvikki Absetz a, T.M. van Elderen b, E. van der Ploeg c, L.J.Th. van der Kamp d a

Department of Epidemiology and Health Promotion, National Public Health Institute, Mannerheimintie 166, FIN-00300 Helsinki, Finland b Department of Clinical and Health Psychology, Leiden University, PO Box 9555, 2300 RB Leiden, The Netherlands c Department of Clinical Psychology, Utrecht University, PO Box 80.140, 3508 TC Utrecht, The Netherlands d Department of Data Theory, Leiden University, PO Box 9555, 2300 RB Leiden, The Netherlands Received 9 August 1999; received in revised form 4 January 2000; accepted 1 March 2000

Abstract The aim of this study was to examine psychological distress in a mammography screening process as a consequence of screening after adjusting for background, personality and prescreening distress. Subjects, aged 50 years, were invitees at their ®rst screening. There were three groups; normal ®ndings (n=1407), false-positive ®ndings (n=492) and referents from outside the screening programme (n=1718, age 48±49 years). Distress was measured as illness worry, anxiety, depression, cancer beliefs and early detection behaviour. Measurements were one month before screening invitation with follow-ups at 2 and 12 months postscreening. At 2 months, there was a moderate multivariate e€ect of group on distress; and intrusive thinking and worry about breast cancer, in particular, were most frequent amongst the false positives. Intrusive thinking still prevailed at 12 months, in addition to a higher perceived breast cancer risk and susceptibility. Distress related to screening and false-positive ®ndings seems to be moderate, but prevailing cancer-speci®c concerns call for improvements in screening programmes. # 2000 Elsevier Science Ltd. All rights reserved. Keywords: Mammography screening; Distress; False-positive ®ndings; Normal ®ndings

1. Introduction Breast cancer screening by mammography, arranged biennially in the age group of 50 years and older can reduce breast cancer mortality by 30% [1]. Many European countries have launched screening programmes for these women and the feasibility of extending screening to both younger and older age groups has also been widely discussed [2,3]. However, the psychological impact of screening, especially amongst those with falsepositive screening results, has created a debate about the harm to bene®t ratio of screening [4±10], and questioned the basis of launching and continuing these programmes [7,10]. Rates of abnormal mammograms in European programmes vary from 3 to 13% [11,12], but the estimated cumulative risk of at least one false-positive mammogram in 10 screening rounds in the USA was * Corresponding author. Tel.: +358-9-47-44-8264; fax: +358-9-4744-8338. E-mail address: arja.aro@ktl.® (A.R. Aro).

approximately 50% [8]. Studies on the psychological impact report a short-term increase in distress, anxiety and intrusive thoughts mainly amongst those with an abnormal mammogram. Behavioural impact varies from the excess practice of breast self-examination to both increased adherence and to non-adherence of recommended screening [4,9,13±16]. However, most studies have measured only short-term psychological impact and also su€er from methodological shortcomings: for example only a few studies have had a prescreening Ð not to mention a pre-invitation Ð baseline measurement [15,17±19]. Invitation to screening and publicity campaigns inevitably make women aware of forthcoming screening and induce worry about cancer. Studies have been based on selected, often small study populations, and a variety of mostly non-standardised measures and timeframes have been used. Some prospective studies on routine screening have reported a decrease in anxiety from pre- to postscreening [15,17]. In a retrospective study [6] false-positives did not di€er in anxiety or distress from population

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referents, but both `false-positives' and `referents' differed from the `normal ®nding' group in being more distressed. These di€erences were interpreted more as relief in the `normal ®nding' group than as raised anxiety and distress in the `false-positive' group. The aim of the present study was to evaluate the psychological distress induced by a mammography screening process and by the type of ®nding amongst women invited to their ®rst screening round. In addition to having both short- and long-term measurements, we have taken into account background factors, personality factors and prescreening levels of distress, and we present the results using standardised indices of e€ect size. 2. Patients and methods The Finnish nationwide public health screening programme invites biennially 50±59-year-old women to free mammography screening. The invitation letter from the local health authority mentions possible further examinations as follows: `The majority of the changes in the breasts are benign. We hope that you remember this in case you are recalled for further examinations'. A normal result is mailed within 2 weeks postscreening. Those recalled are phoned by a nurse. Waiting time from screening to recall varied from 1 to 20 days, and from recall to further check-up from 1 to 7 days. 2.1. Participants Subjects of the study were women, age 50 years, at their ®rst screening (1992±1994). The uptake rate was 88% [20]. The study included a postal survey with a reply paid envelope one month before screening invitation, and follow-ups at 2 and 12 months postscreening. The normal ®ndings group (n=1407) came from a random sample of the target population (n=16 886), the false-positives (all cases recalled for further examination after the ®rst screening, and then found normal, n=492/ 15 191, 3.2% of those screened) from the whole target population and the referents outside the screening programme (n=1718, age 48±49 years) from the population registry in the municipalities of the random sample. At baseline, the covering letter of the questionnaire described the study as `a survey on perceived health and health behaviour'. Response was encouraged by stating that the results will be used for the development of healthcare services to better meet the needs of the customers. At the follow-ups, the covering letters to the groups were identical with the exception that experience of screening was mentioned in the letter of the screened groups. Response rates varied between 54 and 65% for prescreening, when as screening was impending only one reminder was sent to all subjects. In contrast, two reminders were sent at 2 and 12 months following

screening and the corresponding response rates were between 73 and 87% at 2 months and between 73 and 80% at 12 months. The reminders increased the response rates by 30% and 13% at 2 and 12 months respectively. The cases with self-reported cancer diagnosis prescreening were excluded (n=53) as were those who responded after the mailing of screening invitations (n=51). After dropping the cases with incompletely ®lled questionnaires and with missing values >20%, the numbers of the study groups in the analyses were: prescreening: normal ®ndings, n=724, false-positive ®ndings, n=299 and referents, n=901; at 2 months: n=709, n=259 and n=725, respectively; and at 12 months: n=585, n=232 and n=364, respectively (304 referents had entered screening during the follow-up). 2.2. Measures 2.2.1. Distress measures 1. Illness worry was measured by a scale [21], consisting of 27 items (range: 0±4) on seven subscales in this data set (maximum likelihood factor analysis, varimax rotation, 49.8% of variance explained): concern about pain and bodily preoccupation (4 items, coecient alpha 0.70), e€ects of symptoms (3 items, 0.90), thanatophobia (fear of death) (3 items, 0.71), health habits (2 items, 0.64), worry about illness (4 items, 0.60), treatment experiences (3 items, 0.86) and fear of illness (6 items, 0.73). Compared with the original scale two items (item no 5 and item no 9) were omitted for better homogeneity; 2. state anxiety was measured by an inventory [22] containing 20 items (range: 1±4), and was used as a unidimensional sumscore (range: 20±80, alpha 0.95); 3. depression was measured by a 21-item (range: 0±3) widely used scale [23] allowing also clinical classi®cation, unidimensional sumscore (range: 0±63, alpha 0.88) was used to depict the severity of depression; 4. breast cancer-speci®c beliefs were measured by an 11-item scale [24±26], validated in the present data set to consist of 8 items (range: 1±4) on two subscales (perceived susceptibility to breast cancer: 5 items, alpha 0.69 and severity of breast cancer: 3 items, alpha 0.60), which explained 33.2% of the variance of the items. Single items (Table 3) were used to measure frequencies of intrusive thinking and worry about breast cancer, perceived breast cancer risk, con®dence in breast cancer prevention, con®dence in and importance of breast self-examination, perception of the health of the breasts, perceived symptoms in breasts, and frequency of health thoughts and worries, perceived health and stress;

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5. as a behavioural indicator of distress, frequency of breast self-examination was measured (Table 3). In addition, health behaviour was measured as visits to the doctor and days ill during the past year. 2.2.2. Background variables 1. Trait anxiety was measured [22] to depict tendency to react anxiously: 20 items (range: 1±4), a sumscore was used (range 20±80, alpha 0.91); 2. perceptions about controllability of health were measured by a scale [27] consisting of 27 items (range: 1±4) with three subscales in the data set: chance control (9 items, alpha 0.84); provider control (8 items, alpha 0.80); and own control (10 items, alpha 0.73); 3. background variables included socio-economic factors like marital status (classi®ed for analyses: married/non-married), area of living (rural/urban), years of education and income level (low, medium and high), working status (working/not), history of life changes, history of serious illnesses, breast cancer in signi®cant others (yes/no), past mammogram (yes/no), and six items on social support and quality of intimate relationship. 2.3. Statistical analysis Numbers of dropped cases due to missing values (>20% missing criteria) in di€erent standardised scales varied as follows: normal ®ndings: baseline 3±30, 2 months 4±53, 12 months 8±11; false-positives: 3±15, 2± 18, 3±8, respectively; and referents: 6±58, 2±59, 1±6, respectively. Missing values for cases not dropped were replaced using regression imputation [28]. Crosssectional univariate analysis of group di€erences were tested using frequency distributions for nominal scale variables, Chi square tests, P<0.05 as a signi®cance level; di€erences in the means of the continuous variables were tested by two-sided Student t-tests both for independent and paired (Wilcoxon) samples. PRINCALS analysis [29] was used to select variables clustering with the scales or subscales of distress measures for a multivariate analysis of covariance (MANCOVA). MANCOVA was executed using the distress measures as the outcome measures, and the background factors, personality measures and baseline values of the outcome measures as covariates. To check the in¯uence of outliers on the results, the Mahalanobis distance for all the variables involved was computed, and subjects with a distance over critical Chi square at 95% were omitted after this check [30]. Due to a violation of homogeneity of regression, separate regression lines were ®tted for the three groups at 2 months. E€ect size (ES, Wilks' Lambda) was used to describe the magnitude of the e€ects. SURVO 84C software and

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SPSS/WIN, version 6 software package were used for statistical analyses. 3. Results Results are presented as (1) univariate between group analyses; (2) univariate within group analyses; and ®nally (3) as a multivariate analysis of covariance showing the net e€ect of screening on distress. 3.1. Prescreening group di€erences The false-positive group consisted of more rural women and had less past mammograms than the referents (Table 1). Amongst them there were more of those with both education <9 years and >12 years than in the other groups (Table 1). The groups did not di€er in the personality measures of trait anxiety and health locus of control. In the distress measures, the false-positive group had less thanatophobia and fear of illness than either the normal ®ndings group or the referents, and the normal ®ndings group perceived breast cancer as more severe than the false-positives (Table 2). 3.2. Di€erences at 2 months postscreening At 2 months postscreening there were no signi®cant between-group di€erences in any of the standardised distress scales (Table 2). However, the false positives reported most often intrusive thinking and worry about breast cancer, and most active, even excess practice of breast self-examination (Table 3). The false-positives were also slightly less con®dent in breast self-examination, perceived their breasts to be less healthy and had more breast symptoms than those with normal ®ndings. Those with normal ®ndings worried less about breast Table 1 Selected background characteristics of the study groupsa: normal ®ndings (NF, n=721), false-positives (FP, n=296) and referents (REF, n=892)

Married Urban area Education <9 years 9±11 years >12 years Working Breast cancer in signi®cant others Past mammogram

NF n (%)

FP n (%)

REF n (%)

559 (77.5) 439 (60.6)

224 (75.7) 156 (52.9)

669 (75.0) 572 (63.5)*

198 269 254 476 310

106 105 72 189 125

238 318 344 719 408

(27.5) (37.3) (35.2) (79.6) (44.5)

345 (48.3)

(32.9) (27.9) (39.3) (77.5) (43.6)

130 (44.5)

(26.4) (35.3) (38.2)* (81.6) (47.7)

461 (51.9)*

Signi®cance (*P<0.05) tested NF/FP, NF/REF, FP/REF over two classes (yes/no) except for education over three classes. a Some data are missing due to incomplete questionnaires.

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cancer but also practised breast self-examination more actively and excessively than the referents. 3.3. Di€erences at 12 months postscreening 12 months post-screening the groups di€ered signi®cantly in two standardised subscales (Table 2): the normal ®ndings group was more afraid of illness than the referents, and the false-positive group perceived their breast cancer susceptibility signi®cantly higher than the referents. The false-positives had more often intrusive thinking and worry about breast cancer, they were most active of the three groups in breast selfexamination, and also perceived most often their breast cancer risk to be high. They also had more breast symptoms, and perceived their breasts to be not healthy more often than the women with normal ®ndings (Table 3). In summary, in the univariate, between-group analyses it was the false-positive group who was the most

distressed, especially in the breast cancer-speci®c indicators, whilst general mood, anxiety and health worry measures hardly showed any di€erences. However, both screened groups intended to re-attend screening if/when invited again Ð 98.2% of the normal ®ndings group and 98.7% of the false-positive group did so. 3.4. Change in distress levels from prescreening to postscreening Amongst those with normal screening ®ndings, worry about illness decreased from prescreening at both 2 months (P<0.001) and 12 months postscreening (P<0.001); depression decreased from prescreening levels at 2 months (P=0.002), and then rose back to almost prescreening levels at 12 months (P=0.049); concern about pain/bodily preoccupation decreased from prescreening levels at 2 months (P=0.013). Health habits increased from prescreening levels at 2 months (P=0.043). Amongst the false-positives, perceived

Table 2 Depression, state anxiety, dimensions of illness worrya and breast cancer susceptibility in the process of screening. Prescreening

Depression Anxiety Illness worrya CP/BP

M S.D. M S.D.

M S.D. EfS M S.D. Th M S.D. HH M S.D. WI M S.D. TE M S.D. FI M S.D. Breast cancer susceptibility severity M S.D. susceptibility M S.D.

2 Months postscreening

12 Months postscreening

NF M S.D.

FP M S.D.

REF M S.D.

NF M S.D.

FP M S.D.

REF M S.D.

NF M S.D.

FP M S.D.

REF M

7.82 7.60 34.21 10.18

7.24 7.02 33.71 9.64

7.76 7.82 34.83 10.27

6.58 7.24 33.91 9.58

6.89 6.95 34.86 9.99

7.00 7.59 35.36 11.00

7.44 7.94 34.33 9.96

7.54 8.17 33.17 10.46

6.61 7.12 33.33 9.05

3.70 2.43 2.10 2.83 1.97 2.08 5.01 2.09 5.48 2.88 3.95 2.15 3.03 3.39

3.60 2.51 2.08 2.68 1.86 2.01 4.84 2.17 5.78 2.93 4.05 2.01 2.99 3.12

3.92 2.74 2.00 2.61 2.04 2.16 4.79 2.16 5.55 3.15 4.05 2.19 3.01 3.45

4.05 2.70 2.39 2.91 2.06* 2.26 4.78 2.02 6.47 3.00 4.03 2.28 3.12* 3.45

3.93 2.52 2.21 2.80 1.76* 1.99 4.90 2.11 6.27 2.96 3.92 2.19 2.54* 2.92

5.34* 1.63 10.42 2.26

5.12* 1.54 10.38 2.68

4.21 2.72 2.15 2.72 2.22* 2.23 4.79 2.09 6.56 3.12 4.07 2.27 2.96* 3.25 5.29 1.72 10.35 2.46

± ± ± ±

± ± ± ±

± ± ± ±

3.79 2.55 2.25 2.83 2.06 2.04 4.77 2.14 5.70 2.92 4.11 2.29 3.27* 3.59 5.43 1.62 10.45 2.05

3.70 2.50 1.85 2.60 1.86 2.03 4.79 2.13 5.77 3.09 3.82 2.29 2.82 3.05

3.93 2.50 2.02 2.73 1.95 2.17 4.89 2.04 5.60 2.85 3.86 2.23 2.70* 3.20

5.42 1.51 10.72* 2.16

5.31 1.51 10.19* 2.26

The groups normal ®ndings (NF, prescreening n=694±724 (varying due to missing values); 2 months postscreening n=575±626; 12 months postscreening n=560±567), false-positives (FP, n=287±298/237±255/221±228, respectively) and referents (REF, n=845±901/650±707/345±349,b respectively); M, means; S.D., standard deviations; and statistical signi®cance tested by two-sided Student t-tests. a CP/BP, concern about pain/bodily preoccupation; EfS, e€ects of symptoms; Th, thanatophobia; HH, health habits; WI, worry about illness; TE, treatment experiences; FI, fear of illness. b 304 women had entered the screening programme during the follow-up. ± not measured due to avoiding anxiety arousal. *Statistically signi®cant between-group di€erences prescreening. Th, NF/FP (1.946 (1015), P=0.050), FP/REF (3.162 (1193), P=0.002); FI, NF/ FP 2.542 (1019, P=0.011, REF/FP (1.967 (1197), P=0.049), breast cancer severity, NF/FP (1.970 (1004), P=0.049); at 12 months: FI, NF/REF (2.22 (914), P=0.016; breast cancer susceptibility, FP/REF (2.78 (569), P=0.006).

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Table 3 Reported beliefs and practices of breast cancer in the screening process. Prescreening NF FP % %

REF %

2 months postscreening NF FP REF % % %

12 months postscreening NF FP REF % % %

Intrusive thinking of breast cancer Never/seldom Occasionally Often/all the time

± ± ±

± ± ±

± ± ±

n=620 n=251 n=705 37 35 46 61 55 50 2 10 4 Chi2=36.62(df=4), P<0.001

n=564 n=229 n=349 41 27 43 57 65 53 3 8 4 26.47(df=4), P<0.001

Worried about breast cancer No/a little Somewhat A lot

± ± ±

± ± ±

± ± ±

n=619 n=252 n=706 71 51 64 28 44 33 1 5 3 39.38(df=4), P<0.001

n=563 n=229 n=349 65 53 63 34 42 34 1 5 3 16.96(df=4), P<0.001

BSE practice Never Occasionally Monthly Weekly or more frequent

n=530 20 54 21 5 ns

n=213 28 45 20 7

n=899 26 50 20 4

n=623 n=251 n=706 22 14 30 50 43 45 22 28 22 6 14 3 71.54(df=6), P<0.001

n=567 n=228 19 17 53 46 24 27 5 10 13.13(df=6), P<0.05

n=348 24 49 22 5

Con®dence in BSE No/not really Somewhat (Nearly) fully

n=533 19 42 39 ns

n=214 18 44 38

n=898 17 43 40

n=623 n=253 13 15 46 46 42 38 9.96(df=4), P<0.050

n=704 15 38 47

n=564 14 45 40 ns

n=229 22 47 31

n=346 16 46 38

Importance of BSE Not at all Quite Very

n=533 7 36 57 ns

n=214 6 40 54

n=898 7 40 53

n=623 8 41 51 ns

n=253 7 41 52

n=704 10 43 47

n=564 10 51 39 ns

n=229 9 48 43

n=346 11 50 39

Con®dence in breast cancer prevention No/not really Somewhat (Almost) fully

n=533 44 36 20 ns

n=214 42 36 22

n=896 44 34 22

± ± ±

± ± ±

± ± ±

n=563 40 34 26 ns

n=227 38 39 23

n=348 33 40 27

Perceived breast cancer risk Low/non-existent Moderate High Very high

n=722 28 22 42 8 ns

n=298 33 18 38 10

n=895 31 19 40 10

± ± ± ±

± ± ± ±

± ± ± ±

n=563 n=229 n=347 31 21 27 26 25 28 38 41 40 5 13 5 24.32(df=6), P<0.001

Healthy breasts No Yes

± ±

± ±

± ±

n=615 n=249 2 17 ± 98 83 ± 59.88(df=1), P<0.001

n=564 n=229 n=346 29 46 33 71 54 77 21.98(df=2), P<0.0001

Symptoms in breasts No Yes

± ±

± ±

± ±

n=615 n=249 85 75 ± 15 25 ± 10.90(df=2), P<0.004

n=567 n=229 n=345 85 75 85 15 25 15 12.57(df=2), P<0.002

The groups normal ®ndings (NF, n=530±533 (varying due to missing values) at prescreening, n=622±623 at 2 months, n=564±567 at 12 months postscreening), false-positives (FP, n=213±214/251±253/228±228, respectively) and referents (REF, n=898±900/704±707/346±348, respectively), % distributions, signi®cance tested by Chi squared testa ±, not measured due to avoiding anxiety arousal; BSE, breast self-examination; ns, non-signi®cant. a Test calculated over the three groups whenever possible and all the classes of the variable.

breast cancer severity increased from prescreening levels at 12 months (P=0.035). Amongst the referents, concern about pain/bodily preoccupation decreased from prescreening levels at 2 months (P=0.033), depression

decreased from prescreening levels at 12 months (P=0.018), anxiety ®rst increased from prescreening levels at 2 months (P=0.019) and then decreased at 12 months (P=0.003), and worry about illness decreased

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from prescreening levels at 2 months (P<0.001) and remained at that level at 12 months (P<0.001). 3.5. Multivariate analyses at 2 and 12 months postscreening In the multivariate analysis after adjustment for background factors, personality measures and the prescreening distress levels, the e€ect of group on distress was signi®cant at 2 months postscreening with a moderate e€ect size of 2.1% (Table 4). Univariate tests of MANCOVA revealed signi®cant e€ects on intrusive thinking and worrying about breast cancer Ð the falsepositives thought and worried more than the others. Excluding the outliers (n=124) the group e€ect was smaller (F= 1.52 (26, 1770), P=0.044), although the ES remained 2.2%; also the univariate e€ect for intrusive thinking was smaller without outliers whilst that for worrying remained the same (ES 0.8% for both). Thus, in general, the between-group di€erences were enlarged by the outliers. At 12 months, the group e€ect on distress was non-signi®cant (Table 4), with an ES of 2.5%; with univariate signi®cant e€ects in perceived breast cancer susceptibility, perceived breast cancer risk and intrusive thinking about breast cancer Ð those with false-positive ®ndings being most distressed. The group e€ect also remained non-signi®cant when the outliers were excluded. 4. Discussion In our prospective study with a long-term follow-up, including groups of normal ®ndings, false-positive ®ndings, as well as community referents, false-positive ®nd-

ings were related to an increased breast cancer-speci®c distress. In the univariate analyses, the false-positive group reported more intrusive thinking and worry about breast cancer, increased frequency of breast selfexamination, as well as a heightened perceived risk and more breast symptoms both 2 and 12 months postscreening. The groups also di€ered in distress in the multivariate analysis; intrusive thinking and worry about breast cancer were higher, in particular, in the false-positive group. The multivariate e€ect of distress was no longer statistically signi®cant 12 months postscreening. False-positive ®ndings seemed to function as a sensitising factor. This was seen in behavioural indicators of distress such as the increased practice of breast self-examination, even to excess levels of weekly or more frequent practice. This can hardly be seen to be bene®cial, especially when there is no good evidence that breast self-examination reduces breast cancer mortality. These women also paid more attention to their breast symptoms and/or had more symptoms than others and thus felt their breasts were less healthy than the other groups. The levels of general distress indicators of state anxiety and depression at all time points in the groups were in the range of the reference values (mean 34.05 (S.D. 10.10) for anxiety, 7.91 (S.D. 7.28) for depression) in the target population [31]. Amongst both the normal ®ndings group and the referents worry about illness decreased and mood improved during follow-up. Our study was able to overcome the diculties of many previous studies due to the large sample size. In addition, baseline measurements before screening invitation enabled us to avoid possible contamination e€ects of the invitation. There was a long-term followup of one year and both general standardised measures

Table 4 Signi®cant multivariate di€erences in distress 2 and 12 months postscreening between groups of normal screening ®ndings (NF), false-positive ®ndings (FP) and referents (REF) outside screening, prescreening valuesa, and background variablesb as covariates F value 2 months postscreening, NF n=365, FP n=147, REF n=560 Multivariate group e€ect 1.65 Univariate signi®cant e€ects Intrusive thinking 9.75 Worry about cancer 4.33 12 months postscreening, NF n=352, FP n=139, REF n=290c Multivariate group e€ect 1.10 Univariate signi®cant e€ects Perceived breast cancer risk 5.62 Perceived susceptibility 4.47 Intrusive thinking 3.09

df

P value

ES %

26,2024

0.020

2.1

2,1024 2,1024

<0.001 0.013

1.7 0.8

36,1432

0.449

2.5

2,733 2,733 2,733

0.004 0.012 0.046

1.5 1.2 0.8

E€ect size, ES%; df, degrees of freedom. Prescreening values of distress measures: level of anxiety, depression, illness worry (seven subscales), breast cancer susceptibility (two subscales), perceived breast cancer risk, breast self-examination frequency and con®dence. b Background variables: marital status, education, area of living, income, working status, serious illnesses in life, life changes, breast cancer in signi®cant others, previous mammogram, social support (6 items); trait anxiety and health locus of control beliefs (three subscales). c 304 women from the REF had entered screening and were thus excluded. a

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and breast cancer and screening speci®c measures were used. We also adjusted for the baseline distress levels, personality measures and background factors, and used e€ect size measures to indicate the magnitude of e€ects. Here we report results only on those women with falsepositive ®ndings who were recalled and went through further examination, where they were found not to have cancer. Our study does not include that small proportion of women (0.7%) that was sent further for a surgical biopsy, where half subsequently proved to have benign ®ndings. Women going through biopsy, including those with subsequent benign ®ndings, face a surgical intervention and a greater cancer threat and thus can get more distressed [5]. The generalisation of our results is somewhat weakened by our moderate response rate, especially prescreening. A moderate response rate was probably due to both a long, tedious questionnaire and the inability to send any targeted reminders prescreening because of the tight screening schedule. However, the non-respondents prescreening did not di€er from the respondents in the area of residence, which were the only data that were available about these non-responders. In addition, some of the signi®cant indicators of distress, e.g. thinking and worrying about breast cancer, were not measured prescreening due to the ethical considerations of avoiding unnecessary awakening of ruminative reactions. The group of referents at 12 months was markedly reduced because, women having their 50th birthday during the follow-up year, had entered the screening and were thus not included in the analyses. However, we still had approximately 300 referents at 12 months postscreening. We measured postscreening distress 2 and 12 months postscreening, not at screening, because we regard this long-term e€ect as more important than the immediate e€ect upon well being, subsequent health behaviour, and the impression that will be communicated further to other women. Distress related to the screening process and ®ndings can have public health consequences if it a€ects screening behaviour. Moderately perceived breast cancer risk, low con®dence in own capabilities in breast cancer prevention and a higher perceived susceptibility to breast cancer are predictive of attendance in mammography screening, whereas general distress measures are not [15,20]. Non-pathological worry seems to also motivate the uptake of self-initiated mammogram and breast selfexamination [32]. It looks like moderate distress does not deter from participation in the ®rst screening round, although a major problem in the generalisation of ®ndings is that screening non-participants tend to have low response rates in the surveys [15,20]. Recently [16] it was shown that the false-positive ®ndings in screening may even increase adherence to recommended screening. Nevertheless, as some reports show (e.g. Ref. [33]) that negative screening experiences may reduce re-attendance,

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screening organisers should put e€ort into reducing unnecessary distress whenever possible. High attendance is a prerequisite for a successful screening programme in the ®ght for a reduction in breast cancer mortality. The present data add to the studies showing moderate negative short-term psychological consequences amongst women with false-positive ®ndings in mammography screening [4±6,9,14,15,17,19]. We support Scaf-Klomp and colleagues [6]) who commented that although general distress might be short-lived, breast cancer worries last longer than a few months. False-positive ®ndings can have a quite lasting impact on the perception of a higher breast cancer risk and breast cancer as a more severe disease and can also increase preoccupation with thoughts and self-checking behaviour related to breast cancer, facts which have also been noted in earlier studies [4,33]. It is possible that standardised scales of distress do not tap breast cancer or screening-speci®c concerns. However, we believe that general distress is not increased in the screening process when the ®nding in the end proves to be normal. We claim that the breast cancer-speci®c distress, like ruminative thinking and worry about breast cancer, as well as excess breast self-examination are indicators of distress, which can be acted upon, for example by providing information and counselling in the course of screening. To guarantee high quality screening services, however, anxiety-provoking waiting times in the diagnostic process ought be kept as short as possible. There seems to be no need for special therapy interventions to alleviate psychological distress caused by an organised screening programme and the ®ndings from it. In this our data support Sutton and associates [15] and ScafKlomp and colleagues [6]. It may also be that organised screening can more easily provide information [4] Ð e.g. warning about possible false-positive ®ndings already in the invitation to screening as was carried out in our programme Ð and also psychosocial support than programmes relying on self-initiated attendance. Finnish women seem to have quite a good knowledge and realistic view of the breast cancer risk, lumps found in screening and of mammography as a screening method [20]. In addition, the public health screening programme keeps a rather low pro®le in an e€ort to ensure anxiety and fears are minimal. Increase of health habits in the normal ®ndings group, although only in the short term can be seen as a positive impact of screening. Health habits asked here were about avoiding unhealthy food and other things and about bodily checking. This suggests that screening could be further developed to enhance health knowledge and behaviour in the target group. This could be done by printed or other edited material without burdening the timetable and technical screening process. With this purpose in mind, we have developed a lea¯et in the

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context of the study to introduce mammography screening, and prepare women for the sometimes painful imaging [34] but also to give facts about breast health, early detection practices and contact addresses for the women invited to screening. Our descriptive results on decreasing distress from pre- to postscreening in the normal ®ndings group are in line with Sutton and associates [15] and Walker and colleagues [17]. Either there is a relieving e€ect following a breast health check with normal ®ndings Ð a position held by Scaf-Klomp and colleagues [6], or the decrease is due to repeated measurements. The latter appears most likely, since there was also a decrease in distress in the reference group. Organised mammography screening programmes for women 50 years and older, biennially or every three years, have an established role in western Europe. In these programmes false-positive rates are low, but in the course of several screening rounds and taking into account the large numbers of screened women, the number of those facing elevated cancer distress due to recall and false-positive ®ndings are substantial. However, as a public health programme targeted to asymptomatic population, organised mammography screening seems to be quite acceptable with only moderate shortterm negative side-e€ects of distress. Thus, these European programmes meet the consensus criteria of acceptability and minimal psychological harm for mammography screening [35]. This can be held as a counter-argument against the recent criticism of screening programmes [10], and as a green light for screening. However, the increase in breast cancer-speci®c concerns amongst women with false-positive screening ®ndings warrants further development in screening programmes together with the health education and support of all women in the target groups of screening. Acknowledgements We acknowledge ®nancial support from the Cancer Society of Finland, the Signe and Ane Gyllenberg Foundation and the YrjoÈ Jahnsson Foundation. We thank the screening centres and participating women. We are also grateful to Professors J. LoÈnnqvist and M. Koskenvuo, Dr M. Pamilo, and Ph.D.s K. LouhivuoriLaako and A. Uutela for participating in designing the study and formulating the hypotheses, W.P. den Brinker for his statistical advice, and M. Schreck for SURVO statistical analyses. References 1. Kerlikowske K, Grady D, Rubin SM, Sandrock C, Ernster VL. Ecacy of screening mammography. A meta-analysis. J Am Med Assoc 1995, 273, 149±154.

2. Fletcher SW, Black W, Harris R, Rimer BK, Shapiro S. Report of the International Workshop on Screening for Breast Cancer. J Natl Cancer Inst 1993, 85, 1644±1656. 3. Boer R, de Koning HJ, Therfall A, et al. Cost-e€ectiveness of shortening screening interval or extending age range of NHS breast screening programme: computer simulation study. N Engl J Med 1998, 317, 376±379. 4. Rimer BK, Bluman LG. The psychosocial consequences of mammography. J Natl Cancer Inst Monogr 1997, 22, 131±138. 5. Gram IT, Lund E, Slenker SE. Quality of life following false positive mammogram. Br J Cancer 1990, 62, 1018±1022. 6. Scaf-Klomp W, Sanderman R, van de Wiel HBM, Otter R, van den Heuvel WJA. Distressed or relieved? Psychological sidee€ects of breast cancer screening in The Netherlands. J Epidemiol and Commun Health 1997, 51, 705±710. 7. Thornton H. The voice of the breast cancer patient Ð a lonely cry in the wilderness. Eur J Cancer 1997, 33, 825±828. 8. Elmore JG, Barton MB, Moceri VM, Polk S, Arena PJ, Fletcher SW. Ten-year risk of false positive screening mammograms and clinical breast examinations. N Engl J Med 1998, 338, 1089±1096. 9. Lowe JB, Balanda KP, Del Mar C, Hawes E. Psychological distress in women with abnormal ®ndings in mass mammography screening. Cancer 1999, 85, 1114±1118. 10. Thornton H, Baum M. Should a mammographic screening carry the warning: screening can damage your health? Br J Cancer 1999, 79, 691±692 (editorial). 11. Lidbrink E, Elfwing J, Frisell J, Jonsson E. Negelected aspects of false positive ®ndings of mammography in breast cancer screening: analysis of false positive cases from the Stockholm trial. Br Med J 1996, 312, 273±312. 12. Fracheboud J, de Koning HJ, Beemsterboer PMM, et al. Nationwide breast cancer screening in the Netherlands: results of initial and subsequent screening 1990±1995. Int J Cancer 1998, 75, 694± 698. 13. Lerman C, Trock B, Rimer BK, Jepson C, Brody A. Psychological side e€ects of breast cancer screening. Health Psychol 1991, 10, 259±267. 14. Cockburn J, Staples M, Hurley SF, De Luise T. Psychological consequences of screening mammography. J Med Screen 1994, 1, 7±12. 15. Sutton S, Saidi G, Bickler G, Hunter J. Does routine screening for breast cancer raise anxiety? Results from a three-wave prospective study in England. J Epidemiol Commun Health 1995, 49, 413±418. 16. Burman ML, Taplin SH, Herta DF, Elmore JG. E€ects of falsepositive mammograms on interval cancer screening in Health Maintenance Organization. Ann Intern Med 1999, 131, 1±6. 17. Walker LG, Cordiner CM, Gilbert FJ, et al. How distressing is attendance for routine breast screening. Psycho-Oncology 1994, 3, 299±304. 18. Swanson V, McIntosh IB, Power KG. The psychological e€ects of breast screening in terms of patients' perceived health anxieties. Br J Clin Pract 1996, 50, 129±135. 19. Gilbert FJ, Cordiner CM, A‚eck IR, Hood DB, Mathieson D, Walker LG. Breast screening: the psychological sequelae of falsepositive recall in women with and without a family history of breast cancer. Eur J Cancer 1998, 34, 2010±2014. 20. Aro AR, de Koning HJ, Absetz P, Schreck M. Psychosocial predictors of ®rst attendance for organised mammography screening. J Med Screen 1999, 6, 82±88. 21. Kellner R. Abridged Manual of the Illness Attitude Scales. University of New Mexico, Albuquerque, USA, Department of Psychiatry, School of Medicine, 1987. 22. Spielberger CD, Gorsuch RL, Luchene R. Manual for the State Trait Anxiety Inventory. Palo Alto, CA, Consulting Psychologists Press, 1970. 23. Beck AT, Ward CH, Mendelson M. An inventory for measuring depression. Arch Gen Psychiatry 1961, 4, 561±571.

A.R. Aro et al. / European Journal of Cancer 36 (2000) 1089±1097 24. Stillman M. Women's health beliefs about breast cancer and selfexamination. Nurs Res 1977, 26, 121±127. 25. Fallow®eld LJ, Rodway A, Baum M. What are the psychological factors in¯uencing non-attendance and re-attendance at a breastscreening centre. J Roy Soc Med 1990, 83, 547±551. 26. Slenker SE, Grant MC. Attitudes, beliefs and knowledge about mammography among women over forty years of age. J Cancer Educ 1989, 4, 61±65. 27. Lau RR, Ware JF. Re®nements in the instrument of health speci®c locus-of-control beliefs. Med Care 1981, XIX, 1147±1157. 28. Little RJA, Schenker N. Missing data. In Areninger G, Clogg CC, Sobel ME, eds. Handbook of Statistical Modelling for the Social and Behavioral Sciences. New York and London, Plenum Press, 1995, 39±75. 29. Gi® A. Princals. Leiden, Leiden University. Department of Data Theory, 1985, 3±43. 30. Stevens J. Applied Multivariate Statistics for Social Sciences. Hillsdale, NJ, Laurence Erlbaum, 1996.

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31. Aro AR. Mammogra®aseulontaan osallistumista selittaÈvaÈt tekijaÈt (Psychosocial factors associated with participation in mammography screening). Kansanterveyslaitoksen julkaisuja A2/1996. Publications of the National Public Health Institute A2/1996, English summary, Helsinki, 1996. 32. McCaul KD, Schroeder DM, Reid PA. Breast cancer worry and screening: some prospective data. Health Psychol 1996, 15, 430±433. 33. Scaf-Klomp W, Sonderen FLP, van den Heuvel WJA. Compliance after 17 years of breast cancer screening. Factors associated with re-attendance for periodic breast screening. Eur J Publ Health 1997, 2, 1872±1877. 34. Aro AR, Absetz-YloÈstalo P, Eerola T, Pamilo M, LoÈnnqvist J. Pain and discomfort during mammography. Eur J Cancer 1996, 32, 1674±1679. 35. Kirkpatrick A, ToÈrnberg S, Thijssen MAO, eds. European Guidelines for Quality Assurance in Mammographic Screening. Commission of the European Communities. Report EUR 14821. Luxembourg, 1990, 1±15.