Participation in breast screening programs: A review

Sot. Sci. Med. Vol. 30, No. IO. pp. 1107-1118, Printed in Great Britam All rights reserved

PARTICIPATION

1990 Copyright

IN BREAST SCREENING A REVIEW

0277-9536/90 $3.00 + 0.00 Q 1990 Pergamon Press plc

PROGRAMS:

SALLY W. VERNON,’ * ELIZABETH A. LAVILLE? and GILCHRIST L. JACKSON’ ‘The University of Texas Health Science Center at Houston. School of Public Health, Houston, TX 77225, *M.D. Anderson Cancer Center, Houston, TX 77030 and ‘The Cancer Prevention Center of the Kelsey-Seybold Foundation for Medical Research and Education, Houston, TX 77030, U.S.A. Abstract-Despite recommendations by the American Cancer Society and other organizations for use of screening mammography, data on reported utilization of this procedure by American women show that these guidelines are not being met. We reviewed published studies that reported participation rates or that examined factors associated with participation in selected breast screening programs. In general, women at high risk due to age and family or personal history of breast disease were not more likely to participate in breast screening programs than women without those risk factors. The one group of variables that was fairly consistently associated with participation was the practice of other preventive health behaviors. Women who expressed more concern about their health and who were more knowledgeable about breast cancer screening and its benefits also were more likely to complete mammography. Approaches to increasmg participation are discussed in the context of the literature on this subject. Ky, words-mammography,

breast neoplasms. compliant behavior, cancer screening

INTRODL’CTION Breast cancer is the most frequently occurring cancer in women, and until recently it was the leading cause of cancer deaths in this group [l, 21. It also is a type of cancer for which early detection through screening mammography and physical examination of the breasts has been shown to improve survival [3-l l] in all but one study [12]. Although there are a few who would argue against routine breast screening [ 13-151, data are sufficiently convincing that both European and American groups have issued guidelines concerning the recommended frequency of mammography for women in various age groups. The National Cancer Institute, the American Cancer Society, the U.S. Preventive Services Task Force, and the American College of Radiology have issued recommendations for annual screening with mammography and breast palpation of women 50 years of age and older [16-191 and for periodic screening of women 40-49 years of age [16-181. The International Union Against Cancer Project on the Evaluation of Screening for Cancer, which includes researchers from a number of countries. recommends that “In countries where breast cancer is common and where the necessary resources are available, screening using mammography alone or mammography plus physical examination is applicable as public health policy” [20. p. 21. They concluded that screening women aged 5069 years will yield the greatest initial benefit. The European Group for Breast Cancer Screening meets annually to assess progress in the field of breast cancer research and to establish and maintain con-

*Address correspondence to: Professor Sally W. Vernon, School of Public Health, University of Texas Health Science Center. P.O. Box 20186. Houston, TX 77225, U.S.A.

tacts among breast cancer screening projects [21]. At the present time, recommendations for which age groups should be screened and for appropriate screening intervals vary somewhat across countries [20-241. Given the widespread official sanctioning of breast cancer screening, it is surprising that there is not greater acceptance of these procedures both by women who stand to benefit from them and by their physicians. Data on reported utilization of mammography by American women over 50 years of age show that only between 17 and 46% have had a mammogram some time in their lives [25-271, and an even smaller proportion in this age group receive it annually. Hall [28] estimated that only 5% of women over age 50 years have annual mammograms, although a Gallup survey [29] conducted in 1986 found that 19% of women 50 years of age and older reported having an annual mammogram. In any case, some of these procedures undoubtedly were done for diagnostic rather than for screening purposes. A greater proportion, between 42 and 58%, of women report having had a breast examination within the past year [27, 30, 311, but this association is inversely related to age, indicating that those women at greater risk are less likely to have breast examinations. These considerations underscore the importance of understanding what factors are associated with participation in screening programs for breast cancer. To this end, we reviewed the literature for programs that reported participation rates and for studies that analyzed factors associated with participation in breast screening programs. To be included in this review, the breast screening program had to be offered to a defined population of women, e.g. women living in a defined geographic area or women belonging to a health maintenance organization (HMO). At the minimum. participation rates had to

1107

Tabiir

er ul. [2X. 291

cl ul. 1351

Rlmer

Laville

U.K. Sweden

45 64

240

240

a lecture

‘Employees

who

a risk assessment

form

IS]. Attendance

lecture,

and eligible

M

M

M

invited

$40

Free

Free

Free

Free

Free

?

Varied

Free

cost

were sent a letter

inviting

them

Of those maded

~50%.

No

NO

Yes

Yes

Yes Yes Yes

Yes

Y.3

Yes

was for screening.

m this age group

self-examination.

M

M

BSE

PE & M

&/or

PE &/or

PE & M

M

M

PE & M

employees

and were subsequently

the report

questionnaire

from

trial.

mammogram.

al the end of an educational

a risk assessment

form

returned

Worksite

Worksite

HMO

HMO

PE &/or

BSE = breast

services

services

M = mammography;

1985

1985

sites of the U.K.

but excluded

and Guildford

m the program

out a risk awssment

them

and completed

tilled

(2X] returned

are based on women

31%

‘Rates

Included

screening

exammation;

U)

Co.)

and/or

are: PE = physical

rates are for the Edinburgh

g-75 years were

U.S. (Vanderbdt

‘Participatmn

“Women

U.S. (Pennzoil

rates are for the first exammatlon

for the procedures

340

235

U.S.

WA/NJ)

I986

I985

(NY) U.S.

340

I963

U.S.

40-64

WA)

Social

1970

services

services

services

HMO

Social

1975

Italy

Social

Social

Social

Netherlands

I914

1977

1979

Rescreening

programs

(s)

sponsor

screening

date

breast Procedure

of selected

Slart

I. Description

3545

Table

40-70

5&64

Location

(yr)

‘Participation

“Abbreviations

CI nl. 1391

er ul. 127)

Carter

Rutledge

rr al. [33. 341

Fink

r, ul. [IO, I I]

ZI al. [36]

Palli

Verbeek

el al. (61

er ul. [S, 301.

de Waard

Collette

CI ul. 132).

[31, 37, 381

er al. 191

Trial

Fag&erg

U.K.

Authors

Age range

assessment

Letter

Lecture

Educational

Letter

Letter

Letter

Letter

Letter

Letter

Letter

Letter

for screening.

rirk

About

forms.

method

of contact

Initial

75%

82%

attended

1271 and

25

49’

42’

w

64

60

85

72

896

69

61/69=

rate (%)h

Participation

H

Participation

be reported. Studies of factors associated with completion of screening were carried out in conjunction with a number of programs, usually on a sample of participants and nonparticipants. We reviewed only those studies in which an attempt was made to draw a representative sample of the study population or in which an attempt was made to survey the entire population. SCREENING

PROGRAMS

FOR BREAST

1109

in breast screening programs

CANCER

Table 1 describes a number of characteristics of selected breast screening programs including the age and location of the study population, the year the program began, the sponsor, procedures offered, cost, method of contact, whether or not women were invited for periodic re-screening, and .participation rates [5, 6,9-I 1, 32-401. All of the European studies were based on women living in defined geographic areas [5, 9-l 1, 35, 37,41-43]. Three [32, 34, 381 of the five [32,34,38,40,44] programs in the United States (U.S.) were based on women who were members of HMOs, and two [40,44] were conducted in occupational settings. Most programs used age to determine eligibility for screening [6, 11,25, 34. 37,41,43] although two used other factors as well as age [32,40]. The age range varied across studies, but in general, the focus was on women in their forties and fifties. Most of the programs began in the 1970s and 198Os, many in response to the findings of the Health Insurance Plan (HIP) randomized trial that found a reduction in mortality among women assigned to the study group who received breast screening with physical examination of the breasts and mammography [45]. In all of the programs, breast screening consisted of physical examination of the breasts or mammography or both, and most were provided free of charge (Table I). In all but one program [40], the initial method of contact was by mail. In that program the initial contact was a lecture on cancer detection and prevention, conducted at the worksite, where attendees completed a risk assessment questionnaire that determined whether or not they received a letter of invitation for screening [40]. Two other programs [32, 341 also employed a two-stage screening process; the first stage involved returning a mailed risk assessment questionnaire, and based on those responses, women were invited for breast screening. Precise comparisons among programs of the content and source of the invitation were difficult to make because none of the authors reproduced the material. In a few of the programs [34,43], the letter of invitation came from the woman’s own physician, but in most [6. 9,32, 38,40.44] it appeared to emanate from a more impersonal source. Some invitations offered a tentative appointment [38,42] while others included information about how to schedule an appointment. Most invitations appeared to include some educational messages or material about breast cancer and screening. Most of the programs also appeared to follow-up the initial invitation with ar least one subsequent mailed invitation, and one [38] used more intensive follow-up methods to recruit women into the program.

Baseline examinations

Attendance rates ranged from 25 [44] to 89% [9] (Table 1). In general, European programs 19, 11, 35,41,42] reported higher rates than those conducted in the U.S. [32,33,38,40,44]. In programs which used a two-stage process [32-34,401, participation rates were based on eligible women who completed a risk assessment questionnaire and who subsequently were invited for mammography. Thus, overall completion rates based on the number of eligible women in those study populations were lower than the rates shown on Table 1. Conversely, the completion rate of 89% reported for the Swedish program was higher than the actual rate because women over 74 years of age were excluded from the report, and the completion rate for women in that age group was less than 50% [9]. Two programs [33,40] also involved screening for

colorectal

cancer,

and

those

studies

reported

somewhat

lower attendance rates. In one study [33], women over 50 years of age were asked to return a breast risk assessment questionnaire as well as a fecal occult blood test (FOBT) prior to receiving an authorization form for a free mammogram. Thirtyeight percent of the women in the breast-risk-only group returned the questionnaire compared with only 24% of those also asked to complete the FOBT. In another study 1401, 52% of the women invited only for breast screening completed mammography compared with 46% of those who were invited for both breast and colorectal cancer screening. Re -screening examinations

Very few studies reported completion rates for re-screening examinations [6, 11,37, 391. In the HIP study [39], 60% of those who participated in the initial examination had three subsequent annual examinations. However, completion of all four examinations differed by effort required to bring women in for the initial examination: 67, 50, and 38% of the women requiring an increasing amount of follow-up completed all four examinations. The latter observation is consistent with the finding of de Waard et al. [6] who reported that women responding to the second invitation at the initial screening examination were three times more likely not to attend the second screening examination than women responding to the first invitation. In that study 161, women were invited for subsequent examinations only if they had attended the prior examination. In all [6, 11, 35, 391 but one [37] program subsequent examinations were less well attended than the baseline examination. In Sweden, the program which was an exception, over 80% of the age-eligible women who were assigned to the study group and had not moved out of the study area completed three screening examinations [37].

FACTORS

ASSOCIATED

WITH

PARTICIPATION

Studies of factors associated with participation were conducted in conjunction with a number of the programs discussed above. Some characteristics of these studies including sample size, study design, data collection method, and response rates from efforts to interview participants and nonparticipants are shown

SALLYW. VERNON~I al.

1110 Table 2. Studies

Authors French Maclean Calnan

Hobbs

et al. [43] et al. [44] [41]

of nonoarticination

in breast screenine Data collection method

Study design

Study population

Sample size

R

Edinburgh. U.K. Trial

90 P 110 NP

68 P 49 NP

Interview

Ps interwewed at screening; NPs viewed at home or at the clime.

R

Edinburgh. U.K. Trial

150 NP

>90

Interview (at home)

21 women Interviewed

L

Unnamed site. U.K. Trial

854

77

Interview (at home)

Interviews were conducted at least I month before screening invitation. Questtonnaire based on HBM.

300

-

Interview

Quota sampling was used to interview 100 women in each of 3 groups: Ps. NPs. and self-referred women.

Interview

Ps interviewed at screening. NPs mterviewed by telephone. Data for Ps were analyzed by amount of &Tort required to bring them in for screening. Sample was drawn from wcmen who returned a nsk assessment form and were sent an authorization for a free mammogram. Symptomatic women were excluded.

er al. 1421

R

South Manchester, U.K. Trial

Fink et al. [33,34]

R

HMO,

U.S.

II25 P 301 NP

Rimer et al. [28, 291

R

HMO.

U.S.

484 P&NP

Telephone interview

Rutledge

R

Worksite, U.S.

1495

Mailed

L

Worksite. U.S.

103 P 107 NP

Laville

er al. [39] et al. [35]

“Abbreviations

moerams”

Response rate (%)

used in the table. R = retrospective;

L = longitudinal;

on Table 2. Most investigators interviewed a sample of participants or nonparticipants or both at the time of screening or afterwards [33, 34, 38, 39,44,46-49], but two studies (40,461 gathered attitudinal, health status, or risk factor data prior to the invitation to the program. One study [46] collected data on attitudes and beliefs by interviewing women in their homes one month prior to initiation of the program. The other study [40] collected demographic and risk factor information at the time of an educational lecture on cancer. Some studies examined different subgroups of participants or nonparticipants [38,44,47,48]. Women in the study by’ Fink et al. [38] were divided into four subgroups based on the effort required to bring them into the program: (1) women attending after one mailing (minimum effort group), (2) women who didn’t appear for a scheduied examination and who required additional letters (secondary effort group), (3) women for whom telephone calls or repeated attempts to re-schedule examinations were needed (repeated efforts groups), and (4) nonattenders. Although French ef al. [48] also sampled three groups of nonattenders, they did not analyze their data separately for these subgroups. In addition to interviewing both invited attenders and nonattenders, Hobbs et al. [47] also interviewed women who came for screening of their own accord. i.e. self-referred attenders. Differences in methodology across studies were not great. The primary difference was the method of ascertaining information. One study used telephone interviews [34], one used a mailed questionnaire (441, one used a self-reported questionnaire filled out at the end of a lecture [40], and five used in-person interviews [38,4-91. Two studies [38,48] used different

90 P 75 NP

Self-report questionnaire

P = participant;

NP =

Comments

Questmnnalre

had been screened as reluctant Ps.

inter-

and were

based on the HBM.

Questionnaire on cancer risk factors was completed at the end of an educational lecture. Women were invited for screening based on those responses.

nonparticipant; I-IBM= healthbeliefmo&{.

methods of collecting information from participants and nonparticipants. Interview completion rates were higher for participants than for nonparticipants in all studies reporting this information [34, 38,46, 481. Factors associated with participation screening examination

in baseline

Variables studied in relation to participation can be grouped into six categories: (1) demographic characteristics, (2) medical history and health status information including risk factors for breast cancer, (3) use of medical services and other health behaviors, (4) logistic barriers, (5) beliefs, attitudes, and knowledge about cancer and health care, and (6) intentions. Not all studies included all factors. In fact, apart from some of the demographic variables, there was surprisingly little overlap across studies in the variables examined. Most studies used only bivariate analysis. characteristics. The association Demographic between age and completion of breast screening was generally consistent across studies. All but two [44,48] reported an inverse association between age and completion of screening [6,9, 11, 38,40,46. 47,491. Several studies found that completion was especially low among women over 70 years of age [6, 9, 1 I]. In the Hobbs et al. study [47] where women who were invited for screening were compared with women who were self-referred, women who came in response to the invitation were older than those who initiated the screening process themselves. In fact, the age distributions of attenders and nonattenders were more similar to each other than to that of selfreferred women. Most studies that included socioeconomic status variables found a positive association with comple-

Participation

in breast screening programs

tion. Education was positively associated with mammography completion in three studies [38,44,49]; only one [46] reported no association. One study (381 included income and reported no association with completion, but this could be due to trunc%tion of the range of income because nonattenders were a sample of homes with telephones and 25% of the nonattenders did not have a telephone. Three studies [46,47,49] used a measure of social class based on occupation of head of household. Two [47,49] found a positive association with completion and one found no association [46]. Hobbs et al. [47] and Maclean et al. [49] compared social class distributions of invited attenders and nonattenders with self-referred attenders and found that self-referred women were more likely to come from the upper social classes than attenders or nonattenders. As with age, the social class distributions of the invited attenders and nonattenders were more similar to each other and to Census data than to the distribution for women who came in on their own. Rutledge er al. (441 also reported a positive association between occupational status and completion among women employed by a university; faculty were more likely to complete screening or to have had a recent mammogram than women who were nonprofessional patient care workers. No differences were found between attenders and nonattenders by work status, i.e. employed outside the home or not, in one study [46]. Another found that attenders were somewhat more likely to work outside the home than nonattenders, but invited attenders were less likely to be employed outside the home than self-referred women [47]. Only one study [38] included religion and found that proportionately more Jews than Catholics completed screening. Rimer er al. [34] found that whites were more likely to complete mammography than nonwhites. A number of studies [6,34.38,44,46,48] examined marital status in relation to participation, and results were inconsistent. Two studies [38,44] reported no association between being married and completion, and three [34,46,48] reported that married women were more likely to complete screening. In contrast, one study [6] found that single women were more likely to complete screening than married or ever married women, especially those with large families. None of these studies controlled for potentially confounding variables such as age or socioeconomic status. In the Fink et al. study [38] where attenders requiring minimum effort were compared with attenders requiring repeated effort, there were no differences for age, race, education, occupation, income, marital status, or work status. Women requiring repeated efforts were somewhat more likely to have been born in the U.S. than to have been foreign-born compared with the minimum effort group and to be Catholic. Medical history and health status information including risk factors jar breast cancer. Five studies

[6.40.44,47. 481 looked at the association between reported family history of breast cancer and completion of screening. Laville et al. [40] found a negative association among women invited only for breast

1111

screening, i.e. women with a family history were less likely to complete screening. This finding is consistent with the other worksite-based study [44]; however, women in that study who reported recently having had a mammogram on their own were more likely to have a family history than nonattenders. In the study by Laville et al. [40], women over 50 years of age also were invited for colorectal cancer screening. Among women invited for both types of screening, there was a nonsignificant pattern for women with a family history to be more likely to complete breast cancer screening than those without such a history. Thus, the negative association between participation and family history among women invited only for breast cancer screening could be due to their younger age. Two studies [47,48] found no association while de Waard et al. [6] found a positive association between completion and having a mother with breast cancer, but no association when the relative was a sibling. Three studies [40,44,47] examined reported personal history of breast disease in relation to mammography completion. Hobbs et al. [47] found little difference between invited attenders and nonattenders, about 13% of attenders and nonattenders reported a history of breast disease compared with 36% of the self-referred women. Consistent with those findings, Rutledge er al. [44] reported that about 15% of the participants and nonparticipants had lumps or fibrocystic disease compared with 50% of the women who had been screened before the program began. Laville er al. [40] also found no association between personal history and mammography completion. Fink et al. [38] found that women who reported ever having felt a lump in their breast or who reported having breast symptoms before their period were more likely to complete screening; no differences were observed between the minimum effort and repeated effort groups of attenders. In that study there was no difference among the groups of attenders on self-rated health or for how often women thought about their health; this question was not asked of nonattenders. Use of medical services and other health behaviors. In the study by Fink et al. [38] attenders were more than twice as likely as nonattenders to have used an HIP physician during the year prior to screening. This differential pattern of use also was observed for the minimum effort versus the repeated effort groups of attenders. Additional questions on medical service use were asked only of the subgroups of attenders. Repeated effort attenders were more likely not to have used any physician in the past year and were more likely not to have an HIP family physician. Five studies [34,38,46,47,49] examined the association between mammography completion and other self-reported health behaviors. Completion of breast screening was positively associated with having undertaken other health behaviors such as regular dental checkups, use of seat belts, previous breast, cervical, or FOBT screening, or chest X-rays [46,47,49]. Fink et al. [38] found that minimum effort attenders were more likely than repeated effort attenders to have been vaccinated against polio. In

1112

SALLY

W.

contrast, Rimer et al. [34] found that attenders were not more likely to report practicing BSE. In the study by Hobbs er al. [47], women who were self-referred were far more likely than invited attenders to report the practice of other health behaviors and to have actively sought out tests and procedures. Logistic barriers. Four studies [6, 34, 38.441 looked at logistic barriers to participation such as cost or transportation. De Waard et al. [6] found that women who were privately insured were more likely to complete screening than those who depended on a ‘Sick Fund’. Consistent with that finding, Rutledge et al. [44] reported that one-third of the women not participating in the program cited cost as a barrier. Although Rimer et al. [34] found that attenders and nonattenders did not differ in reporting cost as a barrier, those women were offered free breast screening. Fink et al. [38] found no association between travel time and completion for the subgroups of attenders; this question was not asked of nonattenders. Beliefs, attitudes, and knowledge. Four studies [34, 38,47,48] looked in some detail at attitudes, knowledge, or beliefs about breast cancer and screening; however, even when the same concept was used, the operational definition differed. Two studies [38,48] found a positive association between thinking that it was better to know if one had cancer and mammography completion. In the study by Fink et al. [38], attenders were more likely than nonattenders to report having wondered whether or not they had cancer, and minimum effort attenders were more likely to have wondered if they had cancer than repeated effort attenders. Consistent with those findings, Rimer et al. [34] found that attenders were less likely to report that they would rather not think about mammography. Hobbs et al. [47]. found a positive association between believing that cancer can be cured and program attendance among those invited for screening; self-referred attenders were even more likely than invited attenders to hold this belief. Fink et al. [38] found no difference among subgroups of attenders for this belief; nonattenders were not asked this question. Several studies [34, 38,48,49] found that nonattenders were more likely to believe that X-rays, check-ups, and mammograms were only needed when one was sick or had symptoms. In one study 1381, nonattenders were more likely than attenders to believe that their doctor already knew about their health conditions without their having to take any more special tests; there were no differences among the subgroups of attenders. Repeated effort attenders, however, were more likely than minimum effort attenders to agree that physical exams make you worry and that to have them is to look for trouble [38]. Two studies [34,44] found that nonparticipants were more likely to report that their physician had not recommended mammography. Rimer er al. [34] reported that women who completed mammography were more likely than those who did not to think that the educational materials were useful and reassuring. Women who did not complete mammography were more likely to believe that mammography was inconvenient; they also were

VERNON er

al.

more likely to be worried about radiation and not to realize that the examination was free [34]. Rutledge er al. [44] found that women who completed mammography were more likely than those who did not to perceive themselves as more susceptible to breast cancer. to perceive benefits from screening, and to be more knowledgeable about breast cancer, but there were no differences in the perceived severity of the disease. Intentions. Only one study looked at intentions. Calnan [46] found a strong positive association between intention to attend and attendance at the screening program. Factors associated with participation in re-screening examinations Only two studies [6, 391 examined factors associated with completion of rescreening. De Waard et al. [6] found that younger age and having a mother who had breast cancer were important determinants of rescreening. Fink et al. [39] also found that younger women (aged 4&49 years) were more likely to complete the additional examinations, but. in contrast to de Waard et al. [6] they found that women with a family history were not more likely to complete the series of examinations. De Waard et al. [6] found that women who paid a reduced fee for the initial screening examination, i.e. those who did not have private insurance, were somewhat less likely to complete the second screening as were women who were on drug therapy for heart disease or diabetes at the time of their first examination. Fink et al. [39] found that black and white women were equally likely to complete the examination series and that women in higher categories of education, income, and occupation were more likely to complete all examinations. Although Fink et al. found that women who worked outside the home were as likely as those who did not to complete the full series of examinations, the amount of time it took to travel to the screening location was associated with completion of all four exams; 63% of the women who travelled 15 min or less compared with 50% of women who travelled 30 min or more completed the series. Similar to the differences between attenders and nonattenders at the baseline examination, women who reported that they had an HIP family physician and those who had been to their medical group one or more times during the year prior to the initial screening examination were more likely to complete the series than women who did not report these contacts [39]. Of particular interest was the finding that there were few associations between views of screening expressed at the baseline interview and completion of later examinations [39]. The exceptions were that women who thought that physical examinations make you worry and to have them is to look for trouble were less likely to complete the series. Women who sometimes worried that they might have cancer or who reported breast problems at the initial examination were more likely to complete the later examinations. In all of these comparisons, women in the minimum effort group were more likely than women in the repeated effort group to complete all examinations [39].

Participation

in breast screening programs

DISCUSSION

The estimates shown on Table 1 for participation in breast screening programs ranged between 25 and 89% and are similar to those for cervical screening which ranged from 23 to 89% [50] and to FOBT screening programs which ranged from 8 to 80% [51]. In general, the findings related to age and to family and personal history of breast disease do not support the idea that breast screening programs are reaching high-risk women. an observation consistent with the literature on cervical screening [50, 521. The failure to find a positive association between family or personal history of breast disease and screening participation could occur if women had already sought medical care because of those risk factors. This interpretation is consistent with the finding of Hobbs et al. [47] that women who were self-referred were more likely than attenders or nonattenders to report a personal history of breast disease and with the findings of Rutledge et al. [44] who reported that a high proportion of women with a personal history of breast disease had been screened prior to the program. Most studies reported a positive association between social class indicators and screening completion [38.44,47,49]. Those associations may reflect differences in knowledge about breast cancer and the role of screening in early detection, attitudinal differences, or differences in the ability to pay for the procedure. Only three of the studies reviewed examined cost as a barrier, and two [6,44] found that it was a deterrent. Although attenders and nonattenders in the third study [34] did not differ in reporting cost as a barrier, those women were offered free screening. That cost is a deterrent also is supported by the findings of other studies. Lane and Fine [53] examined the effect of cost and found that offering mammograms free of charge increased compliance and that this effect was inversely related to income; cost.was the most significant factor inhibiting participation among asymptomatic women with normal clinical findings. Johnson and Murata [54] also found that the prevalence of screening at a family health center ranged from 8% for women who were uninsured to 42% for those who were members of an HMO. Consistent with those findings, Lurie et al. [55] reported that cost-sharing was associated with less preventive care for cervical cancer in the Rand Health Insurance Experiment. although the, level of preventive care was low under free care as well. Moreover, cost of mammography was the reason most often given by physicians for disagreeing with American Cancer Society guidelines [56]. The group of variables most consistently associated with screening completion was the practice of other preventive health behaviors such as having regular dental checkups. using seat belts, and having previously had other medical tests and procedures including a mammogram, pap smear. FOBT, or chest X-ray [46.47.49]. In one study [47] there was a gradient of response showing that women who were self-referred for breast screening were the most likely to engage in other preventive health behaviors, followed by women who attended after receiving an invitation. followed by women who did not attend. Consistent with this pattern. Fink et al. [38] found that minimum effort attenders were more likely than

1113

repeated effort attenders to have been vaccinated against polio. Although there was little overlap in the specific measures of attitudes, knowledge, or beliefs across studies, there was general agreement that.participants were more likely than nonparticipants to wonder if they had cancer [38], to think it was better to know if they did [38,48], to be willing to think about mammography [34], to be more knowledgeable about cancer [35], and to believe in the benefits of screening [34,44,47]. In contrast, there were few systematic demographic, medical history, health status, or attitudinal differences across subgroups of attenders who required varying degrees of effort to complete screening [38]. Unfortunately, the basis for differences in attitudes and behavior is not well understood. None ‘of the studies reviewed here examined personality variables or psychologic status in relation to mammography completion; however, a study by Hunt er al. [57] found that women who accepted an invitation but did not complete screening had poorer scores on a measure of psychologic distress than two other subgroups of nonattenders or than attenders. Although not a study of participation, Morris and Greer [58] found that women attending a breast screening clinic did not differ from population norms on neuroticism or extraversion as measured by the Eysenck Personality Questionnaire. Hobbs et al. (471 pointed out that relatively little attention has been paid to the effects of different approaches to inviting women to participate in screening programs or to mechanisms whereby a woman negotiates an appointment for screening. This concern was reiterated by Eardley et al. [50] in discussing cervical screening programs; they noted that not only has little attention been paid to evaluating the efficacy of different types of invitations but also that the effectiveness of the accompanying health education material has not been assessed. Consistent with those observations, we found no studies of strategies to improve women’s participation in breast screening programs. In reviewing the studies discussed above we found what appeared to be a natural experiment of sorts. A report from a feasibility study for the U.K. trial [36] indicated that between 1 September 1975, and 30 June 1977, letters were signed by a woman’s general practitioner, and completion was 82%. Later in the trial, letters were computer-generated and signed by the director of the breast screening clinic [48], although the interest of the woman’s general practitioner was emphasized. In that report [48], completion was about 66%. Baines [59] reported that in Canada response was highest when women were sent personalized letters with follow-up telephone calls, although response rates were less than 20% for all methods of recruitment. Thus it appears that participation might improve if the invitation came from a woman’s own physician. This view is supported in a study by Smith et al. [60] of coronary heart disease in which response rates were higher for persons receiving a questionnaire from their general practitioner compared with those receiving letters from the research unit. Similarly, in a well-designed study of participation in an FOBT

1114

SALLYW. VERNON~I a(.

screening program [61] completion was higher among those receiving a letter from their own physician compared with those receiving an invitation from the Department of Community Health. The effect of increasing knowledge about colorectal cancer by a preliminary letter or personal interview also improved completion. The idea that the opinion of one’s own physician is an important determinant of participation was supported by a number of the studies reviewed here which interviewed women retrospectively about their reasons for participation or nonparticipation [34, 36, 38,491. It also is supported by Reeder et al. [62] who found that although only 15% of women interviewed had ever had a mammogram, 93% said that it was ‘somewhat likely’ they would have one if their physician recommended it. Moreover, of the women advised by their physicians to have a mammogram, less than 3% failed to do so [62]. Those findings support the view that providerinitiated programs could impact women’s screening behavior. The successful implementation of providerinitiated programs, however, requires that the problem of underutilization by physicians of mammography for their patients be addressed [56,63-69]. Although several recent studies [70-721 showed that mammography referral rates could be increased among residents exposed to various interventions, improvement in referral rates in the experimental groups over the comparison groups was modest in two of the three studies [70,71]. Two studies [65, 731 found that physicians were most likely to recommend or provide preventive services to their patients when they judged the importance of those services to be high. Further systematic study of educational intervention programs targeted at physicians is warranted. Whether or not more intensive educational efforts about breast cancer and the screening procedures would increase women’s participation also is an empirical question at this time. Surveys [74, 751 of knowledge, attitudes, and behavior concerning cancer prevention and risk showed relative stability over time. Those surveys, sponsored by the National Cancer Institute in 1983 and 1985, showed that approximately the same proportion of persons (-46%) believed that there was not much one could do to prevent cancer. An older study from the U.K. [76] also found few major shifts in women’s opinions about cancer between 1966 and 1973. In contrast, surveys before and after a pilot program in the Chicago area [77] showed a decrease in the proportion of women reporting fear of radiation (from 49 to 25%) and a similar decrease in the proportion of women who believed that BSE was sufficient for the early detection of breast cancer. In interpreting survey data as well as results from intervention studies now in the field [78-821, secular trends must be considered such as the increasing number of service projects, which are accompanied by educational efforts, including those sponsored by the American Cancer Society in Chicago [77] and Houston [83]. Leathar and Roberts [84] have directly questioned whether or not providing increased factual information would increase participation in breast screening

programs, particularly among older women. Qualitative analysis on data from small focus groups of women invited to participate in the Edinburgh site of the U.K. program suggested that emotional fears having to do with impending expectations of ill health were the basis of nonparticipation [84]. They suggested that providing positive reassurance and feedback to dispel those fears and putting breast screening in a broader context of general health care, rather than emphasizing screening for a single disease, might improve acceptance. Those views are consistent with a recent evaluation of the use of fear in health promotion campaigns [85]. Job [85] concluded that fear was effective only under certain circumstances where specific behaviors. if undertaken, would reduce the fear aroused by the campaign. Several studies reviewed here [34. 38,481 found that nonattenders expressed more concerns about cancer and about mammography than attenders. Moreover, several studies found .that women were not screened because they had no symptoms [34, 38,48,49]. The question is how to address those concerns and misconceptions so that more women will attend breast screening programs. One approach, recommended by Job [85], is a focus on shaping and reinforcing healthy alternative behaviors. In a recent study of predictors of BSE [86], belief in the value of BSE was the most important predictor of performance both in cross-sectional and in longitudinal analysis. Perceived vulnerability to breast cancer, while associated with performance, was less important. Other studies found that women who believed in their ability to detect lumps in their own breasts [87] and women who felt confident in their ability to perform BSE [88] were more likely than women who did not hold those beliefs to report practicing BSE monthly. Such findings indirectly support the suggestion of Leathar and Roberts [84] regarding the value of positive reassurance and feedback. Perhaps educational efforts would be more effective if directed at informing women that mammography can detect breast cancer in the absence of breast symptoms rather than increasing a woman’s perception of her susceptibility by emphasizing the prevalence of breast cancer and its risk factors. It is time to begin to test ideas about the relative effectiveness of the method and source of invitation and of the content of educational materials for breast screening programs. The relatively recent spread of HMOs in the U.S. provides a context for doing so because in this type of organizational structure, it is relatively easy to identify a defined group of women [89]. Unlike European countries that use some type of registry system, health care delivery in the U.S. has not, until recently, lent itself to identifying groups of persons who could be contacted easily and followed for programmatic purposes. Different methods of inviting women for screening as well as the effectiveness, or lack thereof, of different educational interventions could be evaluated in those defined populations of women for both client- and providerinitiated programs. In addition, HMOs also provide a context for intervention to alter physician behavior related to cancer screening practices. Although HMOs provide an important opportunity to study those issues, they serve only a limited

Participation

in breast screening programs

audience [89.90]. Women with fee-for-service insurance coverage and those with no insurance coverage will be missed. Women in the lower socioeconomic status groups and the elderly are most likely to have little or no insurance coverage. Although 75% of the U.S. population in 1986 reported that they had seen a physician wtthin the past year [91], only 60% of those with no insurance coverage had done so [92]. A recent study of cervical cancer screening [93] found that never having an obstetrician-gynecology visit and not having any outpatient visit within the past three years were risk factors for cervical cancer. Moreover, older women were more likely never to have visited an obstetrician-gynecologist [93]. This may be the case for breast cancer as well. In several studies reviewed here, older women (over 70 years of age) were less likely to attend breast screening programs [6,9, 111. Rimer et al. [94] found that older persons held a number of false beliefs and negative attitudes about cancer in general that might keep them from seeking treatment for symptoms. Thus, we must explore “the potential for creative opportunities to reach the underscreened” [95, p. 5111, including fixed or mobile clinics and taking advantage of opportunities for preventive care within the existing health care process when visits or hospitalizations occur for reasons unrelated to screening [95.96]. Another important issue that has not received systematic study is participation in and factors associated with repeated breast cancer screening. The findings from the few programs that included periodic breast screening showed that rates of completion for re-screening examinations tended to resemble those for the initial or baseline examination and varied from 30 to 80% [6, 11. 35, 37, 391. Two studies that reported factors associated with re-screening for breast cancer [6. 391 found that older age was consistently associated with nonattendance at repeated examinations. Women in higher education, income, and occupation categories were more likely to complete the series of examinations [39]. This is in contrast to the findings for cervical screening where Eardley er al. [50] concluded that once a woman is in the screening system, i.e. after they have already had one Pap test, the effects of age and social class are much less marked or do not operate at all. In a similar vein. there are virtually no studies of compliance with follow-up when a patient has a positive test. One study [98] found that 17% of women notified that they had an abnormal cervical smear failed to make or keep a follow-up appointment. Similarly, a number of persons were found not to respond to notification of a positive FOBT result [77]. There clearly is a need for more studies of those issues. Until more is known about the etiology of breast cancer. early detection is the primary means of control. and mammography has been shown to be a safe and effective method of early detection [67.97,99]. Recent studies (32. 100. 1011 indicate that the yield of detected cancers of various types can be increased by screening high-risk persons and by targeting cancer screening in defined geographic areas on the basis of population characteristics and variations in disease risk [ 1011. The observation. based on the studies reviewed here and others [102]. that

1115

high-risk women are no more likely to come for breast screening than women only nominally at risk suggests that interventions need to be developed specifically for those subgroups, i.e. older women and women with a family history of breast cancer. At the present time we do not know whether or not the same educational messages and contact strategies are equally effective across age, race, and socioeconomic groups. For example, Hobbs [IO31 noted that older women and those in the lower social classes may lack the social skills required to arrange a screening appointment. It may be that embedding screening in a broader context of general health care is a strategy that is effective for older women and those of lower socioeconomic status, as some [84,90] have suggested, but not for all subgroups of women. In a similar vein, Kerner et al. [ 101, p. 5441 suggested that it may be possible to design and promote screening programs “to take advantage of existing community social and cultural norms and support systems to change health behaviors related to cancer screening program utilization.” In discussing the concept of ‘avoidable mortality’ in relation to cervical cancer, Howard [95] emphasized that prevention strategies that are effective in one community are not necessarily effective in others. Because of some variability across individuals and communities in demographics, attitudes, ideologies, and social institutions, it is necessary to pilot test interventions prior to their widespread introduction. In conclusion, more studies are’needed not only of characteristics and attitudes of women invited for screening but also of characteristics and attitudes of physicians such as training and beliefs about the usefulness of breast screening [ 1031. One focus should be on how the social and psychologic characteristics both of women and of physicians mediate their understanding of the rationale for and importance of breast cancer screening. For example, anxiety induced by the fear of finding something wrong may inhibit participation unless this fear can be offset by an understanding that the procedure may lead to the detection of disease at a stage when medical treatment can reduce the feared consequences. Moreover, studies of participation would benefit from the systematic application of models or frameworks such as those discussed by Kegeles and Grady [104] and by Leventhal er al. [105]. One approach that has been used in screening programs for colorectal cancer conceptualizes participation as a process involving acceptance or agreement and attendance or completion [106]. This model is particularly appropriate for two-stage screening programs such as those where women return a risk assessment questionnaire prior to an invitation for screening and for programs conducted in the context of routine medical practice where physicians offer screening to eligible women who may or may not subsequently schedule an appointment. Although the voluntary nature of screening will always set limits on participation [95], Warren [107] observed that data from the Swedish study indicated that increasing participation from 60 to 80% could reduce the proportion of advanced breast cancers found. Thus, it is time to concentrate our efforts on developing strategies to increase and maintain

SALLY W. VERNON er al.

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participation in breast screening programs if we are to approach the National Cancer Institute’s goal of a 25-50% reduction in cancer mortality by the year 2000 [99]. Acknowledgemenr-Dr ship from Pennzoil Foundation.

Vernon is a recipient of a fellowCompany through the Kelsey-Seybold

REFERENCES

4.

5.

6.

7.

8.

9.

10.

II.

12.

13 14 15.

16.

American Cancer Society. Cancer Statistics. CA -A Cancer Journal for Clinicians 32, 1.5-31, 1982. American Cancer Society. Cancer facts and figures, 1989. Baker L. H. Breast cancer detection demonstration project: five-year summary report. CA-A Cancer >o&al for klinicians 32, i94-225, 1982. Chu K. C.. Smart C. R. and Tarone R. E. Analvsis of breast cancer mortality and stage distribution by age for the Health Insurance Plan-clinical trial. J. -nati. Cancer Inst. 80. 1125-l 132. 1988. Coilette H. J. A., Day N. E., Rombach J. J. and de Waard F. Evaluation of screening for breast cancer in a non-randomised study (the DOM project) by means of a casecontrol study. Lancef 1, 12241226, 1984. de Waard F., Collette H. J. A., Rombach J. J., Baanders-van Halewijn E. A. and Honing C. The DOM project for the early detection of breast cancer, Utrecht, The Netherlands. J. chron. Dis. 37, 144. 1984. Seidman H., Gelb S. K., Silverberg E., LaVerda N. and Lubera J. A. Survival experience in the breast cancer detection demonstration project. CA-A Cancer Journal for Clinicians 37, 258-290, 1987. Shapiro S., Venet W., Strax P., Venet L. and Roeser R. Ten-to-fourteen-year effect of screening on breast cancer mortality. J. narn. Cancer Inst. 69, 349-355, 1982. Tabar L., Fagerberg C. J. G., Gad A., Baldetorp L., Holmberg L. H., Griintoft 0.. Ljungquist U., LundStrom B., Manson J. C., Kopparberg County Project Group, Ostergotland County Project Group, Eklund G.. Day N. E. and Pettersson F. Reduction in mortality from breast cancer after mass screening with mammography: randomised trial from the Breast Cancer Screening Working Group of the Swedish National Board ofHealth and Welfare. Lancef I, 829-832, 1985. Verbeek A. L. M.. Hendriks J. H. C. L.. Holland R.. Mravunac M. and Sturmans F. Mammographic screening and breast cancer mortality: age-specific effects in Nijmegen project, 1975-82. Lancer 1, 865-866, 1985. Verbeek A. L. M.. Hendriks J. H. C. L., Holland R.. Mravunac M.. Sturmans F. and Dav N. E. Reduction of breast cancer mortality through mass screening with modern mammography:first results of the Nijmegen nroiect. 1975-1981. Lancef 1. 1222-1224, 1984. Andersson I., Aspegren K., Janzon L., Landberg T.. Lindholm K.. Line11 F., Ljungberg 0.. Ranstam J. and Sigfusson B. Mammographic screening and mortality from breast cancer: the Malmo mammographic screening trial. Br. med. J. 297. 943-948, 1988. Bailar J. C. III and Smith E. M. Progress against cancer? New EngI. J. Med. 314, 1226-1232. 1986. Skrabanek P. False premises and false promises of breast cancer screening. Lancer 2, 316-320, 1985. Skrabanek P. The debate over mass mammography in Britain: the case against. Br. med. J. 297, 971-972, 1988. American Cancer Society. National Task Force on Breast Cancer Control: Mammography 1982: a state-

Society. CA-A Cancer 1982. College of Radiology. Policy statement: 17 American guidelines for mammography. American College of Radiology, Reston. VA, 1982. Cancer Institute. Working guidelines for 18 National early cancer detection: rationale and supporting evidence to decrease mortality. U.S. Department of Health and Human Services. Public Health Service. Washington. D.C., 1987. Services Task Force. Recommenda19. U.S. Preventive tions for breast cancer screening. J. Am. med. Ass. 257, ment of the American

Cancer

Journalfor Clinicians 32, X6-230.

2196,

1987.

20. Day N. E. and Miller A. B. (Eds) Screeningfor Breast Cancer. Hans Huber. Toronto, 1988. Group for Breast Cancer Screening. 21 The European Guidelines for breast cancer screening. Clin. Radio/. 38, 217, 1987. 22. Forrest P. Breast Cancer Screening. HMSO. London, 1986. J. Breast Cancer Screen23. Austoker J. and Humphreys ing: Practical Guides for General Practice. Oxford University Press. Oxford. 1988. 24. Tabar L. and Dean P. B. The present state of screening for breast cancer. Semin. Surg. Oncol. 5, 94101, 1989. Public awareness and use of 25. Gallup Organization. cancer detection tests: 1983 survey. Gallup Organization, Princeton, NJ, 1984. S. A basic study of public attitudes toward 26. Lieberman cancer and cancer tests. I. Major results. Lieberman Research, Inc., New York. 1979. Center for Health Statistics. Provisional 27. National estimates from the National Health Interview Survey Supplement on Cancer Control-United States. January-March 1987. J. Am. med. Ass. 260, 1206ff, 1988. prob28. Hall F. M. Screening mammography-potential lems on the horizon. New, Engl. J. Med. 314, 53-55, 1986. Public awareness and use of 29. Gallup Organization. cancer detection tests: 1986 survey. Gallup Organization, Princeton, NJ. 1986. 30. Makuc D. M. Changes in the use of preventive health services. In Health. Unifed Stales, 1981 [DHHS Pub]. N. (PHS) 82-12321, pp. 67-75. U.S. Department of Health and Human Services, Public Health Service, Office of Health Research. Statistics and Technology, Hyattsville, MD, 198 1. 31. National Center for Health Statistics. Use of selected medical procedures associated with preventive care: United States-1973. Vital and Health Statistics, series 10-110. U.S. Department of Health, Education and Welfare, Public Health Service, Health Resources Administration, Hyattsville, MD, 1973. R. S., Bourdeau R. V.. 32 Carter A. P., Thompson Andenes J.. Mustin H. and Straley H. A clinically effective breast cancer screening program can be costeffective, too. Pretlent. Med. 16,-19134, 1987. P. F.. Mvers R.. 33 Rimer B. K.. Davis S.. Enlrstrom Rosan J., Fox L. and McLaughlin R. An examination of compliance and noncompliance in an HMO cancer screening program. In Advances in Cancer Control: Cancer Control Research and the Emergence of rhe Oncology Product Line (Edited by Engstrom P. F.. Anderson P. N. and Mortensen L. E.), pp. 21-30. Liss. New York, 1988. 34 Rimer B. K., Keintz M. K.. Kessler H. B., Engstrom P. F. and Rosan J. Why women resist mammograms: understanding patient-related barriers to acceptance of screening mammography. Radiohgy. 172, 243-246, 1989. H. J. A., Rombach J. J., de Waard F. 35 Coilette and Collette C. An update of the DOM project for the early detection of breast cancer. In Screening /or

Participation

36

37

38

39

40

41

42

43

44

45

46

47

48

49

50

51

52

53

54

in breast

Breasr Cancer (Edited by Day N. E. and Miller A. B.). pp. 17-27. Hans Huber. Toronto, 1988. Edinburgh Breast Screening Clinic. Screening for breast cancer: report from Edinburgh Breast Screening Clinic. Br. med. J. 2, 175-178, 1978. Fagerberg C. J. Cl. and Tabar L. The results of periodic one-view mammography screening in a randomized. controlled trial in Sweden. Part I: background. organization. screening program, tumor findings. In Screening jar Breast Cancer (Edited by Day N. E. and Miller A. B.), pp. 33-38. Hans Huber, Toronto, 1988. Fink R., Shapiro S. and Lewison J. The reluctant participant in a breast cancer screening program. Publ. Hith Rep. 83, 479-490, 1968. Fink R., Shapiro S. and Roester R. Impact of efforts to increase participation in repetitive screenings for early breast cancer detection. Am. J. publ. Hlth 62, 328-336, 1972. Laville E. A.. Vernon S. W.. Jackson G. L. and Hughes J. I. Comparison of participants and nonparticipants in a work site cancer awareness and screening program. J. occup. Med. 31, 221-232, 1989. Palli D.. Del Turco M. R.. Buiatti E., Carli S., Ciatto S.. Toscani L. and Maltoni G. A case-control studv of the efficacy of a non-randomized breast cancer scrdening program in Florence (Italy). Int. J. Cancer 38, 501-504, 1986. U.K. Trial of Early Detection of Breast Cancer Group. Progress report of the U.K. trial of early detection of breast cancer. In Screening for Breasr Cancer (Edited by Day N. E. and Miller A. B.). pp. 4549. Hans Huber, Toronto. 1988. U.K. Trial of Early Detection of Breast Cancer Group. Trial of early detection of breast cancer: description of method. Br. J. Cancer 44, 618627, 1981. Rutledge D. N.. Hartmann W. H.. Kinman P. 0. and Winfield A. C. Exploration of factors affecting mammography behavior. Precent. Med. 17, 412422, 1988. Shapiro S.. Strax P. and Venet L. Periodic breast cancer screening in reducing mortality from breast cancer. J. Am. med. Ass. 215, 1777-1785, 1971. Calnan M. The health belief model and participation in programmes for the early detection of breast cancer: a comparative analysis. Sot. Sci. Med. 19, 823-830, 1984. Hobbs P.. Smith A.. George W. D. and Sellwood R. A. Acceptors and rejectors of an invitation to undergo breast screening compared with those who referred themselves. J. Epidem. commun. Hlrh 34, 19-22. 1980. French K., Porter A. M. D., Robinson S. E., McCallum F. M.. Howie J. G. R. and Roberts M. M. Attendance at a breast screening clinic: a problem of administration or attitudes. Br. med. J. 285, 617-620, 1982. Maclean U.. Sinfield D.. Klein S. and Harnden B. Women who decline breast screening. J. Epidem. rommun. Hlth 38, 278-283. 1984. Eardley A.. Elkind A. K.. Spencer B., Hobbs P.. Pendleton L. L. and Haran D. Attendance for cervical screening-whose problem? Sot. Sci. Med. 20, 955-962. 1985. Blalock’ S. J.. DeVellis B. M. and Sandler R. S. Participation in fecal occult blood screening: a critical review. Prerenr. Med. 16, 9-18. 1987. Magnus K.. Langmark F. and Andersen A. Mass screening for cervical cancer in Ostfold County of Norway 1959977. 1n1. J. Cancer 39, 311-316. 1987. Lane D. S. and Fine H. L. Compliance with mammography referrals: implications for breast cancer screening. .V-.l’. Sr. J. Med. 83. 173-176. 1983. Johnson R. A. and Murata P. J. Demographic. clinical. and financial factors relating to the completion

screening

55.

56.

57.

58.

59.

60.

61.

62.

63.

64

65

66

67

68

69.

70.

71.

72.

73.

74.

programs

Ill7

rate of screening mammography. Cuncer Defecr. Preuenf. 11, 259-266, 1988. Lurie N., Manning W. G., Peterson C., Goldberg G. A., Phelps C. A. and Lillard L. Preventive care: do we practice what we preach? Am. J. publ. Hlrh 77, 801-804. 1987. American Cancer Society. Survey of physicians’ attitudes and practices in early cancer detection. CA-A Cancer Joknal for Clinic&s 35, 197-213, 1985. Hunt S. M.. Alexander F. and Roberts M. M. Attenders and non-attenders at a breast screening clinic: a comparative study. Publ. Hlfh 102,3-IO, 1988. Morris T. and Greer S. Psychological characteristics of women electing to attend a breast screening clinic. Clin. Oncol. 8, 113-119, 1982. Baines C. J. Impediments to recruitment in the Canadian national breast screening study: response and resolution. Controlled Clin. Trials 5, 129-140, 1984. Smith W. C. S.. Crombie 1. K., Campion P. D. and Knox J. D. E. Comparison of response rates to a postal questionnaire from a genera1 practice and a research unit. Br. med. J. 291, 148331485. 1985. Hardcastle J. D., Farrands P. A., Balfour T. W.. Chamberlain J.. Amar S. S. and Sheldon M. G. Controlled trial of faecal occult blood testing in the detection of colorectal cancer. Lancer 2, 14, 1983. Reeder S.. Berkanovic E. and Marcus A. C. Breast cancer detection behavior among urban woman. Publ. Hlth Rep. 95, 276-281, 1980. Battista R. N. Adult cancer prevention in primary care: patterns of practice in Quebec. Am. J. publ. Hlfh 73, 1036-1039, 1983. Cummings K. M., Funch D. P., Mettlin C. and Jennings E. Family physicians’ beliefs about breast cancer screening by mammography. J. Fum. Pracf. 17, 1029-1034, 1983. Dietrich A. J. and Goldberg H. Preventive content of adult primary care: do generalists and subspecialists differ? Am. J. oubl. Hlth 74. 223-227. 1984. Fox S., Baum J. K., Klos D.‘S. and Tsou C. V. Breast cancer screening: the underuse of mammography. Radiolog?: 156, 607-611, 1985. Howard J. Using mammography for cancer control: an unrealized potential. CA-A Cancer Journal ,for Clinicians 37, 3348, 1987. McPhee S. J., Richard R. J. and Solkowitz S. N. Performance of cancer screening in a university generat internal medicine practice: comparison with the 1980 American Cancer Society guidelines. J. gen. intern. Med. 1, 275-281, 1986. Woo B., Woo B., Cook E. F., Weisberg M. and Goldman L. Screening procedures in the asymptomatic adult: comparison of physicians’ recommendations, patients’ desires, published guidelines, and actual practice. J. Am. med. Ass. 254, 148&1484, 1985. Cohen D. I., Littenberg B., Wetzel C. and Neuhauser D. B. Improving physician compliance with preventive medicine guidelines. Med. Cure 20, 1040-1045, 1982. Fox S., Tsou C. V. and Klos D. S. An intervention to increase mammography screening by residents in family practice. J. Fam. Pracf. 20, 467-471, 1985. McDonald C. J., Hui S. L.. Smith D. M., Tiemey W. M.. Cohen S. J., Weinberger M. and McCabe G. P. Reminders to physicians from an introspective computer medical record: a two-year randomized trial. Ann. intern. Med. 100, 130-138, 1984. Romm F. J.. Fletcher S. W. and Hulka B. S. The periodic health examination: comparison of recommendations and internists‘ performance. South. med. J. 74, 265-271, 1981. National Cancer Institute. Cancer Prevention Awareness Survey Technical Report. NIH Publ. No. 84-2677.

1118

75.

76. 77.

78.

79.

80.

81.

82.

83.

84.

85.

86.

87.

88.

89.

SALLY

W.

U.S. Department of Health and Human Services, Public Health Service. Washinaton. D.C.. 1984. National Cancer Institute. Cancer Prevention Awareness Survey Wave II. Management Summary. U.S. Department of Health and Human Services, Public Health Service, Washington, D.C., 1986. Knopf A. Changes in women’s opinions about cancer. Sot. Sci. Med. 10, 191-195. 1976. Winchester D. P., Lasky H. J., Sylvester J. and Maher M. L. A television-promoted mammography screening pilot project in the Chicago metropolitan area. CA-A Cancer Journal for Clinicians 38, 291-309, 1988. Fox S. A., Gallagher D. G. and Murata P. J. Utilization of mammography by women over 35 years of age in Los Angeles. Paper presented at the 1161h Annual Meetings of the American Public Health Association. Boston, MA, 15 Nov., 1988. Harris R. P., Fletcher S. W., Gonzalez J. J.. Lannin D. R., Earp J. and Kleinbaum D. G. 1988 breast cancer screening in rural North Carolina. Paper presented at the 116th Annual Meerings of the American Public Health Association, Boston, MA, 15 Nov., 1988. Rimer B. K., Keintz M., Engstrom P. F. and Rosan J. Predictors of participation in a breast screening program. Paper presented at the 116rh Annual Meetings of fhe American Public Health Association, Boston, MA, 15 Nov., 1988. Zapka J. G.. Costanza M. E., Stoddard A., Spotts D. and Barth R. S. Behavioral profiles of breast cancer screening in two northeast urban communities. Paper presented at the 116th Annual Meerings of the American Public Health Association, Boston, MA, 15 Nov., 1988. Lane D. S., Poiednak A. P. and Burg M. A. Evaluation of varied interventions on increasing community-wide breast cancer screening. Paper presented at the 116th Annual Meetings ofrhe American Public Health Associafion, Boston, MA, 15 Nov., 1988. Vogel V. G., Peters G. N., Fueger J. J. and Winn R. J. Analysis of barriers and incentives to mammographic screening in the American Cancer Society 1987 Texas Breast Screening Project. Prevent. Med. 17, 240-241, 1988. Leathar D. S. and Roberts M. M. Older women’s attitudes towards breast disease. self examination, and screening facilities: implications for communication. Br. med. J. 290, 668470, 1985. Job R. F. S. Effective and ineffective use of fear in health promotion campaigns. Am. J. publ. Hllh 78, 163-167, 1988. Calnan M. and Rutter D. R. Do health beliefs predict behaviour? A follow up analysis of breast self-examination. Sot. Sci. Med. 26, 463465, 1988. McCusker J. and Morrow G. R. Factors related to the use of cancer early detection techniques. Prevent. Med. 9, 388-397. 1980. Celentano D. D. and Holtzman D. Breast selfexamination competency: an analysis of self-reported practice and associated characteristics. Am. J. publ. Hlrh 73, 1321-1323. 1983. Shapiro S. Cancer control and the health-care system. Prevent. Med. 15, 321-329, 1986.

VERNON

et al.

90. Warnecke R. B.. Havlicek P. L. and Manfredi C. Awareness and use of screening by older-aged persons. In Perspectives on Precenrion and Trearmenr of Cancer in the Elderly, Vol. 24. Aging Series (Edited by Yancik R.), pp. 275-287. Raven Press. New York. 1983. Center for Health Statistics. Health, United 91. National States. 1987. DHHS Pub]. No. (PHS) 88-1232. US. Government Printing Office, Washington, D. C., Table 58, 1988. 92. Andersen R.. Chen M., Aday L. A. and Cornelius L. Health status and medical care utilization. Hlth Afluirs Spring, 136156, 1987. D. D., Klassen A. C., Weisman C. S. and 93. Celentano Rosenshein N. B. Cervical cancer screening practices among older women: results from the Maryland cervical cancer case-control study. J. clin. Epidem. 41, 531-541, 1988. 94. Rimer B., Jones W., Wilson C., Bennett D. and Engstrom P. Planning a cancer control program for older citizens. The Gerontologisr 23, 38&389, 1983. 95. Howard J. ‘Avoidable mortality’ from cervical cancer: exploring the concept. Sot. Sci. Med. 24, 507-514, 1987. 96. Fruchter R. G., Boyce J. and Hunt M. Missed opportunities for early diagnosis of cancer of the cervix. Am. J. publ. Hlrh 70, 418420, 1980. risk from mammography: is 97. Feig S. A. Radiation it clinically significant? Am. J. Roenrgenology 143. 469475, 1984. R., Diseker R. A., Young L. D. and May 98. Michielutte W. J. Noncompliance in screening follow-up among family planning clinic patients with cervical dysplasia. Prevenr. Med. 14, 248-258, 1985. Cancer Institute. Greenwald P. and Sondik 99. National E. J. (Eds) Cancer Control Objectives for the Nation: 1985-ZOOO.NC1 Monographs, 1986. recruitment 100. Halper M. and Diemer K. Risk-related increases cancer yield. Prevent. Med. 16, 274, 1987. 101. Kerner J. F., Andrews H.. Zauber A. and Struening E. Geographically-based cancer control: methods for targeting and evaluating the impact of screening interventions in defined populations. J. clin. Epidem. 41, 543-553, 1988. 102. Krischer J. P., Cook B. and Weiner R. S. Identification and screening of women at high risk of breast cancer. Cancer Detecl. Prevent. 13, 65-74, 1988. P. The behavioural aspects of breast and 103. Hobbs cervical screening. Radiography 52, 287-290, 1986. 104. Kegeles S. S. and Grady K. E. Behavioral dimensions. In Cancer Epidemiology and Prevention (Edited by Schottenfield D. and Fraumeni J. F.), pp. 1049-1063. Saunders, Philadelphia, PA, 1982. R. and Gutmann M. Com105. Leventhal H., Zimmerman pliance: a self-regulation perspective. In Handbook of Behavioral Medicine (Edited by Gentry W. D.), pp. 369436. The Guilford Press, New York, 1984. 106. Macrae F. A., Hill D. J.. St John D. J. B., Ambikapathy A., Garner J. F. and The Ballarat General Practitioners Research Group. Predicting colon cancer screening behavior from health beliefs. Precenr. Med. 13, 115-126. 1984. in 107. Wqrren R. The debate over mass mammography Britain: the case for. Br. med. J. 297, 969-970, 1988.