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Reductions in breast cancer mortality as evidenced in screening trials require mammographic screening to be routinely repeated1-5, as cancers are frequently detected even after several normal screens have been achieved3,6.
Despite the benefits of early detection obtainable through mammography, regular screening according to guidelines has not yet been widely attained. Although in most settings the majority of women report having had a mammogram, fewer report having had one recently, and still fewer (20%-27%) report having had multiple screens or an age-appropriate number7-9. Although repeated screening seems to be more prevalent in organized programs, results from nine rounds of screening in Nijmegen, the Netherlands, showed that less than 40% of women completed all rounds, despite 90% participating at least once5,6.
Participation in screening programs declines at subsequent screening rounds5,10, although women who do return are more compliant10,11. Women are more receptive of mammography if they have previously had a mammogram, and prior screening is strongly predictive of return for further screening12-15. Previous attenders are more likely to reattend than those who previously did not attend or who were previously ineligible to do so16. In a variety of settings, the proportion of previous attenders returning for rescreen was high (70%-90%), depending on the interval measured and the number of examinations considered14,17-24.
Despite the fact that prior screening increases the likelihood that women will return, in some settings even these women are unlikely to be rescreened, with reported frequencies of repeat screening as low as 25% to 57%25-29. The statistical cutoff interval for considering women as having returned for screening can have a major influence on the actual rate of repeat screening28,30.
Although many programs have successfully achieved high levels of attendance at rescreening, attendance within the recommended time intervals for rescreening is lower. Regardless of the recommended screening interval specified by the program, compliant attendance appears to be a further challenge. In a study of the National Health Service breast screening program in the United Kingdom, fewer than half of screened women had been rescreened within the recommended 3-year interval, although by 38 months nearly three-quarters had been rescreened and eventually nearly 90% returned for rescreen19. In an Australian program with a recommendation for biennial screening, the median time from first to second screen was 27 months, so more than half the returning women were noncompliant with program recommendations17.
Compliance with mammography screening recommendations can be affected by a number of factors, and achieving compliant attendance in programs that screen annually may be even more difficult. In a Canadian screening trial, half the participants preferred screening every 2-3 years over annual screening, but despite this preference many women can comply with annual screening regimens or at least return for future screening12. Still, in the British Columbia screening program, of the women who returned within 15 months, only 41% returned in the recommended annual interval29, and in another U.S. program that provided women with annual reminders, a substantial number of women waited up to 2 years to have a repeat mammogram28.
Previous studies of regular adherence to mammographic screening have been limited. Some, particularly those from the United States, have relied on self-reported information8-9,26,28,31-34. This method is likely to overestimate mammography use because of social desirability biases and to underestimate the time that has elapsed since previous mammography as a result of telescoping biases. Others studies are unable to distinguish the extent to which participation in subsequent rounds is due to reattenders or new recruits and thus have not distinguished determinants of participation from determinants of reattendance5,10,13. However, the most prominent factor limiting comparisons among both programs and prior studies is the use of varying definitions of reattendance and compliance.Disentangling the separate effects of reattendance, compliance with recommended intervals, and long-term compliance has been hampered by a lack of quantitative data19, but efforts have been made to assess these various factors independently19,30,35. Some studies have looked at repeat mammography but provided limited or no information about the timing of such return visits or reattendance patterns outside of the chosen time interval, and therefore did not consider that women may return within an interval that will still offer some advantages of early detection7,8,25,26,28. Sometimes reattendance and compliance issues are not considered separately. For example, the proportion of eligible women receiving a screen in the previous 3 years ("coverage") is a performance indicator in breast screening programs in the United Kingdom19 and can be adversely affected if women do not attend for initial or repeat screening or if they do not do so within the recommended interval.
Finally, a number of factors come into play that challenge or aid programs in maintaining participation for subsequent screening.
Age, demographic variables, facility characteristics, provider factors, health history, prior mammography, psychosocial factors and recruitment factors are all associated with reattendance or compliance.
Participation, reattendance, and compliance with mammography have been reported to occur less frequently in both younger29,36,37 and older women3,5,10,14,18,22. Consistent with these results is the finding that repeat screening is highest among women aged 55-64 as compared with levels of screening among both younger and older groups9,25 . However, the findings are inconsistent: some have found that younger women are more likely to participate in a full series of four annual mammograms11, adhere to screening guidelines8,13, drop out of screening trials after just one or two screens37, and obtain annual mammograms33. Others have reported that age is unrelated to having repeat mammograms17,26,38.
Various studies8,11,26,27,32,33,37,39,40 have shown that women with higher socioeconomic status are more likely to have multiple mammograms, to return for repeat mammography, and to adhere to screening guidelines. However, education seems to be the most consistent factor, as negative findings have been demonstrated for several other factors such as employment status and home ownership11,17. Being married has been shown to be both unrelated to rescreening11 and related to compliance with annual mammography and to long-term repeated screening26,37,39. Various ethnic and cultural factors have been examined9,11,40,41, and findings have been inconsistent, though foreign-born women were less likely to participate in rescreens11,41.
Several facility-related factors have been examined, and accessibility of the screening clinic has been prominently associated with reattendance and compliance with rescreening recommendations11,12,17,29. One study found that hospital sites were preferable to clinics25. Staff at screening facilities also appear to play a role in promoting reattendance: compared with reattenders, non-reattenders have reported finding clinic staff less courteous, less welcoming, unhelpful, harder to question, or unsupportive with problems arising from the test and, with regard to technologists, less competent12,20,21. When reminder systems are in place, women are more likely to adhere to screening guidelines8, but the capacity of the centre also plays a role. Overwhelmed centres are unable to screen women within the time recommended by guidelines without increased resources19. If women must wait a long time between their physician's recommendation and the mammography screening appointment they may be less likely to get rescreened7,12.
A woman's usual physician plays a major role in whether women reattend and comply with mammography intervals. Physician referral for a mammogram is a strong promotor of screening. Increased referrals for mammography result in increased screening mammography and are strongly associated with women having had repeat mammograms7,27,32. Women with a regular physician and women who had visited a physician in the year before recruitment have been shown to be more likely to comply with repeat mammography screening11,42. Having a physician who criticizes or does not encourage screening is a barrier to reattendance and compliance12,29. The type of practitioner may also have an impact. One study found that routinely visiting a gynecologist was positively associated with having multiple screens34. Women were more likely to adhere to screening guidelines if they reported participating with their doctor in the decision to be screened8.
A woman's health status can also affect her attendance and compliance with screening. Those who fail to reattend have frequently cited acute illness as the reason20, and women who did return for repeat screening had better self-reported health11. A family history of breast cancer is a commonly reported factor associated with increased likelihood of reattending21,27 and long-term compliance with a program35, although some evidence shows that this has no impact11,17.
Women who have had previous mammography, either screening or diagnostic, are more likely to reattend and comply with recommended screening intervals15,17,6,35. Reporting breast problems (e.g. lumps) did not affect reattendance at a second round of screening in one study17, but women were less likely to reattend in another40. In others studies, reporting of breast problems was associated with adhering to screening guidelines8,9. Regular performance of clinical breast examination has a positive association with mammography adherence9,33,35.
Despite indications that women suffer long-term morbidity, increased anxiety about breast cancer43, and recent unnecessary biopsy12, most studies show that women are either equally likely16,17,20,21,26,43-45 or more likely25,44,46 to return or intend to return if they experienced prior false-positive mammography results. Few contrary findings have been published. One study found that women who returned annually for screening were more likely to have had a normal initial study than were late compliers or noncompliers47. Another found that a false-positive screening result was associated with nonattendance at the next round in six screening rounds5. In both cases, it is uncertain whether this was the result of a negative attitude toward screening or toward continued clinical follow-up5. However, in a British study, 15% of women who had had an initial false-positive result did not attend for subsequent mammography, as compared with 8% of women whose first mammogram was negative48.
Although previous attenders appear to reattend more frequently, previous experience with mammography may result in nonattendance. Some disincentives to return have included radiation concerns12,29 and negative views of initial screening, for example, that it was uncomfortable, painful, stressful, embarrassing, distressing, worse than expected, or not reassuring and that attendance was not worthwhile12,20,21,49.
Whether women's concern over their breast cancer risk influences reattendance and compliance is uncertain: it has been shown to be associated with both a higher11 and a lower likelihood of reattending26. Some studies have found that women who perceive a higher susceptibility to breast cancer or are knowledgeable about lifetime risk are more likely to reattend27,32,34. Others report that perceived breast cancer risk has no effect on reattendance20. Women who perceive greater benefits of mammography have a higher frequency of mammography and shorter time interval since the last mammogram50. Guideline adherence is associated with a belief that breast cancer is curable31, and reattenders are more likely to believe that mammography is efficacious in detecting and curing breast cancer20,21. Women who have had multiple screens are more likely to express a willingness to pay $75-$100 for a mammogram, possibly indicating their view of its worth. On the other hand, women who express more anxiety about mammography or associate physical examinations with worry are less likely to obtain repeat mammography11,27.
Women who are preventively oriented may be more likely to reattend and comply with recommended screening intervals17,50. Other positive practices, such as participation in cervical screening8, regular breast self-examination12,29, and being a nonsmoker32, have been associated with screening guideline adherence and repeat screening, although these findings have been contradicted elsewhere17.
Social support may influence a woman's decision to return12. However, some studies have reported that the influence of a woman's friends, partner, children, co-workers, and physician did not affect second round attendance17, contrary to much of the literature on the role of the physician.
Women who do not reattend may be less aware of screening guidelines. Knowledge of the screening guideline recommendations has been found to be associated with adherence to screening within the recommended interval31. Some studies have shown that women who failed to reattend did not believe in or were unaware of the need for further screening20,21,29. In some cases this view was supported by their physician29.
Ease of recruitment plays a major role in women's reattendance and compliance with recommended rescreening intervals, as indicated by the literature on the "reluctant participant". Women who require repeated recruitment efforts are less likely to reattend or return for a series of screens than women who require minimal effort11,17,18,35,51. Despite a reduced tendency to reattend, recruitment of reluctant participants has been demonstrated to be worthwhile in elevating participation levels and improving prognosis in detected breast cancers11.
Even if women are invited in a timely fashion, compliance with recommended rescreen intervals may be adversely affected if there is delay in making an appointment or a change in the appointment time19. Women have cited lack of time and inconvenient appointment times as reasons for not reattending12,20.
For 20 years of their lives women will have access to regular screening by mammography. Interventions aimed at maintaining this habit have an important role in the fight against breast cancer. Relatively simple interventions that can be maintained over the years should be the objective.
The advantages of invitations as a recruitment approach have been previously discussed. Recall letters, whether signed by the physician or the screening program, significantly increase participation in mammography as compared with no letter52,53. Invitation by telephone can also be a useful strategy54.
Use of tailored letters containing information about previous screening history is not effective, although such letters may be more helpful than a standard letter in improving reattendance of women with prior false-positive findings16. A tailored leaflet enclosed with every invitation and directed at women who had previously undergone mammography did not enhance reattendance55.
A telephone follow-up can be considered for women who do not respond to the letter of invitation for rescreening. Use of the telephone carries the advantage that the reasons why women are not returning can be discussed and barriers can be addressed. Relative costing needs to be examined more formally.
A further concern regarding rescreening after the first screen is the tendency to increase the screening intervals. By scheduling an appointment one might minimize the chances of delays past 2 years. Other alternatives might be to schedule the next appointment for 2 years' time at the initial mammogram. A reminder card can be issued. The program can also advise women that when their rescreen is due, they will be sent an appointment letter with a time that could be changed if they so choose. An invitational letter with a scheduled appointment could then be sent out 1 to 2 months beforehand. Programs may want to consider trials of such alternatives.
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