Adherence to Cancer Screening
Barbara K. Rimer, DPH
Cancer Prevention, Detection
and Control Research at Duke University, Durham, NC
Routine breast cancer screening
for women 50 years of age and older can reduce mortality from breast cancer
by 30% to 35%. Regular Papanicolaou tests can decrease mortality from cervical
cancer dramatically, and skin cancer screening could decrease deaths from melanoma.
Adherence to recommended screening procedures for breast, cervical, and skin
cancer screening increases the potential to lower the risk of death and disability
from these diseases. The National Cancer Institute's goals include increasing
the proportion of women who get regular mammograms to 80%, and similar goals
have been issued for Pap tests. Yet, most women still are not being screened
for breast or cervical cancer on a regular basis, and most people do not have
regular skin checks for cancer.
Introduction
Adherence in the context
of cancer control means that recommended screening procedures are followed.
Screening techniques for reducing mortality from breast, cervical, and skin
cancers are proven, available, and cost effective. Yet, for reasons attributable
to providers, the health care system, and the people themselves, screening falls
short of the ideal. Nonadherence reduces the potential of screening to lower
the risk of death and disability from these diseases. Clinicians play important
roles in encouraging patients to undergo screening for breast, cervical, and
skin cancers through effective use of their office systems, by counseling individual
patients, and by responding to patient barriers. Larger-scale scientific efforts
are required to overcome other barriers. These barriers and the solutions to
overcoming them are similar for other screening efforts, including colorectal
cancer screening.[1]
Recommendations for Breast
Cancer Screening
Establishing an appropriate
age guideline for screening women for breast cancer is controversial (Table
1). The National Cancer Institute (NCI), American College of Physicians, American
College of Family Medicine, and the United States Preventive Services Task Force
recommend mammograms every one to two years for women aged 50 through 69 years.
The American Cancer Society, American College of Radiology, and American College
of Obstetrics and Gynecology recommend mammograms every one to two years for
women aged 40 through 69 years. Since mammography has not been shown in randomized
clinical trials to unequivocally reduce mortality for women aged 40 through
49 years, the NCI in 1993 withdrew its recommendation for regular mammograms
for this age group and instead issued a statement of evidence,[2,3] which has
been met with considerable debate. A recent meta-analysis indicates a statistically
significant reduction of mortality in the under-50 age group, but the data are
as yet unverified.[4] Although too little is known about the efficacy of mammography
for women aged 70 years and older, in view of the increased risk of breast cancer
with advancing age, prudence dictates regular mammograms for older women who
are otherwise healthy.[5]
Table 1. Current Screening
Mammography Recommendations ______________________________________________________________________________
| Organization |
Every 1-2 Years
Ages 40-49 |
Every Year or 1-2 Years
Ages 50-69 |
| National Cancer Institute |
|
X |
|
American College of Physicians |
|
X |
|
US Preventive Services Task Force |
|
X |
|
American College of Family Medicine |
|
X |
|
American Cancer Society |
X |
X |
|
American College of Radiology |
X |
X |
|
American College of Obstetrics
and Gynecology |
X |
X |
|
_____________________________________________________________________________
The most rigorous efforts
to encourage women to obtain mammograms should occur among women 50 through
69 years of age. While routine mammograms are not universally recommended for
women aged 40 through 49 years, some women in this age group may require mammograms,
eg, those with a strong family history of breast cancer, women with a personal
history of breast cancer or atypical hyperplasia, and women who are extremely
anxious about breast cancer (although screening for these women is questionable).
Physicians should encourage women to make informed decisions. Many women aged
40 through 49 years receive regular mammograms. Women also should practice breast
self-examination monthly and obtain a yearly clinical breast examination from
a health provider.
Recommendations for Cervical
Cancer Screening
Controversial issues remain
for cervical cancer screening. The NCI and many other organizations recommend
screening every three years when a history of negative tests has been established.[6]
Papanicolaou (Pap) tests decrease mortality rate of cervical cancer among women
aged 20 through 79 years, but many clinicians discontinue such testing when
the patient reaches 65 years of age.[7,8] Physicians should verify that an older
woman has had a history of negative examinations, since many elderly women are
dying of cervical cancer.[9]
Approaches to Promoting
Screening Adherence
Several theoretical approaches
have been developed to explain why individuals do or do not undergo screening.
A widely used theoretical model, the Health Belief Model,[10] postulates that
before undergoing screening, a patient must believe that the problem is serious,
that he or she is susceptible to the problem, that an effective action is available,
and that he or she must receive some sort of a cue to action. The Health Belief
Model has limited application for screening adherence in that it explains only
a small amount of the variance in health behavior.
The Transtheoretical Model
depicts the behavioral changes in cervical cancer screening as a circular process.
The Transtheoretical Model
is now becoming the dominant theoretical approach in cancer screening as it
has in smoking cessation.[11] This model has been extended to breast cancer
screening by Rakowski et al[12] and most recently to cervical cancer screening[13]
and posits that behavior change is a circular process (Figure). As an example,
women who are not even considering mammograms are labelled precontemplators,
while those who are considering a mammogram but have not yet taken action are
labelled contemplators. Women who have had one mammogram are defined as in the
action stage, and the small proportion of women who are receiving regular mammograms
are in the maintenance stage (Table 2). Some women who have received mammograms
in the past have relapsed, ie, they are not planning future mammograms. A similar
approach can be taken for skin cancer screening and screening for cervical cancer.
Table 2. Stages of the
Transtheoretical Model Approach in Cancer Screening ____________________________________________________________________
| Stage |
Definition |
| Precontemplation |
Not considering mammograms |
| Contemplation |
Considering mammograms but no action taken yet |
| Action |
Had had at least one mammogram |
| Maintenance |
Receives regular mammograms |
___________________________________________________________________
The Transtheoretical Model
is effective in planning interventions to increase mammography use on a macro
level and in counseling patients on mammography, Pap tests, skin cancer screening,
or smoking cessation. People in different stages have different barriers to
and beliefs about mammography, and they require different information and education.
For example, precontemplators need to be convinced that mammograms are necessary,
while women in the action stage may need a referral, and those in the maintenance
phase may require only reinforcements and reminders. Appropriately placing a
patient within the cycle enables effective use of the clinician's time and efforts
by matching the message to the woman's needs.
Current Status of Mammography
in the United States
In 1995, more than 182,000
women will be diagnosed with breast cancer and 46,240 women will die of the
disease.[14] The proportion of American women who are receiving regular mammograms
has increased dramatically since 1987, when only approximately one third of
women had ever had a mammogram and only approximately 17% had one in the preceding
year.[15] By 1990, nearly two thirds of women aged 40 years and older reported
having had at least one mammogram, although only approximately 31% were following
guidelines.[16] The NCI's goals include increasing the proportion of women who
get regular mammograms to 80%.[17]
The 1990 National Health
Interview Survey (NHIS) showed that 63% of women over 40 years of age reported
having had a mammogram and that use had almost doubled since 1987. Only 39.8%
of women reported having had both a clinical breast examination and a mammogram
in the preceding year, and 38% of women had never had a mammogram.[18] Rakowski
et al[12] concluded that only 29% of women are getting regular mammograms, according
to data from the 1990 NHIS. Thus, while significant increases in screening use
have occurred, the majority of women are not on a program of regular mammograms
and Pap testing.
In 1987, the NHIS showed
that most underusers were less educated, resided outside of metropolitan areas,
or were members of a minority. By 1990, the racial gap had been reduced on a
national level, although it was still significant in many regions of the US.
Currently, the most relevant demographic factors for predicting mammography
use are lower income status and less education,[18] which transcend the impact
of race alone.
Barriers and Facilitators
to Mammography
The characteristics of women
who do not get regular mammograms are generally consistent from study to study
(Table 3) and are similar to those for Pap tests.[19] The most important barrier
is the lack of a recommendation by a woman's physician.[20-23] Women who are
older, black, or Hispanic are less likely than middle-aged white women to report
receiving such a recommendation. Other factors contributing to women's nonparticipation
in mammography, according to their self-report, are an absence of breast problems
or the belief that mammograms are unnecessary in the absence of symptoms.
Table 3. Characteristics
of Underusers for Breast and Cervical Screening ______________________________________________________________________________
| Has no regular source of care |
|
Smokes |
|
Does not exercise regularly |
|
Is not familiar with breast self-examination |
|
Does not live in a standard metropolitan statistical area |
|
Is a member of a minority |
|
Has a low income level |
|
Is older |
|
Has less than a high school education |
|
__________________________________________________________________________
Other barriers to mammography
exist, but they account for much less of the variance in explaining the behavior.
These barriers, which may be important for individual women or subgroups of
women, include anxiety about the possibility of finding a problem and concern
about radiation and pain. These concerns may be important for individual women
or subgroups of women. For example, black and Hispanic women seem to be more
concerned about pain and report more anxiety about the mammography experience.
There is some evidence that older black women are more fatalistic about cancer
in general,[24] and unmarried women are less likely to have had mammograms.[25]
Smokers also are less likely to get mammograms,[26-27] but this behavior may
correlate with lower standards of health care in general.
Access and environmental
barriers also may be important factors in mammography use. A study conducted
in a health maintenance organization (HMO)[27] found that nonparticipants had
more difficulty getting to the facility, would have to travel farther, and were
more likely to rate the facility as inconvenient. Women without health insurance
are less likely to participate in mammography or Pap testing.[18] Although not
a major barrier, cost has been reported as a barrier for some, eg, women aged
50 to 59 years of age or Hispanic women.[21] However, studies show that even
when the cost barrier is removed, other important psychological barriers remain.20
If these barriers are not addressed, women still may not pursue regular mammograms.
In some ways, the facilitators
to mammography are the obverse of the barriers. Women are more likely to get
mammograms when advised by their physicians,[15,20] when they know the recommended
screening interval for their age, and when they are aware of the relationship
between age and breast cancer screening.[28,29] There also is evidence that
women with more social ties are more likely to have mammograms.[30]
The role of family history
has been inconsistent as a predictor of screening. Some studies show that a
family history of breast cancer increases the likelihood that women will get
regular mammograms, while others do not.[31,32] In a review of the data, Lerman
et al[33] showed that different studies found that different relationships between
family risk and screening behavior produced different effects, ranging from
a negative effect, no effect, or a positive effect. However, many of the studies
have used self-selected groups of women who volunteered to participate in high-risk
programs. Perceptions of personal risk and levels of distress may mediate actual
risk in determining screening behavior. When Curry et al[34] reinforced family
history as a risk factor, women were more likely to participate in a screening
program. Most recently, Schildkraut et al[35] found that the majority of women
in a high-risk sample did not understand the implications of the relative's
age at onset as a risk factor and as a rationale for meticulous surveillance.
Barriers for physicians
and facilitators are different from those reported by women. Physicians are
more likely to be deterred by cost considerations or to believe that women will
reject a referral.[36] Physicians also cite the daily demands of providing acute
and chronic care, failure to remember to recommend prevention and early detection,
and concern about equivocal radiology reports.[36-40] As was previously stated,
cost is not the major barrier for women, and most women get mammograms when
recommended by their physicians. This is especially important for older minority
women.
Current Status of Cervical
Cancer Screening in the United States
In 1995, cervical cancer
will be diagnosed in 15,800 women, and 4,800 will die of the disease.[14] Compared
to breast cancer screening, less is known about the use of cervical screening
among US women. According to the 1987 NHIS, the percentages of women who reported
never having had a Pap test were approximately 11% of women overall, 10% of
white women, 11.9% of black women, and 24.7% of Hispanic women. The proportion
of women who reported having had a Pap test declined as age increased.[41] Black
women aged 30 through 49 years were more likely to be screened regularly, but
white women aged 70 years and older were more likely to have had a Pap test
in the last three years. This shows that Pap test use is negatively related
to age and positively associated with income.[42]
Barriers and Facilitators
to Cervical Cancer Screening
Many of the barriers and
facilitators to Pap testing are similar to those for breast cancer screening.
Older women and women past childbearing age may not recognize that Pap tests
are still necessary,[43] and some women and physicians believe that women who
are not sexually active do not need Pap tests.[44]
Knowledge and beliefs vary
by age and ethnicity. For example, Hispanic women are less likely to be aware
of Pap tests and therefore may require educational information. Most studies
show a relationship between a belief in the benefits of Pap tests and regular
screenings.[45]
Women who are embarrassed
about getting a Pap test and those who say they are too busy also are less likely
to be screened.[46] Women who do not participate in screening are more likely
to cite procrastination or a belief that the test is unnecessary as reasons
for not being screened.[47] As with mammography, women who do not pursue other
preventive services are less likely to participate in Pap testing.[45,48] Minority
women seem to be more embarrassed than white women about getting Pap tests.[25]
Older Hispanic women are
especially at risk for underusing both mammography and Pap testing. Some studies
show that women who are more knowledgeable about Pap tests, including the recommended
screening interval, are more likely to be tested.[49]
Current Status of Skin
Cancer Screening in the United States
Skin cancer is increasing
dramatically in the United States. Cases of melanoma have increased by 120%
for men and by 48% for women since 1958.[50] In 1995, approximately 800,000
new cases of skin cancers will be diagnosed in the United States, and most of
the 9300 deaths will be the result of melanoma.[14] Since screening for skin
cancer requires no special technology and is quick, painless, and inexpensive,
it should be acceptable to most patients and clinicians. The American Cancer
Society advises that adults 20 through 40 years of age have a skin examination
every three years and annually after 40 years of age. Because the skin is accessible,
patients also should be trained to observe their own skin and to be aware of
changes.
Koh et al[51] and others
have suggested that skin cancer screening should focus on high-risk individuals,
eg, those who are white or those with fair skin, with dysplastic nevi, with
a propensity for sunburns, or with a family history. Since the risk of skin
cancer increases with age, older people require special attention.
Barriers and Facilitators
to Skin Cancer Screening
Little is known about the
extent to which breast and cervical cancer screening barriers apply to skin
cancer screening (eg, patient embarrassment and lack of provider time).
Follow-Up of Abnormal Test
Results
It is beyond the scope of
this report to address the issues associated with adherence to follow-up procedures
when test results are abnormal. However, extensive evidence exists that a significant
proportion of people who are screened for breast, cervical, or skin cancer do
not receive appropriate evaluation.[7,52] The ideal intervention strategy varies
according to the population. For example, Marcus et al[53] demonstrated that
transportation incentives for low-income women were highly effective in increasing
adherence to follow-up when a Pap test was abnormal. However, personalized approaches
and a slide-tape program were more effective among other women. A reminder in
the form of a letter or telephone call should be the first step. However, some
people will require more intensive methods of follow-up. Lerman et al[54] and
others have shown that the psychological consequences of abnormal test results
can be profound. Adequate support should be provided to such patients.
Interventions to Increase
Screening Adherence
Beast Cancer and Cervical
Cancer More studies have been conducted to test interventions to increase
screening for breast cancer than with other cancers. The literature shows that
the best approach to screening is to use multiple interventions directed at
patients, physicians, the system and, if possible, the community. Multistrategy
interventions generally are more effective, although single approaches have
been successful in some cases.[19] For example, a nurse practitioner in a hospital
clinic was given the responsibility for identifying older, poor, black women
who were due for mammograms and then approaching them.[7 ]This intervention
resulted in a significant increase in the proportion of these women who received
mammograms. In another case, a video was created that highlighted a woman's
internal attributions about her personal responsibility for getting mammograms,[55]
which increased use of mammography, according to self-reports.
Strategies that physicians
can use to increase their mammography referrals and their performance of Pap
tests include using audits with periodic feedback, detailing strategies, and
implementing computerized reminders. These strategies have not been used widely
outside of academic medical centers. Costanza et al[31] recently showed that
a hospital-based, in-service program significantly improved mammography referrals
in their intervention community.
The most effective behavior
change investigations used a mix of intervention strategies directed at physicians,
patients and, in some cases, the community.[31,56-58] The physician-directed
strategies included traditional continuing medical education programs at community
hospitals, as well as office-based strategies based on the academic detailing
model.[59] Most used reminder systems as integral to the interventions. Austin
et al[60] recently demonstrated the cost-effectiveness of such reminders. All
of these successful studies also developed and tested special interventions
for women.
In one study, women in an
independent practice association model HMO were invited to participate in breast
cancer screening.[56] Nonadherent women were sent reminders, which significantly
increased adherence. For women who remained nonadherent, telephone counseling
tripled the chances that a woman would get a mammogram. During a brief counseling
session that averaged five minutes, the counselor's goal was to identify and
overcome a woman's personal barriers to mammography.
Costanza et al[31] conducted
patient education in a community health center, and Fletcher et al[58] implemented
a community-wide media campaign. Lane et al[57] used community health education
strategies, including a game.[23] These studies also included free or low-cost
mammograms as part of the intervention package. Thus, these programs included
strategies that were patient-directed, physician-directed, system-directed,
and sometimes community-based.
Although less research has
been applied to cervical cancer screening compared with breast cancer screening,
many of the same approaches appear to be effective. Community health workers
can increase use of cervical cancer screening, and in- reach interventions within
community health centers can be effective.[61,62] In addition, attempts to streamline
the process of appointments and waiting time contribute to improved adherence,[63]
and invitations from providers also increase cervical cancer screening.[64]
There is some evidence that screening of emergency hospital patients can be
a useful component of case finding.[65,66] The literature shows that usually
more than one intervention strategy is required and that those interventions
should be directed not only at patients, but also at physicians, other providers,
and the health care system.
Skin Cancer Screening
The United States lags behind
many other countries in the creative application of interventions to reduce
the incidence of and mortality from melanoma and other skin cancers. Australia,
which has the highest reported incidence of melanoma, has mounted successful
population-based programs that have produced dramatic results.[67,68] Because
early sun exposure is a predictor of skin cancer and particularly melanoma,
education of children and interventions with their parents are necessary components
of programs, whereas interventions for breast and cervical cancer screening
focus on adult behaviors.
Because prevention strategies
are available (eg, using sunscreens, limiting sun exposure), prevention must
be a major feature of education programs. Many intervention strategies have
been used to decrease sun exposure.[69] In general, the literature shows that
combinations of interventions, including mass-media and community-based education,
can increase the number of people who practice safe-sun behaviors. However,
fewer concerted efforts have occurred in promoting skin cancer screening. Skin
cancer screening is not technology-driven, thus checks can be performed almost
anywhere. Programs have been conducted in mobile settings and at churches, health
fairs, and county fairs.[51] The American Academy of Dermatology sponsors an
annual free skin cancer screening day. As with similar breast and cervical cancer
screening events, individuals with low income are under-represented.
Skin cancer screening should
be integrated into routine primary care, since over 90% of the US population
has a routine source of medical care and 85% consult a physician every two years.
Thus, use of the same prompting systems that increase breast and cervical cancer
screening also can increase skin cancer screening.
The Clinician's Role in
Promoting Cancer Screening
Although breast cancer screening
lags behind Pap testing, they can be considered as integrated behaviors, since
some women do not participate in either test. In addition, the Pap test is often
the gateway to preventive medicine for women. A Pap test, as well as breast
and skin examinations, can be incorporated into a routine checkup and can be
performed in the context of women's health. A referral for a mammogram also
can be given at the same visit. The clinician can increase the use of breast
and cervical cancer screening by including the following recommendations in
clinical practice (Table 4).
Table 4. Clinical Approaches
to Improve Adherence _____________________________________________________________________________
| Use an office system. |
|
Maintain a detailed family history. |
|
Counsel patients about the importance of screening. |
|
Use age- and ethnicity-appropriate patient education materials. |
|
Take a stage-based approach. |
|
Get feedback from patients. |
|
Have a system in place for follow-up. |
|
Track effectiveness. |
|
Consider adjuncts to increase counseling. |
|
Participate in low-cost, community-based screening activities. |
|
______________________________________________________________________________
Use an office system.
-- System-wide innovations, such as prompts and manual- or computer-generated
reminders, can increase the use of breast and cervical cancer screening and
are cost effective.[60,70- 73] Such systems also could increase the acceptance
of skin cancer screening. Fewer than one third of physicians report using office
systems, but without planned systems, recommendations for cancer screening often
are sporadic and inconsistent. Ideally, yearly reminders for Pap testing and
breast cancer screening should be sent, and most women welcome these reminders.
Skin cancer screening can be integrated into annual checkups for both men and
women.
Maintain a detailed family
history -- Genetic information will become increasingly available to characterize
the 5% of patients who are at increased risk for cancer due to family history.
A detailed family history should be maintained for all patients, and the impact
of risk on recommendations for surveillance should be discussed with patients
in order to determine if they should be offered genetic screening and counseling
and if they should be on more aggressive screening schedules.
Counsel patients about
the importance of screening -- The most important reason why women receive
screening is that their health care providers have recommended they do so. Patients
rarely refuse breast and cervical screening when recommended by physicians.[74]
Brief, articulate advice regarding the importance of screening can be effective
in increasing the use of mammography and Pap testing. This recommendation should
be accompanied by a referral, which facilitates the behavior, or the receptionist
or office nurse can schedule the mammogram appointment while the woman is in
the office. Similarly, women should be given a strong message about the importance
of regular Pap testing. Ideally, the test could be performed during a routine
visit, or a follow-up visit could be scheduled.[75] During a routine checkup,
a physician should not only perform a skin examination, but also emphasize the
importance of regular, thorough breast and skin self-examinations.
Counseling should reflect
a recognition of the patient's personal health behaviors that may affect risk.
For example, current or previous smoking, sexual history, and oral contraceptive
use affect the risk of cervical cancer, and these factors should be considered
when counseling patients.
Use age- and ethnicity-appropriate
patient education materials -- The impact of counseling can be enhanced
when augmented with education materials that are appropriate to the patient's
age and ethnicity. Excellent materials are available at no cost from the American
Cancer Society (1-800- ACS-2345) and the NCI's Cancer Information Service (1-800-4-CANCER).
Take a stage-based approach
-- The clinician's advice can be most effective when a stage-based approach
is used.[11] The woman who refuses to consider a mammogram has different educational
needs from one who has regular mammograms. The former may benefit from information
about the relationship between age and breast cancer incidence or the ability
of mammography to detect early, curable cancers, while older precontemplators
may not know that women need to continue regular Pap testing and may benefit
most from recommendations for regular screenings and a referral. Still other
patients may not appreciate the value of sun protection or regular skin examinations.
Thus, the most effective recommendations address each patient's individual circumstance.
Get feedback from patients
-- Women who are referred for mammograms or Pap tests can provide important
information about mammography facilities and other referral services. If they
complain about waiting time for appointments or how they are treated, it may
be time to identify a new facility.
Have a system in place
for follow-up -- Women who are given referrals for mammograms will not always
follow through with their appointments, and even those with abnormal Pap or
mammography test results may not complete the recommended diagnostic tests.
Compliance to recommended skin cancer diagnostic procedures also may be incomplete.
The reminder system or another follow- up system should be used to track adherence
to recommended procedures.
Track effectiveness
-- Many clinicians believe they are doing better than they actually are. Chart
audits and other procedures can be used to obtain this information on a regular
basis. Areas of below-par performance then can be identified and appropriate
strategies can be devised for improvement.
Consider adjuncts to
improve counseling -- Reminder letters are one of the cost-effective techniques
that can double the proportion of women who receive cancer screening.[76] Telephone
counseling, in which a trained counselor calls a woman to identify and overcome
her individual barriers to mammography, can triple the odds that a woman will
have a mammogram.[76] Telephone counseling currently costs approximately $5.00
per successful call. Patients also can be referred to the NCI's free telephone
information line, the Cancer Information Service (1-800-4-CANCER).
Participate in low-cost,
community-based screening activities -- Many communities now offer organized
approaches to cancer screening that can reduce financial barriers for many low-income
people. These events also should include referral and follow-up for those with
abnormal findings.
Conclusions
Regular screening for breast
cancer, cervical cancer, and skin cancer can reduce mortality from these cancers.
Physicians can do much to overcome patients' barriers to participation in screening.
Most of these steps require only a modest amount of time but could exert a major
impact on mortality from cancer.
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