Volume 1: No. 1, January 2004
Nonadherence to Breast and
Cervical Cancer Screening: What Are the Linkages to Chronic Disease
Steven S. Coughlin, PhD, Robert J. Uhler, MA, H. Irene Hall, PhD, Peter
A. Briss, MD
Suggested citation for this article: Coughlin
SS, Uhler RJ, Hall HI, Briss PA. Nonadherence to breast and cervical cancer
screening: what are the linkages to chronic disease risk? Prev Chronic
Dis [serial online] 2004 Jan [date cited]. Available from: URL: http://www.cdc.gov/pcd/issues/2004/
Several preventive practices that reduce chronic disease risk have been
associated with breast and cervical cancer screening, including maintenance
of normal weight and avoidance of cigarette smoking. A history of certain
chronic illnesses such as diabetes and cardiovascular disease has also been
related to cancer screening. Nevertheless, studies that have attempted to
identify women who are less likely to have had a recent breast or cervical
cancer screening test have infrequently examined the associations of breast
and cervical cancer screening with multiple health factors that influence
chronic disease risk.
To clarify relationships between cancer screening and health behaviors and
other factors that influence chronic disease risk, we examined the
self-reported breast and cervical cancer screening practices of women in the
United States by using data from the 1999 Behavioral Risk Factor
Surveillance System. The women were described according to their recent use
of mammography and the Papanicolaou test, physician visits within the past
year, health insurance coverage, and preventive practices that reduce
chronic disease risk.
Overall, 74.5% (95% CI, 73.9%-75.1%) of the women in this sample aged 40
years or older (n = 56,528) had received a mammogram within the past 2
years. The percentage of women who had been screened for breast cancer,
however, varied widely by factors associated with reducing the risk of chronic
disease (e.g., cholesterol check in the past 2 years, blood pressure check
in the past 2 years, normal weight, avoidance of cigarette smoking) and
having access to health care (e.g., health insurance coverage, recent
physician visit). Similarly, 84.4% (95% CI, 83.9%-84.9%) of all women aged
18 years or older who had not undergone a hysterectomy (n = 69,113) had
received a Papanicolaou test in the past 3 years, and factors associated
with reduced chronic disease risk and health care access were related to
having had a recent Papanicolaou test.
The results of this study suggest that underscreened women who are at risk
for breast and cervical cancer are likely to benefit from programs that
identify and address coexisting prevention needs. The identification of
coexisting prevention needs might assist in developing interventions that
address multiple risks for chronic disease among women and might
subsequently help improve the efficiency and effectiveness of prevention
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Several preventive practices that reduce chronic disease risk have been
associated with breast and cervical cancer screening in previous studies.
These practices include maintaining a normal weight (1-3), avoiding
cigarette smoking (4-6), and testing for cholesterol level (7).
In addition to preventive practices, a history of certain chronic
illnesses such as diabetes, obesity, and cardiovascular disease has been
associated with cancer screening behaviors (8). For example, recent studies
have found that obese women in the United States are less likely to adhere
to cancer screening recommendations than normal weight women (2,3). In
addition, obesity is associated with increased risks of several chronic
diseases, including coronary heart disease, diabetes, and breast cancer
Studies that have linked a history of chronic illness with cancer
screening behavior (for example, women who are obese or who have had a prior
cardiovascular event are less likely to have had a recent breast or cervical
cancer screening test) frequently have not examined the association of
cancer screening behavior with health-related behaviors that affect the risk
of cardiovascular disease such as cholesterol and blood pressure checks,
level of physical activity, and avoidance of cigarette smoking (7,13). Thus,
researchers and clinicians do not completely understand the relationships
between cancer screening and factors associated with chronic disease risk.
Cardiovascular disease and cancer are the 2 most common causes of death
among women in the United States (14).
Interrelationships between preventive health behaviors are partly due to
individual contact with the medical care system. For example, women are more
likely to have had a recent Papanicolaou (Pap) test if they have seen a
physician in the past year or if a health care provider has recommended that
they undergo the procedure (15,16). Engaging in regular health care has been
shown to be a predictor of cancer screening among women. Additionally,
physician visits for other chronic diseases may be related to an increased
likelihood of cancer screening (8). Among older women who were studied as
part of the Women's Health Initiative, breast and cervical cancer screening
was inversely related to having diabetes and cardiovascular disease (8).
To clarify the relationships between cancer screening and health-related
behaviors and other factors that influence chronic disease risk, we examined
the self-reported breast and cervical cancer screening practices of women in
the United States using data from the 1999 Behavioral Risk Factor
Surveillance System (BRFSS). The preventive practices examined included
screening mammography, Pap test, and other health-related behaviors. We
examined possible correlates of screening among the women, including whether
they had received a cholesterol or blood pressure check in the past 2 years,
had maintained normal weight, were physically active, or avoided cigarette
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The data used in this study were from women who were interviewed as part
of the 1999 BRFSS, a state-based telephone survey of adults aged 18 years or
older (17). We used data from 1999 rather than more recent data because
during that year the survey collected information about additional
preventive health practices.
The BRFSS uses a random-digit-dialing technique and multistage cluster
sampling in each participating state to sample noninstitutionalized adults
who have telephones (18). Trained interviewers administered a
computer-assisted interview. The interviews included questions about general
health status, demographic and socioeconomic characteristics, height and
weight, mammography, use of Pap tests, and other health-related behaviors,
including alcohol use, cigarette smoking, testing for occult blood in the
stool, and cholesterol or blood pressure checks. We asked each adult female
respondent whether she had ever had a mammogram; we then asked those who
responded positively how long it had been since their last mammogram. Next
we asked similar questions about the Pap test. We also asked women whether
they had undergone a hysterectomy.
We limited analyses of mammogram use to women aged 40 years or older (n =
56,528), whereas we limited analyses of Pap test use to women aged 18 years
or older (n = 69,113). Women who reported that they had undergone a
hysterectomy, and therefore did not have an intact uterine cervix, were
excluded from the analyses of Pap test use. Data on physical activity were
only available for respondents in Georgia, Hawaii, Illinois, Michigan,
Nebraska, New Mexico, Ohio, Oklahoma, Tennessee, Utah, and Virginia (n =
10,381 for analyses of mammography and n = 12,600 for analyses of Pap test
use in relation to physical activity).
Physical activity levels were categorized as physically inactive (no
reported activity), irregular activity (any reported physical activity
engaged in for either less than 20 minutes or less than 3 times per week),
regular activity (any physical activity engaged in for 20 or more minutes
3 or more times per week), and regular and vigorous activity (any
physical activity that likely required rhythmic contraction of large muscle
groups at 50% of functional capacity for 20 or more minutes 3 or more
times per week). Body mass index (BMI) was calculated using weight and
height [weight (kg)/height squared(m)2] (14) and was categorized as
underweight (BMI < 18.5), normal weight (BMI > 18.5 and < 25),
overweight (BMI 25 to 29), and obese (BMI > 30) according to the
International Obesity Task Force classification (19).
We examined the percentage of women who had had a recent mammogram or Pap
test in relation to combinations of selected preventive health behaviors,
based on the framework proposed by Langlie (Figure) (20). Selected preventive health
behaviors included detecting disease or reducing the possibility of future
disease (checking cholesterol level, checking blood pressure, and avoiding
cigarette smoking) and health maintenance behaviors (maintaining normal
weight and engaging in physical activity).
|Behaviors That Serve to Detect Disease or Reduce the Possibility of
Blood pressure check
Avoidance of cigarette smoking
|Health Maintenance Behavior
Maintenance of normal weight
Categories of Health Behaviors Associated With Chronic Disease Risk That
Were Examined in Relation to Mammography and Pap Testing.
Adapted from Langlie JK (20).
Age-adjusted rates of screening test use were estimated using the direct
method and the overall age distribution of U.S. women who responded to the
1999 BRFSS. In examining bivariate associations, levels of statistical
significance were obtained using Cochran-Mantel-Haenszel chi-square tests.
All analyses used SAS and SUDAAN to calculate 95% confidence intervals (CIs)
and to allow for weighting of the estimates (21). The samples were weighted
to compensate for the following 3 factors: 1) unequal sampling probability
resulting from the unique number of telephones per household; 2) number of
unique telephone numbers per primary sampling unit; and 3)
poststratification by age, sex, and race. Using logistic regression
techniques and SUDAAN, we carried out a multivariate analysis of predictors
of screening test use (21, 22). We used the logistic model to obtain point
estimates of the predicted marginals, which were the multivariate-adjusted
screening rates expressed as a percentage (22). Each covariate and
explanatory variable in the model was tested for association with the
response variable using a Wald chi-square test. All pairwise comparisons
were performed using general linear contrasts (22).
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The overall response rates (Council of American Survey Research
Organizations ) for the 1999 BRFSS among households of all races and
ethnicities was 55.2%.
Overall, 86.9% (95% CI, 86.4%-87.4%) of women aged 40 years or older
reported receiving a mammogram at least once, after adjusting for age. In
addition, 74.5% (95% CI, 73.9%-75.1%) of women aged 40 years or older
reported receiving a mammogram within the past 2 years, after adjusting for
age. Not having a mammogram within the past 2 years was associated with not
being currently married, lower education level, lower household income,
being currently unemployed, larger number of children or persons in
household, poorer general health status, not having seen a physician within
the past year, lack of health insurance coverage, lack of use of other
screening tests including recent cholesterol or blood pressure check,
obesity, physical inactivity, and current alcohol or cigarette consumption (Table
1). We found similar results in multivariate analysis, although a
smaller sample of women was used because of missing data. However, the
associations between recent mammography and blood pressure or cholesterol
checks were less pronounced after adjusting for multiple factors associated
Approximately 94.2% (95% CI, 93.9%-94.5%) of all women aged 18 years or
older without a history of hysterectomy reported having received a Pap test
at least once, after adjusting for age. In addition, 84.4% (95% CI, 83.9% to
84.9%) of women aged 18 years or older had received a Pap test within the
past 3 years, after adjusting for age. Not having had a Pap test within the
past 3 years was associated with race/ethnicity, not being currently
married, lower education level, lower household income, number of children
or persons in household, not being currently employed, poorer general
health, not having seen a physician within the past year, lack of health
insurance coverage, lack of use of other screening tests including recent
cholesterol and blood pressure check, obesity, physical inactivity, and
current alcohol or cigarette consumption (Table
2). Similar results were
seen in multivariate analysis (in a somewhat smaller sample of women).
However, the associations between a recent Pap test and a blood pressure
check, a cholesterol check, and weight were less pronounced after adjusting
for multiple factors associated with screening, and the association with
employment status disappeared.
Breast and cervical cancer screening and factors associated with chronic
The percentage of women who had undergone a recent mammogram was examined
in relation to combinations of selected behaviors associated with chronic
disease risk. After adjusting for multiple factors associated with
screening, only 22.5% (95% CI, 12.9%-32.1%) of the women who reported not
having a cholesterol or blood pressure check within the past 2 years and who
were current cigarette smokers had had a recent mammogram (Table
comparison, 81.7% (95% CI, 80.9%-82.4%; P < .001) of the women who
had had recent cholesterol and blood pressure checks and who were
non-smokers had had a recent mammogram (Table 3). Because of missing data,
the sample size available for multivariate analysis was smaller than the
sample size available for age-adjusted results. Differences in the
percentage of women who had had a recent mammogram were less pronounced
across combined categories of weight and physical activity. For example,
after adjusting for multiple factors associated with screening, similar
proportions of women who were obese and physically inactive and women who
had a normal weight and were physically active had had a recent mammogram
[73.7% (95% CI, 69.2%-78.1%) vs. 75.5% (95% CI, 72.6%-78.5%), P =
After adjusting for multiple factors associated with screening, only
54.5% (95% CI, 48.6%-60.5%) of the women who reported not having a
cholesterol or blood pressure check within the past 2 years and who were
current cigarette smokers had had a recent Pap test (Table
comparison, 90.7% (95% CI, 90.1%-91.3%; P < .001) of the women who
had had recent cholesterol and blood pressure checks and who were nonsmokers
had had a recent Pap test (Table 4). Differences in the percentage of women
who had had a recent Pap test were similar or less pronounced across
combined categories of weight and physical activity. For example, after
adjusting for multiple factors associated with screening, 86.5% (95% CI,
83.4%-89.5%) of the women who were obese and physically inactive had had a
recent Pap test (Table 4). Similarly, 86.4% (95% CI, 84.4%-88.4%; P =
.964) of the women who had a normal weight and were physically active had
had a recent Pap test (Table 4).
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The present analysis of relationships between breast and cervical cancer
screening and other factors associated with chronic disease risk was guided
by the framework proposed by Langlie for categorizing preventive health
behaviors (20). Similar frameworks for understanding the relationships between
cancer screening tests and other preventive health behaviors have been
proposed by other authors (24-26). Preventive health behaviors include
behaviors that serve to detect disease (e.g., mammograms), behaviors that
reduce the possibility of future disease (e.g., cholesterol checks,
maintenance of normal weight, avoidance of cigarette smoking), and behaviors
that maintain health (e.g., exercise, diet) (20,24). These categories are not
mutually exclusive. Simpler models or categorizations (e.g., primary and
secondary prevention) have also been used.
Nonadherence to breast and cervical cancer screening was positively
related to chronic disease risk factors, especially cigarette smoking and
not participating in cholesterol and blood pressure checks. Associations
with disease reduction and health maintenance behaviors, such as physical
activity and maintenance of normal weight, were small and much weaker. (Data
on physical activity were only available for respondents in 11 states.)
Current cigarette smokers who had not had a recent cholesterol or blood
pressure check were particularly unlikely to have had a recent mammogram or
Pap test. These findings probably reflect, in part, individual factors —
knowledge and attitudes, lack of contact with physicians, poor access to
routine health care — although differences in cancer screening practices
persisted in multivariate analysis after adjusting for such factors as
recently seeing a physician and having health insurance coverage. The
findings may also be partly explained by errors in self-reported medical
testing. Individuals who under-report one test might be more likely to
under-report other tests; conversely, any increase in reported screening
(due, for example, to social desirability bias) might act across screening
These results agree with those of other studies that have found a
relationship between having Pap tests and having medical checkups, other
cancer screening tests, and cholesterol tests (7,8,24). For example, in a
factor analysis of BRFSS data from Maryland, Liang et al observed a
clustering of Pap tests, clinical breast examinations, and medical checkups
among women of all ages (27). Among women older than 40 years, mammograms and
cholesterol checkups were clustered (27).
In addition to lack of access to health services, possible explanations
for clusters of health factors associated with chronic disease risk include
socioeconomic factors that make a healthy lifestyle difficult to establish
and maintain. Factors such as poverty, unemployment, and lower educational
level have consistently been found to pose barriers to cancer screening (8).
Consistent with other studies, age, higher education level, having health
insurance coverage, and seeing a physician within the past year were
positively associated with cancer screening in the current analysis (8,28).
Healthy lifestyle behaviors and better socioeconomic status were also
related to the likelihood of having had a recent medical checkup (28). In
the current study, however, the associations between nonadherence to breast
and cervical cancer screening and chronic disease risk factors persisted
after adjusting for education level, number of children, number of persons
in household, and other demographic and socioeconomic factors. Controlling
for education, unemployment, and other factors reduced, but did not
eliminate, the associations with cancer screening.
Prior studies have found that obese women are less likely to undergo breast
and cervical cancer screening (1-3,29). Obese women may be more reluctant to
undergo procedures such as pelvic examinations and clinical breast
examinations that involve disrobing or the physical examination of their
bodies (1-3). Obesity may also deter physicians from recommending procedures
such as pelvic examinations because of potential technical difficulties
(30). Although the results of the current study may agree statistically with
results from prior studies (1-3,29) the magnitude of the associations with
obesity are small, especially after physical activity and other factors are
taken into account (< 1 percentage point difference between obese and
normal weight women for Pap test and < 2 percentage point difference
between obese and normal-weight women for mammography).
Limitations of the current study include a low response rate and the fact
that the telephone survey excluded individuals living in households without
a telephone. Individuals without a household telephone may be more likely to
have a lower income, to engage in unhealthy lifestyle practices, or to not
adhere to recommendations for routine breast and cervical cancer screening
(31). As a result, the estimates of breast and cervical cancer screening in
the present study may be biased upwards. Information bias is also a
possibility, because of the use of self-reported information about height,
weight, cancer screening practices, and other factors. Nonetheless, studies
of the reliability of cancer screening information collected as part of
BRFSS have shown that self-reported information about screening mammography
and Pap tests is reliable (32,33). Studies based on self-reporting have
found that overweight participants underestimate their weight and all
participants overestimate their height (34,35). However, self-reported
weight has been found to be highly correlated with measured weight (34,35).
(As previously mentioned, data on physical activity were only available for
respondents in 11 states.)
The results of the current study are important because of the increasing
prevalence of physical inactivity and obesity in the United States, which
increase the risk of cancer and other chronic diseases, and because of the
need to identify women who are rarely screened for breast and cervical
cancer (36-38). Although the majority of women in the United States have
received a mammogram and Pap test, innovative approaches for identifying and
reaching underscreened populations are needed. The observation that women
who have not received a recent mammogram or Pap test may also lack a recent
cholesterol or blood pressure check suggests that underscreened women who
are at risk for breast and cervical cancer are likely to benefit from
programs that identify and address coexisting prevention needs. The
identification of coexisting prevention needs might help to improve the
efficiency and cost-effectiveness of prevention programs. One example of
this approach is the Centers for Disease Control and Prevention's WISEWOMAN
program, which provides low-income, underinsured and uninsured women aged 40
to 64 years with chronic disease risk factor screening, lifestyle
intervention, and referral services to prevent cardiovascular disease (39).
Currently funded projects provide preventive services including blood
pressure and cholesterol testing as well as interventions to help women
increase physical activity and improve nutrition.
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The authors thank Dr. Rosalind Breslow and Dr. Mona Saraiya for their
helpful comments during the planning stages of this manuscript.
Corresponding Author: Steven S. Coughlin, PhD, Epidemiology and Applied
Research Branch, Division of Cancer Prevention and Control, National Center
for Chronic Disease Prevention and Health Promotion, Centers for Disease
Control and Prevention, 4770 Buford Hwy. NE (K-55), Atlanta, GA 30341.
Phone: 770-488-4776. E-mail: firstname.lastname@example.org
Robert J. Uhler, MA, Division of Cancer Prevention and Control, National
Center for Chronic Disease Prevention and Health Promotion, Centers for
Disease Control and Prevention, Atlanta, Ga; H. Irene Hall, PhD, Division of
HIV/AIDS Prevention, Centers for Disease Control and Prevention, Atlanta, Ga
(work performed at Division of Cancer Prevention and Control, National
Center for Chronic Disease Prevention and Health Promotion, Centers for
Disease Control and Prevention, Atlanta, Ga); Peter A. Briss, MD, Division
of Prevention Research and Analytic Methods, Epidemiology Program Office,
Centers for Disease Control and Prevention, Atlanta, Ga.
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