Content uploaded by Melody S Goodman
Author content
All content in this area was uploaded by Melody S Goodman on Nov 24, 2017
Content may be subject to copyright.
Perceived Barriers to Mammography among Underserved
Women in a Breast Health Center Outreach Program
Oluwadamilola M. Fayanju, MD, MPHS1, Susan Kraenzle, BA, RN, CBCN2, Bettina F. Drake,
MPH, PhD1, Masayoshi Oka, MES, DDes1, and Melody S. Goodman, MS, PhD1
1Department of Surgery, Washington University School of Medicine, St. Louis, MO
2Joanne Knight Breast Health Center, The Alvin J. Siteman Cancer Center at Barnes-Jewish
Hospital and Washington University School of Medicine, St. Louis, MO
Abstract
BACKGROUND—To investigate perceived barriers to mammography among underserved
women, we asked participants in the Siteman Cancer Center Mammography Outreach Registry –
developed in 2006 to evaluate mobile mammography's effectiveness among the underserved –
why they believed women did not get mammograms.
METHODS—The responses of approximately 9000 registrants were analyzed using multivariable
logistic regression. We report adjusted odds ratios (OR) and 95% confidence intervals (CI)
significant at two-tailed p<0.05.
RESULTS—Fears of cost (40%), mammogram-related pain (13%), and bad news (13%) were the
most commonly reported barriers. Having insurance was associated with not perceiving cost as a
barrier (OR 0.44, 95%CI 0.40–0.49) but with perceiving fear of both mammogram-related pain
(OR 1.39, 95%CI 1.21–1.60) and receiving bad news (OR 1.38, 95%CI 1.19–1.60) as barriers.
CONCLUSION—Despite free services, underserved women continue to report experiential and
psychological obstacles to mammography, suggesting the need for more targeted education and
outreach in this population.
Keywords
breast cancer; health beliefs; health disparities; mobile mammography; screening
INTRODUCTION
Mirroring national trends, breast cancer is the most commonly diagnosed non-cutaneous
malignancy and the second most common cause of cancer-related mortality among women
© 2014 Excerpta Medica, Inc. All rights reserved
Corresponding Author Oluwadamilola Fayanju, MD, MPHS Campus Box 8109 660 S. Euclid Ave St. Louis, MO 63110 USA
fayanju@wustl.edu| telephone: (314) 747-2691 | fax: (314) 454-7941.
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our
customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of
the resulting proof before it is published in its final citable form. Please note that during the production process errors may be
discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
NIH Public Access
Author Manuscript
Am J Surg. Author manuscript; available in PMC 2015 September 01.
Published in final edited form as:
Am J Surg. 2014 September ; 208(3): 425–434. doi:10.1016/j.amjsurg.2014.03.005.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
in Missouri.1 Since 2000, there has been a significant decline in breast-cancer-specific
mortality throughout the state,1 but this overall improvement masks statewide disparities.
Compared with whites and in contrast to the nation as a whole, African-American women in
Missouri have higher incidence rates of breast cancer than whites (142.5 versus 122.1
breast-cancer diagnoses for every 100,000 women in 2005–2009), and the age-adjusted
breast-cancer mortality rate among African-American women is also higher (24.4 versus
23.1 breast-cancer-specific deaths for every 100,000 women in 2005–2009).2 In addition,
disproportionately high rates of late-stage (locally advanced or metastatic) breast cancer
have been reported among women in North St. Louis, an urban, low-income, and
predominantly African-American community,3–5 while in the rural, southeastern Bootheel
region of Missouri, women have lower mammography utilization rates and higher breast-
cancer mortality rates than women in almost any other part of the state.6
As part of an effort to redress these disparities in the breast-cancer continuum of care,
several outreach efforts to medically underserved communities have been initiated by the
Alvin J. Siteman Cancer Center at Barnes-Jewish Hospital and Washington University
School of Medicine, the only National Cancer Institute (NCI)-designated Comprehensive
Cancer Center in the state of Missouri. Over the past 10 years, Siteman's Mammography
Van has significantly expanded its geographic catchment area throughout the St. Louis
metropolitan area and in the Missouri Bootheel region.7 Furthermore, women found to have
breast abnormalities through van mammograms are now referred directly to Siteman for
follow-up, regardless of insurance coverage, rather than being referred back to their primary
care physicians.7 Finally, Siteman has worked with two organizations in order to fund
mammograms for low-income and under/uninsured women: Show Me Healthy Women
(SMHW), a program providing free breast- and cervical-cancer screening for Missouri
residents over the age of 35,8 and the St. Louis Affiliate of Susan G. Komen for the Cure,
which has funded the Breast Health Care for At-Risk Communities (BHCAC) program at
Siteman for 15 years.9
To assess and enhance the effectiveness of Siteman's mammography services among the
medically underserved, Siteman's Mammography Outreach Registry was established in
2006. Any woman who received a free or reduced-cost mammogram at Siteman's Joanne
Knight Breast Health Center (BHC) or on the mammography van was included in the
registry. Because many of the Outreach Registry participants reside in zip codes where
screening participation has historically been low, we wanted to explore registrants' health
beliefs regarding mammography, with the hope that their beliefs might shed light on factors
associated with screening nonparticipation in their communities. In formulating our
questions, we utilized the Health Belief Model for assessing health behavior.
The Health Belief Model (HBM, Figure 1), first developed by social psychologists in the
United States (US) Public Health Service in the 1950s, is a theory of health behavior widely
used not only to examine why people do or do not take action to prevent, screen for, or treat
disease but also to guide the development of interventions aimed at improving healthcare
participation.10 Over the past 30 years, the HBM has been advanced by Victoria Champion,
Celette Skinner, and others as a means through which to improve rates of breast-cancer
screening amongst the underserved.11 Indeed, in large part because of community-based
Fayanju et al. Page 2
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
interventions informed by the HBM, racial disparities in mammography utilization in the US
have essentially been eliminated.12 However, as already discussed, geographic pockets of
disparity remain both in the state of Missouri and throughout the nation.
Previous studies have demonstrated that within the HBM (Figure 1), perceived barriers
represent the set of health beliefs most likely to predict health behavior.11 Thus, in order to
efficiently evaluate the efficacy of our mobile mammography program and assess the
potential for increased screening participation in the communities served by the
mammography van, we asked registrants to share with us their impressions of why women
in general might be more or less likely to undergo a screening mammogram: that is, what
psychological, logistical, and/or experiential factors did they believe women were likely to
perceive as barriers to getting screened? Here, we report the results of our prospective cohort
study, which represents the largest review ever conducted of a mobile mammography
population.
METHODS
Population studied
Beginning in 2006, women who received screening mammograms funded by SMHW or
Komen's BHCAC programs were registered in the Siteman Mammography Outreach
Registry during their first screening visit at either the Siteman Mammography Van or at the
BHC. Participation in the registry was not required for receipt of services, but the vast
majority of women – approximately 99% – who presented for mammograms agreed to
participate.
Data collection
At registration, each participant completed a 6-item questionnaire about their experiences
with mammography in general and as part of the Siteman Mammography Outreach Registry
in particular. The questionnaire was written at a sixth-grade reading level and was designed
by the nurse manager of the BHC and a public-health trained breast radiologist. In
accordance with Siteman's institutional policy guaranteeing interpreter services to all who
need them, the questionnaire was interpreted on an ad hoc basis for all women with limited
English proficiency. The first item of the questionnaire – “What is the reason women don't
get a mammogram?” – was included for the purpose of assessing perceived barriers to
mammography, and respondents were encouraged to select one response from a set of 11
standardized responses (Table 1) to this query.
Registrants also agreed to provide access to their medical record information and to share
demographic information. Women who had been previously screened through a Siteman
provider, whose mammograms were provided during employee-targeted van visits to
corporate sites, whose mammograms were covered entirely by private insurance, or who
were under the age of 18 years were excluded. The Washington University Human Research
Protection Office (i.e., institutional review board) approved this study. Verbal consent was
obtained by a trained member of the BHC or mammography van staff prior to the
questionnaire's being administered.
Fayanju et al. Page 3
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Statistical Analysis
Bivariate associations between demographic characteristics and registrants' perceived
barriers to mammography – i.e., responses to the first item of the questionnaire – were
analyzed using chi-square (χ2) tests for which two-tailed p<0.05 was considered significant.
Demographic characteristics found to have statistically significant associations in bivariate
tests were included as independent variables in multivariable logistic regression analyses
modeling each of the most commonly reported barriers to mammography as a yes/no binary
outcome; non-significant predictors were removed via stepwise elimination to reach the final
regression models. The total number of respondents for each regression model reflects the
number of registrants for whom complete demographic data and questionnaire responses
were available. We report adjusted odds ratios (OR) and 95% confidence intervals (CI)
significant at two-tailed p<0.05. Statistical analyses were conducted using SAS 9.3 (SAS
Institute Inc., Cary, North Carolina).
In addition, participants' responses were geocoded to assess the regional distribution of
perceived obstacles to mammography participation. Zip-code-specific distributions of the
most commonly reported barriers were calculated and translated into color-coded maps
created through ArcGIS 10 (ESRI, Inc., Redlands, California).
RESULTS
Between April 2006 and May 2011, a total of 9082 women (Table 2) entered the Siteman
Mammography Outreach Registry. Mean age of registrants was 52.04 years (standard
deviation 8.65). The majority of registrants were black (54%), uninsured (74%), screened on
the mammography van (83%), resided in the greater St. Louis region (85%), and reported a
good or excellent experience as part of the outreach program (92%).
The three most commonly reported barriers to mammography were fear of cost (n=3537,
40%), fear of mammogram-associated pain (n=1152, 13%), and fear of getting bad news
(n=1178, 13%). These barriers were further examined in multivariable logistic regression
models (n=8739).
As shown in Table 3, registrants who were employed (OR 1.11) or who lived in the
Missouri Bootheel (OR 2.32) were more likely to perceive fear of cost as a barrier to
mammography, while those who had health insurance (OR 0.44) or who were (as compared
with non-Hispanic [NH] whites) NH black (OR 0.58) or Hispanic (OR 0.34) were less likely
to report fear of cost as a potential barrier.
As shown in Table 4, registrants who were screened on the van (OR 1.63), had health
insurance (OR 1.39), or were NH Black (OR 1.32) were more likely to report fear of
mammogram-related pain as a potential barrier to getting a mammogram. However,
registrants who reported Other race/ethnicity were less likely to perceive fear of
mammogram-related pain as a barrier (OR 0.57).
As shown in Table 5, having insurance (OR 1.38), being NH Black (OR 2.46), and being
Hispanic (OR 2.98) predicted perceiving fear of receiving bad news as a barrier, while older
Fayanju et al. Page 4
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
women (OR 0.99) and women who were screened on the van (OR 0.77) were less likely to
report this concern.
Insurance status was the only demographic characteristic significantly associated with all
three of the most commonly reported barriers, but its directionality of association was not
consistent: having insurance was associated with a lower likelihood of perceiving cost as a
potential barrier to mammography, but it was associated with a greater likelihood of
reporting fears of mammogram-related pain and receiving bad news as barriers.
The proportions of patients reporting fears of cost, pain during mammography, and
receiving bad news as barriers to mammography were also calculated based on registrants'
residential zip codes. A total of 8916 registrants resided in 282 zip codes at the time of
registration (mean and median of 31.61 and 4 registrants, respectively, per zip code; range of
1 to 542 registrants per zip code). The mean proportions of women per zip code reporting
fears of cost, mammogram-related pain, and receiving bad news as barriers were 49%, 9%,
and 10%, respectively (Figure 2). As noted above, residence in the Missouri Bootheel region
was the only geographic factor found to be associated with a perceived barrier – fear of cost
– in regression analysis.
DISCUSSION
In this study, a variety of demographic variables were associated with perceived barriers to
mammography as reported by registry participants. Most of the registrants were NH black
and/or uninsured, and both race and socioeconomic status (for which insurance coverage can
serve as a proxy measure) have historically been associated with disparities in breast
screening utilization.13–21 Yet, while registrants share demographic characteristics with
population subgroups at risk for screening avoidance, study participants obviously differed
from screening nonparticipants by virtue of having received a screening mammogram. It is
notoriously difficult to engage screening non-participants in research studies precisely
because they are unlikely to have routine, let alone research-specific, contact with the
medical establishment.19,22 However, there is evidence that screeners and non-screeners
from the same communities are more likely to differ with regards to the intensity rather than
the absence or presence of particular emotions or beliefs known to impact health behavior.
For example, a recent qualitative study comparing the characteristics of colorectal screening
participants and nonparticipants – all of whom had health insurance – demonstrated that
while fear of cost was the most common barrier reported by non-screeners, it was also the
second-most commonly reported barrier among screeners.23 In addition, it would be a
mistake to think that our registrants, having been screened for the first time, do not remain at
high risk for future nonparticipation. Lopez et al.'s examination of screeners and non-
screeners in Mississippi revealed that the two groups reported similar barriers to
mammography, indicating that the divide between those who get mammograms and those
who do not s is less fixed and finite than one might initially think.24 The members of our
registry are largely women who belong to demographic groups that are traditionally
underrepresented in screening populations. We feel that they represent an important non-
screener proxy group heretofore uncaptured at this scale (>9000 women) or in this region
(few screening participation studies have been conducted in the lower Midwestern and
Fayanju et al. Page 5
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Southern US). To learn from their responses, we need to explore what characteristics might
make our study participants different from nonscreeners that are otherwise similar to them.
But we also need to determine whether or not the perceived barriers study participants
reported were representative of the beliefs held by nonscreeners within their communities.
Specifically, to interpret our study participants' perceptions of possible barriers to
mammography and to contextualize their responses in light of known risk factors for
mammography nonparticipation, we must consider not only how fears and perceived
barriers to screening translate into health-related behaviors but also the extent to which the
pervasiveness and degree of these barriers might differ between screening participants and
screening nonparticipants.
Fear – sometimes described interchangeably with anxiety and worry – is the most commonly
studied emotional and psychological regulator of screening behavior.13 Fear of cost is a
commonly reported barrier to health-related behaviors in general, and to screening in
particular, and it was the most commonly reported perceived barrier in our cohort.
Consistent with our participants' responses, fear of cost has been shown to persist even when
women are provided with free or low-cost mammograms, as was the case in our sample, or
if they have insurance coverage, particularly if women are African-American, low-income,
older, and/or from an inner-city area.21,25,26 In addition, fear of cost must be further
separated into fear of the cost of the screening procedure itself and fear of the costs
associated with abnormal screenings and a potential cancer diagnosis, including wages lost
while treatment is being conducted. Employed registrants may have been more likely than
unemployed registrants to report fear of cost as a perceived barrier because they were all too
aware of the wages they might lose not only while getting a mammogram but also while
receiving breast cancer treatment, as was found to be the case for early-stage breast cancer
patients in a recent study.27
In our study, registrants from the Missouri Bootheel were also more likely to report fear of
cost as a possible deterrent to mammography. For these women, who live in a rural area
marked by high levels of poverty and a paucity of healthcare facilities offering screening,28
the financial costs associated with physically accessing both a screening provider and a site
for breast-cancer care might prove particularly prohibitive. Regardless of which components
of breast-cancer detection and management contribute to reported fear of cost, it appears to
be a perceived barrier among both screening participants and nonparticipants. But for the
women in our registry, fear of cost was not sufficient to deter them from obtaining a
mammogram, suggesting that free mobile mammography is a successful strategy to address
the cost barrier among underserved populations. Lack of knowledge of such services might
explain why many women in the registry had not been screened previously. Furthermore,
cost may continue to be perceived as a barrier among registry participants because if free
screening were not available, these women might not feel able to afford future
mammograms.
The extent to which fear of mammography-related pain promotes or deters mammography
utilization may depend on the relationship between this type of fear, other fears and
perceived barriers, and emotional coping mechanisms in a given individual.13,29,30 For
example, when coupled with a strong or catastrophic fear of receiving bad news after
Fayanju et al. Page 6
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
screening, fear of mammography-related pain has been demonstrated in various studies to be
greater, and the emotional distress associated with both anticipating and receiving a
mammogram is heightened.31 In previous studies, African-American and Hispanic women
have been found to be more likely than white women to report fear of procedural pain as a
concern that might keep them from getting mammograms.19 In our sample, NH black race
was predictive of seeing mammogram-related pain as a potential barrier to mammography
participation, but Hispanic ethnicity was not (Table 4). This is likely due to the registry's
small Hispanic sample, which reflects the size of Missouri's Hispanic population. According
to the 2010 census, less than 4% of Missourians reported Hispanic ethnicity as compared to
17% of the US population.32 It is unclear to what extent certain unmeasured demographic
characteristics (e.g., country of origin, degree of acculturation, legal immigration status)
within our sample's Hispanic participants are comparable to those characteristics reported in
other studies exploring mammography barriers among Latinas,16,33–35 but such differences
might help explain why Hispanic ethnicity was not associated with procedure-related pain in
our analysis.
It is important to note that insured women in our study were significantly more likely to
report fear of pain as a possible barrier, though there is no evidence in the literature on
screening of a connection between having health insurance and fearing procedural pain. This
finding further validates the concern that free screening programs and health insurance
coverage do not necessarily alleviate anxiety about the logistical and personal challenges
associated with obtaining a screening mammogram.
Fear of “receiving bad news”, i.e., of abnormalities being found during cancer screening, has
been found in some studies to be associated with decreased screening utilization, particularly
among black and Hispanic patients,15–17,20 but fear of finding cancer per se has not been
universally found to be a deterrent to cancer-screening participation.36 Indeed, fear of being
diagnosed with cancer has been shown in some studies to be a motivating factor in
promoting regular screening utilization.36,37 Fear of getting cancer – which reflects both
perceptions of personal susceptibility and disease severity according to the HBM (Figure 1)
– may be an important distinguishing factor between women who do not plan to get a
mammogram, women who plan on getting mammograms, and women who actually receive
mammograms.18 Thus, the fact that fear of receiving bad news was one of the three most
commonly reported perceived barriers in our cohort may not be a particularly surprising
finding given that all of our study participants actually underwent screening mammography.
Indeed, it may very well be that for these women, fear proved to be a protective emotion,
prompting them to get screened. However, study participants might have reported fear of
receiving bad news out of recognition that the same fear that ultimately motivated them to
get screened might very well be a deterrent to screening among their friends and family and
might even at one time have been a personal deterrent for the registrants themselves.
Thus, a potentially powerful strategy for improving screening utilization in the communities
from which registrants come is to incentivize women who sign up to get a mammogram to
return in future years and also to refer a friend, in much the same way retailers encourage
customers to refer their favorite vendors to their friends and receive some kind of reward for
doing so. The incentivization would ideally be trivial and/or in the form of an experience
Fayanju et al. Page 7
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
rather than remuneration, but would be enough to encourage members of the Outreach
Registry to be especially proactive in recruiting their family members and friends. Getting
one's mammogram would be depicted as something friends and family did together to help
themselves and each other.
With regards to targeted education, steps are already underway to specifically address the
fear of getting bad news that might deter women not only from getting screening
mammograms but also from getting diagnostic imaging to follow up abnormal screening
results. In the St. Louis region, efforts have been made to develop a media campaign that
would publicize the curability of breast cancer, the importance of getting annual screening
mammograms and of pursuing follow-up of abnormal mammograms, and the necessity of
undergoing treatment once breast cancer has been diagnosed. This effort and similar “No
Fear” campaigns should be developed in collaboration with cancer centers, community
health organizations, survivor support groups, and primary care providers and would feature
both screening participants who have never had cancer as well as breast-cancer survivors
from demographic groups with historically low mammography participation. Testimonials
from women who look like them would no doubt help demystify the process of getting a
mammogram for women in the medically underserved communities represented by our
registrants.
Our study is novel for a number of reasons. First of all, most studies looking at screening
focus on demographic properties that correlate with participation. While we report these
demographic traits as well, by choosing to look at perceived barriers, we can investigate
mindsets, which – unlike race or education level – are somewhat mutable, though the ways
in which these perspectives, values, beliefs, and preferences are modified must be informed
by the demographic characteristics that help seat a person in a particular culture. Second, our
study is geographically based in the Illinois/Missouri Bi-state region, and there is a relative
paucity of literature on screening participation from Midwestern and Southern regions of the
United States. Furthermore, our inclusion of geographic information system (GIS) analyses
helped illustrate where registrants' perceived barriers were most prominent in our service
region, allowing for geographically targeted interventions. Third, we believe our study
represents the largest review ever conducted of a mobile mammography population and uses
a much larger sample size than previous studies examining barriers to mammography as
perceived by women from medically underserved communities. Fourth, ours is a
prospectively collected database through which we will be able to observe longitudinally the
impact of education and outreach interventions, of changing demographics in the region, and
of implementation of the Affordable Care Act on mammography participation in an
increasingly diverse region with areas of both urban and rural medical need. Historically,
studies examining racial differences in mammography screening have reported complex,
sometimes contradictory findings,24 and our analysis was no exception. But we hope that the
complexity of our findings is embraced as a tool with which to shape solutions regarding
disparities in breast cancer rather than as an indication that these problems cannot be solved.
With the evolution of breast imaging and, as a result, an enhanced ability to diagnose breast
cancer at an early stage, we surgeons are increasingly able to cure breast-cancer patients
through the operations we perform. Accordingly, we believe that promotion of
Fayanju et al. Page 8
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
mammography is a public health goal that should be actively promoted by all surgeons
performing breast surgery. Furthermore, lessons learned from our experience with
mammography among the medically underserved could be applicable to other types of
screening (e.g., colonoscopy for colorectal cancer) that are systematically underutilized by
particular groups in particular regions.
Limitations
Our study had some limitations. First, the outreach registry was not created for the purpose
of conducting research but rather as part of a quality improvement initiative. Thus, although
the process for collecting both objective data and subjective information about registrants'
perceptions and experiences was informed by the HBM, it was not based on validated
research questionnaires; indeed, the public-health trained physician who helped design our
registry's questionnaire was unable to find a validated questionnaire on mobile
mammography at the time the registry was first established in 2006. Nonetheless, the fact
that the results of our statistical analyses of patients' responses were largely concordant with
findings from the screening literature reassured us that our sample was not especially biased
with regards to the perceptions we hoped to study and that the questions and response
prompts from the questionnaire were sufficiently clear to most patients.
Second, no statistical sampling strategy was developed for recruiting patients to the registry,
nor was a target recruitment goal set based on a priori power calculations. Women whose
mammograms were funded by two initiatives developed to provide mammograms to low-
income women were included in our study, and as most of these women were screened on
the mammography van, our registry largely consists of mobile-mammography patients from
all parts of the Missouri/Illinois bi-state region. As far as we know, our study is the largest
review of mobile mammography patients ever conducted. We feel that our large sample of
approximately 9000 participants should somewhat mitigate concerns about selection bias
within our cohort.
CONCLUSION
In summary, women in the Siteman Mammography Outreach Registry reported perceived
barriers to mammography that were similar to concerns that have been expressed by
screening nonparticipants in other studies, though fear of receiving bad news – specifically
of being diagnosed with cancer – might be a concern that not only is more common but also,
somewhat paradoxically, serves as a motivating sentiment among women who receive
screening mammograms. Passage of the Affordable Care Act will make important strides
toward addressing cost as a barrier to mammography,38 but the responses of our registrants
indicate that neither availability of free screening nor having health insurance necessarily
mitigate women's perceived inability to obtain mammograms.
Structural and demographic factors such as age, income, marital status, and ethnicity cannot
be directly or easily modified. Hence, although the study of these variables can help identify
those at risk for poor screening participation, such research offers little direction in terms of
viable interventions.29 It seems increasingly clear that if we are to improve screening rates,
we must develop interventions that target variables that are both amenable to change and for
Fayanju et al. Page 9
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
which there is room for improvement. Screening-averse perceptions and psychological
barriers – unlike race/ethnicity and other immutable demographic variables associated with
screening avoidance – have the potential to be modified through public-health
interventions13 including educational materials and outreach programs developed to
specifically connect with and influence people who have potentially deterrent health
beliefs.18 Having identified fears of cost, mammogram-related pain, and receiving bad news
as significant concerns among women in the registry, we hope not only to improve the
services we provide to the medically underserved women already using our mobile
mammography program but also to encourage peer-to-peer recruitment and to enhance
messaging and outreach in targeted ways that will help expand mammography utilization
among medically underserved women throughout the region.
Acknowledgments
The work of Dr. Fayanju was supported by the National Institutes of Health (NIH) Ruth L. Kirschstein National
Research Service Award Institutional Research Training Grant 5T32CA009621-22. The work of Drs. Goodman and
Drake was supported by the Siteman Cancer Center and NIH via National Cancer Institute (NCI) grant
U54CA153460. The work of Dr. Oka was supported by the NCI Centers for Transdisciplinary Research on
Energetics and Cancer (TREC) (U54CA155496). The authors would like to thank the St. Louis Affiliate of Susan
G. Komen for the Cure, the Show Me Healthy Women initiative, and the Program for the Elimination of Cancer
Disparities (PECaD) of the Siteman Cancer Center at Barnes-Jewish Hospital and Washington University School of
Medicine for their support. We would also like to thank Dione Farria, MD, MPH, for co-writing the registry
questionnaire; Priyanka Garg, MPH, and Xumei Si, MS, MPH, for their assistance with our data analysis; Donna
Jeffe, PhD, and Mary Politi, PhD, for assisting with earlier drafts of the manuscript; and Graham Colditz, MD,
DrPH, for his overall support for this initiative. Portions of this study's findings were presented at the 2012 Breast
Cancer Symposium of the American Society of Clinical Oncology (ASCO), September 13–15, 2012, San
Francisco, CA.
References
1. [Accessed 5 October 2012] The Burden of Cancer in Missouri: A comprehensive analysis and plan,
2010–2015. 2012. http://health.mo.gov/living/healthcondiseases/chronic/chronicdisease/
cancerburdenreport.pdf
2. U.S. Cancer Statistics Working Group. [Accessed 23 July 2013] United States Cancer Statistics:
1999–2009 Incidence and Mortality Web-based Report. 2013. www.cdc.gov/uscs
3. Schootman M, Jeffe DB, Gillanders WE, Yan Y, Jenkins B, Aft R. Geographic Clustering of
Adequate Diagnostic Follow-Up after Abnormal Screening Results for Breast Cancer among Low-
income Women in Missouri. Ann Epidemiol. 2007; 17:704–712. [PubMed: 17574437]
4. Lian M, Jeffe DB, Schootman M. Racial and Geographic Differences in Mammography Screening
in St. Louis City: A Multilevel Study. Journal of Urban Health. 2008; 85:677–692. [PubMed:
18622709]
5. Quesada, LC. [Accessed 16 October 2012] Public Health: Understanding Our Needs - The City of
Saint Louis Department of Health. 2007. http://stlouis-mo.gov/government/departments/health/
documents/upload//UON_VOL_3_20072.pdf
6. Gehlert SJ, Beers CE, Colditz GA. Coordinated care model to reduce rural disparities in breast
cancer mortality. Cancer Epidemiol Biomarkers Prev. 2011; 20(10 Suppl):B65.
7. Fayanju OM, Jeffe DB, Elmore L, Ksiazek DN, Margenthaler JA. Patient and Process Factors
Associated with Late-Stage Breast Cancer Diagnosis in Safety-Net Patients: A Pilot Prospective
Study. Annals of Surgical Oncology. 2013; 20:723–732. [PubMed: 23070783]
8. [Accessed 14 October 2012] Show Me Healthy Women. 2012. http://health.mo.gov/living/
healthcondiseases/chronic/showmehealthywomen/index.php
9. [Accessed 14 October 2012] St. Louis Affiliate of Susan G. Komen for the Cure: Grant Recipients
2012–13. 2012. http://www.komenstlouis.org/site/PageServer?pagename=grants_recipients
Fayanju et al. Page 10
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
10. Champion VL. Instrument development for health belief model constructs. Advances in Nursing
Science. 1984; 6(3):73–85. [PubMed: 6426380]
11. Champion, VL.; Skinner, CS. The Health Belief Model. In: Glanz, K.; Rimer, BK.; Viswanath, K.,
editors. Health Behavior and Health Education: Theory, Research, and Practice. 4th ed. John
Wiley & Sons; San Francisco: 2008.
12. [Accessed 30 November 2012] Disparities in Breast Cancer Screening. 2012. http://
ww5.komen.org/BreastCancer/RacialEthnicIssuesinScreening.html
13. Consedine NS, Magai C, Krivoshekova YS, Ryzewicz L, Neugut AI. Fear, Anxiety, Worry, and
Breast Cancer Screening Behavior: A Critical Review. Cancer Epidemiol Biomarkers Prev. 2004;
13:501–510. [PubMed: 15066912]
14. von Wagner C, Good A, Whitaker KL, Wardle J. Psychosocial Determinants of Socioeconomic
Inequalities in Cancer Screening Participation: A Conceptual Framework. Epidemiol Rev. 2011;
33:135–147. [PubMed: 21586673]
15. Ochoa-Frongia L, Thompson HS, Lewis-Kelly Y, Deans-McFarlane T, Jandork L. Breast and
Cervical Cancer Screening and Health Beliefs Among African American Women Attending
Educational Programs. Health Promot Pract. 2012; 13:447–453. [PubMed: 21451008]
16. Austin L, Ahmad F, McNally M, Steward D. Breast and cervical cancer screening in Hispanic
women: a literature review using the Health Belief Model. Women's Health Issues. 2002; 12:122–
128. [PubMed: 12015184]
17. Bloom JR, Hayes WA, Saunders F, Flatt S. Cancer awareness and secondary prevention practices
in Black Americans: Implications for intervention. Fam Community Health. 1987; 10:19–30.
18. Russell KM, Monahan P, Wagle A, Champion V. Differences in Health and Cultural Beliefs by
Stage of Mammography Screening Adoption in African American Women. Cancer. 2007; 109(2
Suppl):386–395. [PubMed: 17133417]
19. Schueler KM, Chu PW, Smith-Bindman R. Factors Associated with Mammography Utilization: A
Systematic Quantitative Review of the Literature. Journal of Women's Health. 2008; 17:1477–
1498.
20. Vernon SW, Laville EA, Jackson GL. Participation in breast screening programs: a review. Social
Science and Medicine. 1990; 30:1107–1118. [PubMed: 2194294]
21. Young RF, Severson RK. Breast cancer screening barriers and mammography completion in older
minority women. Breast Cancer Research and Treatment. 2005; 89:111–118. [PubMed: 15692752]
22. Meissner HI, Breen N, Taubman ML, Vernon SW, Graubard BI. Which women aren't getting
mammograms and why. Cancer Causes Control. 2007; 18:61–70. [PubMed: 17186422]
23. Medina, GG.; McQueen, A.; Greisinger, AJ.; Bartholomew, LK.; Vernon, SW. Gastroenterology
Research and Practice. 2012. What Would Make Getting Colorectal Cancer Screening Easier?
Perspectives from Screeners and Nonscreeners. doi 10.1155/2012/895807
24. Lopez EDS, Khoury AJ, Dailey AB, Hall AG, Chisholm LR. Screening Mammography : A Cross-
Sectional Study to Compare Characteristics of Women Aged 40 and Older From the Deep South
Who Are Current, Overdue, and Never Screeners. Women's Health Issues. 2009; 19:434–445.
[PubMed: 19879455]
25. Kiefe CI, McKay SV, Halevy A, Brody BA. Is Cost a Barrier to Screening Mammography for
Low-Income Women Receiving Medicare Benefits?: A Randomized Trial. Archives of Internal
Medicine. 1994; 154:1217–1224. [PubMed: 8203989]
26. Urban N, Anderson GL, Peacock S. Mammography Screening: How Important Is Cost as a Barrier
to Use? American Journal of Public Health. 1994; 84:50–55. [PubMed: 8279611]
27. Lauzier S, Maunsell E, Drolet M, et al. Wage Losses in the Year After Breast Cancer: Extent and
Determinants Among Canadian Women. Journal of the National Cancer Institute. 2008; 100:321–
332. [PubMed: 18314472]
28. Rural Policy Research Institute Demographic and Economic Profile; Missouri: 2006. http://
www.rupri.org/Forms/Missouri.pdf [Accessed 6 November 2012]
29. Aro AR, de Koning HJ, Absetz P, Schreck M. Two distinct groups of non-attenders in an
organized mammography screening program. Breast Cancer Res Treat. 2001; 70:145–153.
[PubMed: 11768605]
Fayanju et al. Page 11
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
30. Keefe FJ, Hauck ER, Egert J, Rimer B, Kornguth P. Mammography pain and discomfort: a
cognitive-behavioral perspective. Pain. 1994; 56:247–260. [PubMed: 8022619]
31. Shelby RA, Scipio CD, Somers TJ, Soo MS, Weinfurt KP, Keefe FJ. Prospective Study of Factors
Predicting Adherence to Surveillance Mammography in Women Treated for Breast Cancer. J Clin
Oncol. 2012; 30:813–819. [PubMed: 22331949]
32. United States Census Bureau State & County QuickFacts; Missouri: 2012. http://
quickfacts.census.gov/qfd/states/29000.html [Accessed 6 November 2012]
33. Kagay CR, Quale C, Smith-Bindman R. Screening mammography in the American elderly. Am J
Prev Med. 2006; 31:142–149. [PubMed: 16829331]
34. Mandelblatt JS, Yabroff KR. Breast and cervical cancer screening for older women:
recommendations and challenges for the 21st century. J Am Med Womens Assoc. 2000; 55:210–
215. [PubMed: 10935354]
35. Smith-Bindman R, Miglioretti DL, Lurie N, et al. Does utilization of screening mammography
explain racial and ethnic differences in breast cancer? Ann Intern Med. 2006; 144:541–553.
[PubMed: 16618951]
36. Consedine NS, Magai C, Neugut AI. The contribution of emotional characteristics to breast cancer
screening among women from six ethnic groups. Preventive Medicine. 2004; 38:64–77. [PubMed:
14672643]
37. Edwards NI, Jones DA. Uptake of breast cancer screening in older women. Age and Ageing. 2000;
29:131–135. [PubMed: 10791447]
38. [Accessed 2 February 2013] Women and the Affordable Care Act. 2013. http://
www.healthcare.gov/law/information-for-you/women.html
39. Becker MH, Haefner DP, Kasl SV, Kirscht JP, Maiman LA, Rosenstock IM. Selected psychosocial
models and correlates of individual health-related behaviors. Medical care. May; 1977 15(5
SUPPL):27–46. [PubMed: 853780]
40. Rosenstock IM, Strecher VJ, Becker MH. Social learning theory and the Health Belief Model.
Health education quarterly. Summer;1988 15(2):175–183. [PubMed: 3378902]
Fayanju et al. Page 12
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Figure 1. Health Belief Model Components and Linkages
The major constructs of the Health Behavior Model are perceived susceptibility, severity,
benefits, barriers, and self-efficacy (middle column). Modifying factors (left column) affect
these perceptions, as do cues to action (right column). The combination of beliefs and cues
to action leads to behavior. Perceived barriers (red text) have been demonstrated to be the
single most powerful predictor of health behavior.11,39,40
Fayanju et al. Page 13
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Figure 2.
Geographic distribution of fear of cost (top), fear of mammogram-related pain (middle), and
fear of receiving bad news (bottom) as perceived barriers to mammography
Fayanju et al. Page 14
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Fayanju et al. Page 15
Table 1
Questionnaire Item 1: “What is the reason women don't get a mammogram?”
Standardized Responses
Fear of cost
Being too busy
Fear of mammogram-related pain
Lack of transportation
Not being able to get time off work
Fear of getting bad news
Not knowing they needed a mammogram
Lack of childcare
People they knew were getting mammograms every yeara
Not having health insurance
Other/unspecified barriers
aOnly question response that is NOT a perceived barrier but rather a positive perception associated with mammography utilization.
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Fayanju et al. Page 16
Table 2
Siteman Mammography Outreach Registry Participants' Characteristics, April 2006–May 2011
Demographic Variable (n=9082) n (%)
Age, years (n=8873)
21–39 104 (1.2)
40–45 2189 (24.7)
46–55 3774 (42.5)
56–65 2218 (25.0)
>65 588 (6.6)
Race/Ethnicity (n=8870)
Non-Hispanic Black 4816 (54.3)
Non-Hispanic White 2966 (33.4)
Hispanic 363 (4.1)
Other 725 (8.2)
Annual Income (n=806)
<$10,000 365 (45.3)
$10–20,000 336 (41.7)
>$20,000 105 (13.0)
Education [years of education completed] (n=853)
< High School [0–11] 246 (28.8)
Completed High School [12] 376 (44.1)
Some Post-Secondary Education [13–16] 231 (27.1)
Marital status (n= 8364)
Married 2310 (27.6)
Unmarried 6054 (72.4)
Insurance coverage (n= 8860)
Insured 2278 (25.7)
Uninsured 6582 (74.3)
Site of Residence (n=8908)
St. Louis City 3980 (44.7)
St. Louis County 3597 (40.4)
Bootheel and Other MO 1331 (14.9)
Site of Screening (n=8873)
Mammography Van 7334 (82.7)
Breast Health Center 1539 (17.3)
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Fayanju et al. Page 17
Table 3
Fear of Cost as a Barrier to Mammography (n=8739)a
Demographic Variable Odds Ratio (OR) 95% CIbp-value
Employed vs. not employed 1.11 1.01–1.22 0.032
Site of Residence
North STL vs. Not North STLc0.89 0.79–1.00 0.059
Bootheel vs. Not Bootheeld2.31 1.86–2.88 <0.001
Insured vs. uninsured 0.44 0.40–0.49 <0.001
Race/Ethnicity e
NH Black vs. NH White 0.58 0.52–0.64 <0.001
Hispanic vs. NH White 0.34 0.26–0.43 <0.001
Other vs. NH White 0.65 0.55–0.77 <0.001
Wald χ2df 11= 513.00, p<0.0001
aMultivariable logistic regression model included the following variables (variable values in parentheses with reference group underlined):
employment (employed, unemployed), residence in high-mortality North St. Louis zip code (resident, non-resident), residence in Bootheel zip code
(resident, non-resident), insurance coverage (insured, uninsured), and race/ethnicity (non-Hispanic Black, non-Hispanic White, Hispanic, Other).
bCI = confidence interval
cNorth STL = one of 8 North St. Louis zip codes with disproportionately high rates of both late-stage breast cancer diagnoses and breast-cancer-
specific mortality3–5
dBootheel = southernmost, rural area of Missouri
eNH = Non-Hispanic
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Fayanju et al. Page 18
Table 4
Fear of Mammogram-related Pain as a Barrier to Mammography (n=8739)a
Demographic Variable Odds Ratio (OR) 95% CIbp-value
Site of Screening
Van vs. BHCc1.63 1.33–2.01 <0.001
Insured vs. uninsured 1.39 1.21–1.60 <0.001
Race/Ethnicity d
NH Black vs. NH White 1.32 1.15–1.52 <0.001
Hispanic vs. NH White 1.05 0.73–1.49 0.811
Other vs. NH White 0.57 0.42–0.78 <0.001
Wald χ2df 5= 103.63, p<0.0001
aMultivariable logistic regression model included the following variables (variable values in parentheses with reference group underlined): site of
mammogram provision (on van, at Breast Health Center), insurance coverage (insured, uninsured), and race/ethnicity (non-Hispanic Black, non-
Hispanic White, Hispanic, Other).
bCI = confidence interval
cBHC = Joanne Knight Breast Health Center at Siteman Cancer Center
dNH = Non-Hispanic
Am J Surg. Author manuscript; available in PMC 2015 September 01.
NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript
Fayanju et al. Page 19
Table 5
Fear of Receiving Bad News as a Barrier to Mammography (n=8739)a
Demographic Variable Odds Ratio (OR) 95% CIbp-value
Age 0.99 0.98–0.99 <0.001
Site of Screening
Van vs. BHCc0.77 0.65–0.91 0.003
Insured vs. uninsured 1.38 1.19–1.60 <0.001
Race/Ethnicity d
NH Black vs. NH White 2.46 2.10–2.87 <0.001
Hispanic vs. NH White 2.98 2.22–4.00 <0.001
Other vs. NH White 0.89 0.65–1.23 0.486
Wald χ2df 11= 205.73, p<0.0001
aMultivariable logistic regression model included the following variables (variable values in parentheses with reference group underlined): age
(continuous variable), site of mammogram provision (on van, at Breast Health Center), insurance coverage (insured, uninsured), and race/ethnicity
(non-Hispanic Black, non-Hispanic White, Hispanic, Other).
bCI = confidence interval
cBHC = Joanne Knight Breast Health Center at Siteman Cancer Center
dNH = Non-Hispanic
Am J Surg. Author manuscript; available in PMC 2015 September 01.
