Underuse of Breast Cancer Adjuvant Treatment: Patient Knowledge, Beliefs, and Medical Mistrust

ArticleinJournal of Clinical Oncology 27(31):5160-7 · September 2009with1 Read
Impact Factor: 18.43 · DOI: 10.1200/JCO.2009.22.9773 · Source: PubMed
Abstract

Little is known about why women with breast cancer who have surgery do not receive proven effective postsurgical adjuvant treatments. We surveyed 258 women who recently underwent surgical treatment at six New York City hospitals for early-stage breast cancer about their care, knowledge, and beliefs about breast cancer and its treatment. As per national guidelines, all women should have received adjuvant treatment. Adjuvant treatment data were obtained from inpatient and outpatient charts. Factor analysis was used to create scales scored to 100 of treatment beliefs and knowledge, medical mistrust, and physician communication about treatment. Bivariate and multivariate analyses assessed differences between treated and untreated women. Compared with treated women, untreated women were less likely to know that adjuvant therapies increase survival (on a 100-point scale; 66 v 75; P < .0001), had greater mistrust (64 v 53; P = .001), and had less self-efficacy (92 v 97; P < .05); physician communication about treatment did not affect patient knowledge of treatment benefits (r = 0.8; P = .21). Multivariate analysis found that untreated women were more likely to be 70 years or older (adjusted relative risk [aRR], 1.11; 95% CI, 1.00 to 1.13), to have comorbidities (aRR, 1.10; 95% CI, 1.04 to 1.12), and to express mistrust in the medical delivery system (aRR, 1.003; 95% CI, 1.00 to 1.007), even though they were more likely to believe adjuvant treatments were beneficial (aRR, 0.99; 95% CI, 0.98 to 0.99; model c, 0.84; P < or = .0001). Patient knowledge and beliefs about treatment and medical mistrust are mutable factors associated with underuse of effective adjuvant therapies. Physicians may improve cancer care by ensuring that discussions about adjuvant therapy include a clear presentation of the benefits, not just the risks of treatment, and by addressing patient trust in and concerns about the medical system.

Full-text

Available from: Jenny J Lin
Underuse of Breast Cancer Adjuvant Treatment: Patient
Knowledge, Beliefs, and Medical Mistrust
Nina A. Bickell, Jessica Weidmann, Kezhen Fei, Jenny J. Lin, and Howard Leventhal
From the Departments of Health Policy
and Medicine, Mount Sinai School of
Medicine, New York, NY; and Center
for Research on Health and Behavior,
Rutgers State University of New
Jersey, New Brunswick, NJ.
Submitted March 13, 2009; accepted
May 26, 2009; published online ahead
of print at www.jco.org on September
21, 2009.
Supported by Grant No. NCMHD 2P60
MD00270 from the National Center on
Minority Health and Health Disparities,
Grant No. AHRQ P-01HS10859-02 from
the Agency for Healthcare Research
and Quality, and Commonwealth Grant
No. 20010102 from the Commonwealth
Fund.
Authors’ disclosures of potential con-
flicts of interest and author contribu-
tions are found at the end of this
article.
Clinical Trials repository link available on
JCO.org.
Corresponding author: Nina A. Bickell,
MD, MPH, Mount Sinai School of Medi-
cine, 1 Gustave L. Levy Pl, Box 1077,
New York, NY 10029; e-mail: nina
.bickell@mssm.edu.
© 2009 by American Society of Clinical
Oncology
0732-183X/09/2731-5160/$20.00
DOI: 10.1200/JCO.2009.22.9773
ABSTRACT
Purpose
Little is known about why women with breast cancer who have surgery do not receive proven
effective postsurgical adjuvant treatments.
Methods
We surveyed 258 women who recently underwent surgical treatment at six New York City
hospitals for early-stage breast cancer about their care, knowledge, and beliefs about breast
cancer and its treatment. As per national guidelines, all women should have received adjuvant
treatment. Adjuvant treatment data were obtained from inpatient and outpatient charts. Factor
analysis was used to create scales scored to 100 of treatment beliefs and knowledge, medical
mistrust, and physician communication about treatment. Bivariate and multivariate analyses
assessed differences between treated and untreated women.
Results
Compared with treated women, untreated women were less likely to know that adjuvant therapies
increase survival (on a 100-point scale; 66 v 75; P .0001), had greater mistrust (64 v 53;
P .001), and had less self-efficacy (92 v 97; P .05); physician communication about treatment
did not affect patient knowledge of treatment benefits (r 0.8; P .21). Multivariate analysis
found that untreated women were more likely to be 70 years or older (adjusted relative risk [aRR],
1.11; 95% CI, 1.00 to 1.13), to have comorbidities (aRR, 1.10; 95% CI, 1.04 to 1.12), and to
express mistrust in the medical delivery system (aRR, 1.003; 95% CI, 1.00 to 1.007), even though
they were more likely to believe adjuvant treatments were beneficial (aRR, 0.99; 95% CI, 0.98 to
0.99; model c, 0.84; P .0001).
Conclusion
Patient knowledge and beliefs about treatment and medical mistrust are mutable factors
associated with underuse of effective adjuvant therapies. Physicians may improve cancer care by
ensuring that discussions about adjuvant therapy include a clear presentation of the benefits, not
just the risks of treatment, and by addressing patient trust in and concerns about the medi-
cal system.
J Clin Oncol 27:5160-5167. © 2009 by American Society of Clinical Oncology
INTRODUCTION
Despite the proven effectiveness of adjuvant thera-
pies in the treatment of early-stage breast cancer,
many women do not receive them.
1-4
Patient refusal
accounts for a third of underuse occurrences.
5
Un-
derstanding the benefits and risks of treatment can
be important to the patient experience, as these be-
liefs and perceptions can affect patient behavior. Be-
liefs about cancer are known to affect screening
practices,
6
and perceptions of the risks and benefits
of tamoxifen therapy have been shown to influence
adherence to adjuvant tamoxifen therapy—those
with more positive views are more likely to adhere.
7
Patient knowledge also has been shown to influence
treatment choices,
8
particularly in choosing the type
of breast cancer surgery.
9-12
However, few studies
have reported the effect of patients’ understanding
and beliefs about adjuvant treatment, including
their healthcare experiences and perceptions, on ad-
juvant treatment rates among women who have had
surgery for their breast cancers. By understanding
patient-related reasons associated with underuse of
adjuvant therapies, physicians may be able to tailor
messages to patients to improve rates of treatment.
We sought to identify women’s reasons for un-
deruse by exploring the relationship between pa-
tients’ experiences of medical care, knowledge, and
beliefs about the disease and its treatment. Our goal
was to determine remediable factors that physicians
can affect in the clinical encounter and, in so doing,
improve adjuvant treatment rates.
JOURNAL OF CLINICAL ONCOLOGY
ORIGINAL REPORT
VOLUME 27 NUMBER 31 NOVEMBER 1 2009
5160 © 2009 by American Society of Clinical Oncology
Page 1
Table 1. Survey Domains and Items
Domain Cronbach
Scale Associated With
Higher Values
Items
Emotional social support .88 More support When you had problems, was there someone you could trust to help you
solve them?
If you needed to share your most private worries or fears, was there
someone you could go to?
If you’re worried about an important personal matter, is there someone
you could go to?
Instrumental social support .60 More support If you needed help around the house (ie, cleaning or small repairs), could
you get someone to help without pay?
If you get stranded away from home, is there someone you could call to
come and get you?
Medical mistrust .66 More mistrust Patients have sometimes been purposefully misled at hospitals.
Hospitals often want to know more about your personal affairs or
business than they really need to know.
Hospitals have sometimes done harmful experiments on patients without
their knowledge.
Rich patients receive better care at hospitals than poor patients do.
Male patients receive better care at hospitals than female patients do.
Racism .80 More racism In general, doctors treat African American, Hispanic, and white people
the same.
Racial discrimination in a doctor’s office is common.
In most hospitals, African Americans, Hispanics, and whites receive the
same kind of care.
African Americans and Hispanics can receive the care they want as
equally as white people can.
Self-efficacy .47 More confidence I’m confident I can tolerate and complete my cancer treatments.
I’m confident I can find the doctors I need for my cancer care.
Trust of physician .70 More trust I’m confident in my doctor’s judgments about my medical care.
My doctor would always tell me the truth about my health, even if there
was bad news.
My doctor is well qualified to manage medical problems like mine.
How much do you trust you doctor? (on a scale of 1-10).
Physician communication about
treatment
.79 More communication Your doctor gave you the information you need to make a decision about
your cancer treatment.
Your doctor discussed different types or choice of treatment(s).
Your doctor discussed the pros and cons of each choice with you.
Your doctor understood your concerns about breast cancer and its
treatment.
Your doctor took your preferences into account when making treatment
decisions.
Depression .75 More depressed In the past 4 weeks, how much of the time did you have a lot of energy?
In the past 4 weeks, how much of the time have you felt downhearted
and blue?
In the past 4 weeks, how much of the time have you felt calm and
peaceful?
How often in the past 4 weeks have you had much interest or great
pleasure in doing things?
Adjuvant treatment knowledge
and beliefs
.61 Stronger belief Chemotherapy keeps the cancer from coming back.
Chemotherapy can make women live longer.
Chemotherapy would be harmful.
Chemotherapy would be more harmful than the cancer.
Chemotherapy adverse effects are not worth it.
Hormonal therapy keeps the cancer from coming back.
Hormonal therapy can make women live longer.
Hormonal therapy would be harmful.
Hormonal therapy would be more harmful than the cancer.
Hormonal therapy adverse effects are not worth it.
RT makes it less likely for breast cancer to come back.
RT would be harmful.
RT would be more harmful than the cancer.
Adverse effects of RT would be so bad it might not be worth it.
RT can keep the cancer from coming back.
Abbreviation: RT, radiation therapy.
All scale ranges, 20-100, except for the following: self-efficacy range, 60-100; trust of physician range, 32-100; depression range, 16-100; and adjuvant treatment
knowledge and beliefs range, 15-100.
Patient Reasons for Underuse of Adjuvant Treatment
www.jco.org © 2009 by American Society of Clinical Oncology 5161
Page 2
METHODS
From pathology, we identified eligible women with new, primary, stages I or II
breast cancer whounderwent definitive surgical treatments and required some
form of postsurgical adjuvant therapy, as per the guidelines created by the
project’s Steering Committee, consistent with national guidelines.
13
English-
or Spanish-speaking women who were treated surgically between September
2004 and March 2006 at six New York City hospitals, and who were partici-
pating in a physician-centered tracking and feedback intervention study de-
signed to reduce disparities in breast cancer care,
14
were eligible. Sites included
two tertiary referral centers, three municipal hospitals, and one community
hospital. On the basis of pathology reports, women with stages I or II breast
cancer were contacted by phone after the surgery and were invited to partici-
pate in a physician-centered tracking and feedback study. This study received
institutional review board approval from all participating sites.
To ensure adequate time to complete standard adjuvant therapies, the
women who consented to be in the study were surveyed at least 6 months after
their surgeries. Patient interviews were conducted an average of 11 months
from surgery (range, 6 to 28 months). On the basis of chart abstraction,
women were classified as untreated if they had breast-conserving surgery and
did not receive subsequent radiotherapy, did not receive chemotherapy after
surgery for tumors 1 cm with negative hormone receptors, or did not receive
hormonal therapy for tumors 1 cm with positive hormone receptors, con-
sistent with national guidelines.
13
Data were obtained from inpatient and
outpatient chart reviews; 100 physician offices provided additional treat-
ment information.
14
Table 2. Patient Demographic and Clinical Characteristics by Underuse
Characteristic
Patients
P
Underuse (n 32) Treated (n 226)
No. % No. %
Age .0001
Mean 67.2 56.5
Range 37-90 28-87
Ethnicity .9578
White 20 63 138 61
Black 5 16 44 19
Hispanic 6 19 38 17
Asian 1 3 6 3
Insurance .0001
Commercial 10 31 142 63
Any Medicare 19 59 45 20
Medicaid only 3 14 31 9
Uninsured 0 0 8 4
Less than high school education 11 35 79 35 .9812
Born in United States 23 74 158 71 .6714
Speaks English at home 22 73 190 85 .1117
Has regular source of care 29 91 213 94 .4292
Health .1290
Excellent 2 6 24 11
Very good 8 25 77 34
Good 11 34 76 34
Fair 9 28 47 21
Poor 2 6 2 1
Comorbidity score 1 18 56 53 23 .0001
Depression scale
.8468
Score of 16-100 46.7 45.9
SD 21.6 15.9
Instrumental social support scale† .0262
Score of 20-100 72.5 82.3
SD 26.2 22.6
Emotional social support scale† .9440
Score of 20-100 89.6 89.3
SD 20.5 19.6
Surgery type .2265
Mastectomy 7 22 77 34
Breast-conserving surgery 25 78 149 66
Hospital type .7590
Large tertiary, predominantly white 24 75 175 77
Smaller community, predominantly minority 8 25 51 23
NOTE. Categoric variables were compared with
2
test, and continuous variables were compared with t test.
Abbreviation: SD, standard deviation.
Higher value indicates greater depression.
†Higher value indicates greater support.
Bickell et al
5162 © 2009 by American Society of Clinical Oncology
J
OURNAL OF CLINICAL ONCOLOGY
Page 3
Survey Instrument
The survey instrument was designed to assess patients’ beliefs, attitudes,
and knowledge about breast cancer and its treatment and to record their
experiences with care. Additional, previously validated questions assessed per-
ceived racism,
15
trust in physician,
16,17
trust in the health care system (ie,
medical mistrust),
15
instrumental and emotional social support,
18
and general
and emotional health status.
19,20
Knowledge about adjuvant systemic and local
treatments was asked of all patients (Table 1). Because not all adjuvant treat-
ments were relevant to all women, questions probing belief about a specific
adjuvant treatment were asked only if the woman said her physician recom-
mended that treatment. The survey was translated to Spanish and was back-
translated to English to ensure translation accuracy.
Analysis
To group questions into domains of beliefs, we performed a principal-
components factor analysis with orthogonal rotation. Items were grouped into
the following eight domains with moderate-to-high internal consistency:
emotional social support (
.88), instrumental social support (r .43), trust
of physician (
.70), self-efficacy (
.47), medical mistrust (
.66),
racism (
.80), physician communication about treatment (
.79), and
adjuvant treatment knowledge and beliefs (
.61; Table 1). Items were
summed into scores that were scaled to 100 (range, 5 to 100); questions with
missing response data were imputed to the midpoint. Items that did not load
to a specific factor but were of interest, such as fatalism, were reported as
individual items. General health status was measured with a single item.
Patient beliefs and experiences were compared between treated and
untreated patients as well as by ethnic group. Ethnicity was based on patient
self-report. Bivariate comparisons were conducted with t tests and
2
. As some
independent variables were significantly correlated, interaction terms of inde-
pendent variables were tested; they were not significant and were not included
in the final model. Multivariate analysis included variables significant in the
bivariate analyses. Because underuse of adjuvant therapy was not a rare occur-
rence, odds ratios were converted to adjusted relative risks.
21
All statistical
analyses were performed by using SAS version 9.1.3 (SAS Institute, Cary, NC).
RESULTS
Study Population
On the basis of pathology reports, 401 women had stages I or II
breast cancer, were eligible, and were reachable by phone. Of these, 99
women (25%) refused to participate in the tracking and feedback
study; two did not speak English or Spanish and were not included.
Women age 70 years or older were more likely to refuse consent than
those younger than 70 years (37% v 20%; P .001). Of the 300 eligible
women who consented to chart abstraction, 14 (5%) were unreach-
able, 27 (9%) refused to be interviewed, and one woman was deceased,
which provided a final sample of 258 women. There were no differ-
ences in stage, age, insurance, or hospital between the surveyed
women and those who refused or were unreachable.
Treatment Recommendation and Receipt
As per the guidelines, among the 258 women, 64 should have
received chemotherapy, 150 should have received hormonal therapy,
and 174 should have received radiotherapy. Of these groups, eight
(12.5%) of 64 women, 11 (7.3%) of 150 women, and 15 (8.6%) of 174
women were untreated. Thirty-two of the surveyed women did not
receive adjuvant therapy, and two women did not receive both local
and systemic therapies.
Patient Characteristics
Table 2 lists characteristics of the treated and untreated women.
Approximately 40% of the cohort was ethnic minority. Overall, there
was no statistically significant ethnic difference in underuse of adju-
vant therapy, and a somewhat higher proportion of the treated pa-
tients were black. Treated patients were more likely to have
commercial insurance, whereas a greater portion of underuse patients
were on Medicare. Underuse patients were older, were slightly less
likely to speak English at home, had greater comorbidities, and had
less instrumental social support. Nearly one third of women age 70
years or older experienced underuse, compared with 8% of women
younger than 70 years. There was no significant difference in level of
education, access to care, health status, emotional social support, or
type of hospital where the surgery was performed.
Relationship of Patient Knowledge, Attitudes, and
Beliefs With Underuse
Table 3 lists the relationship between various patient-related be-
liefs, experiences, and underuse. Untreated women report lower levels
of self-efficacy than treated women. Differences in fatalism and trust in
physician were not significant. There was also no significant difference
in patients’ perceptions of financial barriers to treatment.
Untreated women were less likely than treated women to know
adjuvant therapies have been proven to increase survival and were
more likely to believe them harmful (Table 3). Knowledge and beliefs
about treatment were not associated with ethnicity but were associated
with age. On a 100-point scale, women age 70 years and older (71 v 75
points; P .01) and those with comorbidities (72 v 75 points; P .02)
were less likely to think treatments were beneficial. Despite differences
in knowledge and beliefs about treatment, there was no significant
difference found in the underuse patients’ perceptions of their doc-
tors’ communication of information about treatment (88 v 91 points;
P .224) or the patients’ comfort with their physicians, nor was
physician communication of treatment information associated with
patient knowledge (r 0.8; P .21).
Treated women were more likely to say they would undergo
unpleasant or painful treatments if the treatments would improve
their chance of survival (Table 3). Response to this item was asso-
ciated with age: there was a trend for women age 70 years or older
to be less likely to say they would undergo unpleasant treatment
(30% v 70%; P .06).
Women with underuse had greater mistrust of the medical
delivery system (Table 3). Medical mistrust was higher among
women with comorbidities than among those without (58 v 53
points; P .03) and among black and Hispanic women (black, 60
points; Hispanic, 58 points; white, 53 points; Asian, 45 points;
P .02). Medical mistrust did not differ by age but did differ by
education: women with less than a high school education expressed
more mistrust than women who had completed high school or
more education (59 v 52 points; P .01).
Multivariate Model
Multivariate modeling found that the factors most associated
with underuse of adjuvant therapy were older age, comorbidity,
knowledge and beliefs about treatment, and mistrust in the medical
system. Adjusted relative risks ratios are listed in Table 4.
DISCUSSION
Up to one third of episodes of underuse of adjuvant treatment for
early-stage breast cancer are attributed to patient refusal.
1
Refusal of
Patient Reasons for Underuse of Adjuvant Treatment
www.jco.org © 2009 by American Society of Clinical Oncology 5163
Page 4
treatment may be based on patient preferences after informed deci-
sion making or may be due to lack of knowledge about the risks and
benefits of undergoing or foregoing therapies as well as attitudes and
beliefs about cancer and its treatments.
6,7,9
We found that knowledge
and beliefs about adjuvant treatment, mistrust of the medical system,
older age, and the presence of other comorbidities all were associated
with higher rates of underuse of adjuvant breast cancer treatment.
Knowledge and beliefs about adjuvant breast cancer treatment and
mistrust of the medical system are mutable factors and present an
opportunity for doctors to affect treatment rates through improved
communication in their interactions with patients. Older age and
comorbidities are patient characteristics that, although not mutable,
can be used to change physician counseling behaviors and patient
support when discussing treatments.
Women with poorer understanding of the benefit and risks of
adjuvant treatments were more likely to experience underuse of these
treatments, regardless of their levels of education or prior experiences
with individuals with cancer. Disturbingly, women’s knowledge of
treatment benefits and risks were not affected by their physicians’
communications about treatment. Women felt their physicians pre-
sented them with the information needed to make an informed deci-
sion about adjuvant treatment, and their physicians were aware of
their concerns about cancer. Despite physicians’ efforts to explain
Table 3. Relationship of Patient Factors and Underuse
Factor or Statement
Patients
P
Underuse
(n 32)
Treated
(n 226)
Adjuvant treatment beliefs
Knowledge and beliefs about
adjuvant treatment scale .0001
Mean 66.38 10.1
SD 11.8 75.4
I would undergo unpleasant or
painful treatment if it would
improve my chances of living
longer (n 245) .0611
No. 24 207
%8695
Patient beliefs
Medical mistrust scale
.0012
Mean 64.1 53.2
SD 15.2 18.0
Trust scale
.3979
Mean 94.1 95.7
SD 10.2 7.9
Self-efficacy scale .048
Mean 92 96.9
SD 13.5 8.0
Having cancer is like getting a
death sentence (n 249) 1.000
No. 5 41
%1719
If cancer is found early, it can be
cured (n 246) 1.000
No. 29 205
%9795
Knowing someone treated for
cancer made you want to avoid
therapy (n 252) .2549
No. 11 57
%3526
If it’s meant to be, I will stay
healthy (ie, fatalism) (n 236) .4940
No. 18 140
%7566
Communication characteristics
Doctor communication about
treatment scale .224
Mean 88 91
SD 6 13
Doctor gave information needed to
make a decision about treatment .5122
No. 22 196
%8589
Doctor took your preferences into
account in treatment decisions .7042
No. 30 198
%9793
Felt very comfortable with provider .767
No. 27 196
%8487
Financial barriers†
Paying for radiotherapy would be
difficult (n 175) 1.000
No. 3 32
%1920
(continued in next column)
Table 3. Relationship of Patient Factors and Underuse (continued)
Factor or Statement
Patients
P
Underuse
(n 32)
Treated
(n 226)
Paying for chemotherapy would be
difficult (n 159) .7549
No. 4 40
%3127
Paying for hormonal therapy would
be difficult (n 167) .4555
No. 3 21
%2014
NOTE. Categoric variables were compared with
2
or Fisher’s exact test, and
continuous variables were compared with t test.
Abbreviation: SD, standard deviation.
Higher numbers indicate stronger belief.
†Asked only if physician recommended therapy.
Table 4. Multivariate Logistic Model of Patient Factors Associated
With Underuse
Factor
Multivariate Analysis
aRR
95% CI
Age 70 years 1.11 1.06 to 1.13
Comorbidity 1.10 1.04 to 1.12
Mistrust of medical institutions 1.003 1.00 to 1.007
Adjuvant treatment knowledge and beliefs 0.99 0.98 to 0.99
NOTE. Model C statistic 0.84; P ⫽⬍.0001. Self-efficacy, instrumental
social support, and insurance were no longer significant and were not included
in the final model.
Abbreviation: aRR, adjusted relative risk.
Adjusted relative risks of mistrust and of knowledge and beliefs were based
on 1-point incremental scale changes.
Bickell et al
5164 © 2009 by American Society of Clinical Oncology
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OURNAL OF CLINICAL ONCOLOGY
Page 5
treatments, crucial information about the benefits and risks of adju-
vant therapies was somehow lost in translation. This dissociation
between physician communication about treatment options and pa-
tients’ understanding about breast cancer treatment corroborates
similar findings among California’s medical breast cancer popula-
tion.
22
Chen et al
22
found that patients’ knowledge about breast cancer
and its treatment was not related to the quantity of information
provided by the physician but rather to the patients’ emotional con-
nection with their physicians. This communication disconnect raises
the challenge of finding the best strategy to ensure that these messages
are clearly understood.
23-26
Fewer than half of women undergoing
breast cancer surgery knew the impact on survival and recurrence risks
of the two surgical treatment options, despite having discussed the
treatment options with their doctors.
9
Misunderstandings of benefit-
risk information can lead to lack of adherence to treatment regimens
and to decreased satisfaction with the medical encounter.
27-29
New approaches, therefore, are needed to successfully educate
patients to interpret medical risk data.
30
Despite proliferation and
implementation of decision aids,
26,31-33
patients often leave their doc-
tor offices without a clear understanding of their conditions and of
recommended treatments. Decision aids may be helpful in improving
patient understanding; in the case of breast cancer in which adjuvant
treatment is proven efficacious, they may play a crucial role in raising
awareness of treatment options.
34
Computerized informational sup-
port systems have been developed to facilitate communication be-
tween provider and patient and have been utilized by women to learn
about adverse effects of treatment and rates of recurrence
24-26,35,36
;
however, ongoing use of such tools after completion of the grant
funding used to develop and test them is uncertain.
37
Currently, 21 US
states have regulations that require the distribution of pamphlets
describing treatment options for women newly diagnosed with breast
cancer.
38
Enforcement of these rules is difficult at best, and their
implementation and effect on decision making have not been as-
sessed.
39
Although print information may be helpful, personal contact
often is preferred.
40
In fact, patients who received emotional support
from their physicians had better knowledge about breast cancer and its
treatments, which suggests that attending to a patient’s emotional
needs may enable them to hear and learn more technical content and,
thus, improve informed decision making.
22
With increasing demands
on physician time, patient navigators or other patient assistance pro-
viders may be best able to fill this void.
41
A combined approach, one
thatoffersboththeinformation— eitherhardprintor computerized—
and a personal source to answer questions and provide support during
the crucial decision-making time, likely will be most effective in elim-
inating failures to treat. Personal contact can start when a woman
undergoes diagnostic evaluation of a suspicious breast lesion. The
newly diagnosed patient with cancer then can be given breast cancer
information via print pamphlet or computerized support and can be
introduced to a patient assistance provider who can provide the addi-
tional evidence-based information, as well as emotional and practical
support, the patient may need during this highly charged and vulner-
able time.
Providers may communicate differently with patients by age,
ethnicity, education, and income, which leads to disparities.
40,42
We
found that younger women had more accurate knowledge of treat-
ment benefits. However, there is less convincing evidence to support
the benefits of adjuvant treatments among older women.
43-45
Our
findings are similar to other studies, which show that older women
with cancer are more likely to be undertreated.
46-50
Age-related un-
dertreatment of cancer may be due to higher prevalence of comorbidi-
ties, lower overall life expectancy, lower or adverse effects of treatment,
fewer physician referrals for additional treatment, or patient prefer-
ence for less invasive treatment.
44
Although we can not differentiate
among these causes for the lower use of adjuvant therapy among the
older women in this study, the dearth of literature regarding benefits
of adjuvant treatment in older women likely plays a role in both
patients’ and physicians’ preferences about adjuvant treatment and
highlights the critical need to include older women in clinical trials to
strengthen the scientific base needed to inform older women’s deci-
sion making.
Although others have found an ethnic difference in knowledge
and beliefs,
10
we did not. Of note, there was also no ethnic disparity in
treatment in this cohort, although this disparity has been well docu-
mented in other populations.
Mistrust in the medical delivery system was also a significant
mutable predictor of treatment underuse in our population. Ethnic
differences in trust in the medical delivery system have been well
documented in other chronic conditions and have been associated
with poor satisfaction with care.
15
Our results confirm an ongoing
ethnic disparity in trust and extend it from chronic conditions to
adjuvant cancer treatment. Interestingly, however, this ethnic dispar-
ity in medical mistrust did not translate into an ethnic disparity in
treatment receipt, perhaps because of our study population. Survey
respondents had agreed to participate in a study to look at decision
making in breast cancer, but it was a study that activated the surgeons
to reach out to their patients who missed follow-up oncology appoint-
ments. Because our survey responses are cross sectional, we can not
determine whether it was the outreach that helped overcome the
ethnic disparity in mistrust of the medical system and enable women
to get treated. Equally disturbing is the association between mistrust
and presence of another diagnosed comorbidity. This result suggests
that increased exposure to the medical system may lead to greater
mistrust, a finding that should raise a red flag to health care providers.
What experiences in past encounters could have led to such negative
feelings? Our data do not enable us to answer this important question,
but strategies that focus on open communication and disclosure of
medical errors have found specific and teachable communication
behaviors associated with fewer malpractice claims for primary care
physicians.
51
Such approaches may be applied in communicating with
patients with cancer who have had negative medical experiences in the
past that appear to affect attitudes and seem to bear on present treat-
ment decisions.
A major strength of this study is the comparison of beliefs and
experiences among an ethnically diverse population of treated and un-
treated women who underwent surgery for breast cancer. This study
addresses rates of adjuvant treatments proven to increase survival and
factors associated with these treatments, whereas many other studies
focus only on the surgical decision. Survey questions were based on
both focus group findings and previous studies that evaluated beliefs
about breast cancer.
52-55
The survey was conducted via telephone,
which reduced the impact of limited literacy among respondents.
Our study also has important limitations. We recruited our sur-
vey participants from a physician-centered intervention designed to
reduce underuse by closing the referral loop between surgeons and
Patient Reasons for Underuse of Adjuvant Treatment
www.jco.org © 2009 by American Society of Clinical Oncology 5165
Page 6
oncologists. Although the study was directed at physicians, women
had to consent to participate in the survey and chart review. Older
women were more likely to refuse to participate in the intervention
study, which may have influenced our findings, as older women
tended to be more likely to experience underuse and had lesser under-
standing of adjuvant treatment benefits. This study was conducted in
New York City and was in English and Spanish, which limits its
generalizability to other locales and languages. Although our findings
are local, such beliefs may have more global relevance, particularly
given that other studies have demonstrated underlying health and
cultural beliefs to be important barriers to cancer screening, both
among larger US populations and in the United Kingdom.
6,56
Despite physicians’ discussions of breast cancer treatment op-
tions, patients continue to lack important knowledge about the treat-
ments, although this is knowledge that is needed to make truly
informed decisions. To reduce underuse of adjuvant therapies, all
patients should be educated regarding the benefits and risks of treat-
ment; improved patient knowledge may affect underuse of adjuvant
therapy overall and is likely to have a particularly potent effect in
older-age populations. Physicians also should address directly issues
of trust, particularly with minority-population patients and patients
with comorbidities.
AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS
OF INTEREST
The author(s) indicated no potential conflicts of interest.
AUTHOR CONTRIBUTIONS
Conception and design: Nina A. Bickell, Howard Leventhal
Financial support: Nina A. Bickell, Howard Leventhal
Administrative support: Nina A. Bickell, Jessica Weidmann
Provision of study materials or patients: Nina A. Bickell,
Jessica Weidmann, Howard Leventhal
Collection and assembly of data: Nina A. Bickell, Jessica Weidmann
Data analysis and interpretation: Nina A. Bickell, Kezhen Fei, Jenny J.
Lin, Howard Leventhal
Manuscript writing: Nina A. Bickell, Jessica Weidmann, Jenny J. Lin
Final approval of manuscript: Nina A. Bickell, Jessica Weidmann,
Kezhen Fei, Jenny J. Lin, Howard Leventhal
REFERENCES
1. Bickell NA, Wang JJ, Oluwole S, et al: Missed
opportunities: Racial disparities in adjuvant breast
cancer treatment. J Clin Oncol 24:1357-1362, 2006
2. Curtis E, Quale C, Haggstrom D, et al: Racial
and ethnic differences in breast cancer survival:
How much is explained by screening, tumor sever-
ity, biology, treatment, comorbidities, and demo-
graphics? Cancer 112:171-180, 2008
3. Haggstrom DA, Quale C, Smith-Bindman R:
Differences in the quality of breast cancer care
among vulnerable populations. Cancer 104:2347-
2358, 2005
4. Shavers VL, Harlan LC, Stevens JL: Racial/
ethnic variation in clinical presentation, treatment,
and survival among breast cancer patients under
age 35. Cancer 97:134-147, 2003
5. Bickell NA, LePar F, Wang JJ, et al: Lost
opportunities: Physicians’ reasons and disparities in
breast cancer treatment. J Clin Oncol 25:2516-2521,
2007
6. Lannin DR, Mathews HF, Mitchell J, et al:
Influence of socioeconomic and cultural factors on
racial differences in late-stage presentation of breast
cancer. JAMA 279:1801-1807, 1998
7. Fink AK, Gurwitz J, Rakowski W, et al: Patient
beliefs and tamoxifen discontinuance in older
women with estrogen receptor–positive breast can-
cer. Geriatr Nurs 25:372, 2004
8. Gellaitry G, Cooper V, Davis C, et al: Patients’
perception of information about HAART: Impact on
treatment decisions. AIDS Care 17:367-376, 2005
9. Fagerlin A, Lakhani I, Lantz PM, et al: An
informed decision? Breast cancer patients and their
knowledge about treatment. Patient Educ Couns
64:303-312, 2006
10. Hawley ST, Fagerlin A, Janz NK, et al: Racial/
ethnic disparities in knowledge about risks and
benefits of breast cancer treatment: Does it matter
where you go? Health Serv Res 43:1366-1387, 2008
11. Maly RC, Leake B, Silliman RA: Breast cancer
treatment in older women: Impact of the patient-
physician interaction. J Am Geriatr Soc 52:1138-
1145, 2004
12. Hawley ST, Lantz PM, Janz NK, et al: Factors
associated with patient involvement in surgical
treatment decision making for breast cancer. Patient
Educ Couns 65:387-395, 2007
13. National Comprehensive Cancer Network.
Clinical Practice Guidelines in Oncology, 2000.
http://www.nccn.org
14. Bickell NA, Shastri K, Fei K, et al: A tracking
and feedback registry to reduce racial disparities in
breast cancer care. J Natl Cancer Inst 100:1717-
1723, 2008
15. LaVeist TA, Nickerson KJ, Bowie JV: Atti-
tudes about racism, medical mistrust, and satisfac-
tion with care among African American and white
cardiac patients. Med Care Res Rev 57:146-161,
2000 (suppl 1)
16. Safran DG, Taira DA, Rogers WH, et al: Link-
ing primary care performance to outcomes of care. J
Fam Pract 47:213-220, 1998
17. Thom DH, Kravitz RL, Bell RA, et al: Patient
trust in the physician: Relationship to patient re-
quests. Fam Pract 19:476-483, 2002
18. Strogatz DS, Croft JB, James SA, et al: Social
support, stress, and blood pressure in black adults.
Epidemiology 8:482-487, 1997
19. Ware J Jr, Kosinski M, Keller SD: A 12-item
short-form health survey: Construction of scales and
preliminary tests of reliability and validity. Med Care
34:220-233, 1996
20. US Preventive Services Task Force. Screen-
ing for depression: Recommendations and rationale.
Ann Intern Med 136:760-764, 2002
21. Zhang J, Yu KF: What’s the relative risk? A
method of correcting the odds ratio in cohort studies
of common outcomes. JAMA 280:1690-1691, 1998
22. Chen JY, Diamant AL, Thind A, Maly RC:
Determinants of breast cancer knowledge among
newly diagnosed, low-income, medically under-
served women with breast cancer. Cancer 112:
1153-1161, 2008
23. Treiman K, Squiers L: The CIS research agen-
da: Overview of relevant research. US Department
of Health and Human Services, National Institutes of
Health, National Cancer Institute, 2005. http://cis.nci
.nih.gov/research/agenda_overview.pdf
24. Gustafson DH, McTavish FM, Stengle W, et
al: Reducing the digital divide for low-income
women with breast cancer: A feasibility study of a
population-based intervention. J Health Commun
10:173-193, 2005 (suppl 1)
25. Gustafson DH, McTavish FM, Stengle W, et
al: Use and impact of ehealth system by low-income
women with breast cancer. J Health Commun 10:
195-218, 2005 (suppl 1)
26. Shaw BR, Han JY, Baker T, et al: How women
with breast cancer learn using interactive cancer
communication systems. Health Educ Res 22:108-
119, 2007
27. Britten N, Stevenson FA, Barry CA, et al:
Misunderstandings in prescribing decisions in gen-
eral practice: Qualitative study. BMJ 320:484-488,
2000
28. Godwin Y: Do they listen? A review of infor-
mation retained by patients following consent for
mammoplasty. Br J Plast Surg 53:121-125, 2000
29. Logan PD, Scwab RA, Salomone JA, et al:
Patient understanding of emergency department
discharge instructions. South Med J 89:770-774,
1996
30. Woloshin S, Schwartz LM, Welch HG: The
effectiveness of a primer to help people understand
risk: Two randomized trials in distinct populations.
Ann Intern Med 146:256-265, 2007
31. Molenaar S, Sprangers M, Oort F, et al:
Exploring the black box of a decision aid: What infor-
mation do patients select from an interactive CD-rom
on treatment options in breast cancer? Patient Educ
Couns 65:122-130, 2007
32. Whelan T, Levine M, Willan A, et al: Effect of
a decision aid on knowledge and treatment decision
making for breast cancer surgery: A randomized
trial. JAMA 292:435-441, 2004
33. Waljee JF, Rogers MA, Alderman AK: Deci-
sion aids and breast cancer: Do they influence
choice for surgery and knowledge of treatment
options? J Clin Oncol 25:1067-1073, 2007
34. O’Brien MA, Whelan TJ, Villasis-Keever M, et
al: Are cancer-related decision aids effective? A
systematic review and meta-analysis. J Clin Oncol
27:974-985, 2009
Bickell et al
5166
© 2009 by American Society of Clinical Oncology
J
OURNAL OF CLINICAL ONCOLOGY
Page 7
35. Rolnick SJ, Owens B, Botta R, et al: Comput-
erized information and support for patients with
breast cancer or HIV infection. Nur Outlook 47:78-
83, 1999
36. Reference deleted
37. Silvia KA, Ozanne EM, Sepucha KR: Imple-
menting breast cancer decision aids in community
sites: Barriers and resources. Health Expect 11:46-
53, 2008
38. National Cancer Institute, State Cancer Legislative
Database Program. Bethesda, MD, State Cancer Legis-
lative Database, National Cancer Institute, 2007
39. Nayfield SG, Bongiovanni GC, Alciati MH, et al:
Statutory requirements for disclosure of breast cancer
treatment alternatives. JNCI 86:1202-1208, 1994
40. Maly RC, Leake B, Silliman RA: Health care
disparities in older patients with breast carcinoma.
Cancer 97:1517-1527, 2003
41. Battaglia TA, Roloff K, Posner MA, et al:
Improving follow-up to abnormal breast cancer
screening in an urban population. Cancer 109:359-
367, 2007 (suppl 2)
42. Siminoff LA, Graham GC, Gordon NH: Cancer
communication patterns and the influence of patient
characteristics: Disparities in information-giving and
affective behaviors. Patient Educ Couns 62:355-360,
2006
43. Pritchard KI: Have we been guilty of ageism in
the primary treatment of breast cancer? Br J Cancer
96:1011-1012, 2007
44. Hughes KS, Schnaper LA, Berry D, et al:
Lumpectomy plus tamoxifen with or without irradi-
ation in women 70 years of age or older with early
breast cancer. N Engl J Med 351:971-977, 2004
45. Albrand G, Terret C: Early breast cancer in the
elderly: Assessment and management consider-
ations. Drugs Aging 25:35-45, 2008
46. Bouchardy D, Rapiti E, Blagojevic S, et al:
Older female cancer patients: Importance, causes
and consequences of undertreatment. J Clin Oncol
25:1858-1869, 2007
47. Enger SM, Thwin SS, Buist DS, et al: Breast
cancer treatment of older women in integrated health
care settings. J Clin Oncol 24:4377-4383, 2006
48. Hurria A, Leung D, Trainor K, et al: Factors
influencing treatment patterns of breast cancer pa-
tients age 75 and older. Crit Rev Oncol Hematol
46:121-126, 2003
49. Lyman GH, Dale DC, Crawford J: Incidence
and predictors of low dose-intensity in adjuvant
breast cancer chemotherapy: A nationwide study of
community practices. J Clin Oncol 21:4524-4531,
2003
50. Truong PT, Bernstein V, Lesperance M, et al:
Radiotherapy omission after breast-conserving sur-
gery is associated with reduced breast cancer-
specific survival in elderly women with breast
cancer. Am J Surg 191:749-755, 2006
51. Levinson W, Roter DL, Mullooly JP, et al:
Physician-patient communication: The relationship
with malpractice claims among primary care physi-
cians and surgeons. JAMA 277:553-559, 1997
52. O’Malley MS, Earp JA, Harris RP: Race and
mammography use in two North Carolina counties.
Am J Public Health 87:782-786, 1997
53. Mandelblatt JS, Edge SB, Meropol NJ, et al:
Predictors of long-term outcomes in older breast
cancer survivors: Perceptions versus patterns of
care. J Clin Oncol 21:855-863, 2003
54. Hubbell FA, Mishra SI, Chavez LR, et al: The
influence of knowledge and attitudes about breast
cancer on mammography use among Latinas and
Anglo women. J Gen Intern Med 12:505-508, 1997
55. Bickell NA, Young GJ: Coordination of care for
early-stage breast cancer patients. J Gen Intern Med
16:737-742, 2001
56. Thomas VN, Saleem T, Abraham R: Barriers to
effective uptake of cancer screening among black
and minority ethnic groups. Int J Palliat Nurs 11:562,
564-571, 2005
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