Breast Cancer Screening PreferencesAmong Hospitalized Women

Waseem Khaliq, MD, MPH,1 Kala Visvanathan, MB, BS, FRACP, MHS,2,3

Regina Landis, BA,1 and Scott M. Wright, MD1

Abstract

Background: Efforts to increase mammographic screening for early detection of breast cancer among women oflower socioeconomic class and ethnic minorities have been largely unsuccessful. This study explores the receptivityof hospitalized women to inpatient mammography as a novel approach to enhance breast cancer screening.Methods: A cross-sectional study was conducted among 210 hospitalized women, aged 50–75 years, admitted tothe medicine services at Johns Hopkins Bayview Medical Center in early 2012. Unpaired t-test and Chi-squaretests were used to compare characteristics, barriers, and receptivity to inpatient mammography among womenadherent and non-adherent to screening guidelines.Results: One-third of women enrolled were African American, and 60% of study participants reported an annualhousehold income of < $20,000. Thirty-nine percent were overdue for screening, of which, 13% never had amammogram and 28% were at high risk for breast cancer (Gail score ‡ 1.7%). The commonly reported barriers toscreening mammograms were failure to remember appointments and lack of transportation. Most women (91%)believed that it is important for healthcare providers to discuss breast cancer screening while patients are in thehospital. Sixty-eight percent of non-adherent women would agree to have an inpatient screening mammogram ifit was due and offered.Conclusions: A significant number of hospitalized women from lower socioeconomic class are at high risk ofdeveloping breast cancer and non-adherent to mammographic screening. Inpatient hospital stay may be afeasible time for screening and education to ensure adequate breast care and promote screening among thesewomen.

Introduction

Breast cancer is now the most commonly diagnosedcancer globally among women and the leading cause of

cancer death.1 In the United States during 2012, an estimated226,870 new cases of invasive breast cancer and 39,510 breastcancer deaths are expected among women.2 Mortality frombreast cancer has steadily decreased in women since 1990 as aresult of progress in early detection, improved treatment, andrecently decreased incidence.2 Mammography remains thescreening test of choice3 and has reduced breast cancer mor-tality by 22%–35% among women age 50 years and older.4

Despite the steady utilization of screening mammography(67.1% in 2008), studies suggest that women older than 50years, low-income, uninsured, and minorities (especially Af-rican Americans) are initiating mammography later than re-

commended, not having mammography at recommendedintervals, and not receiving appropriate follow-up after apositive screen.5–7

According to the National Health Interview Survey, wo-men aged 40 years and older reporting a mammogram withinthe past two years increased from 29% in 1987 to 70% in 2000.8

Thereafter, the prevalence of mammogram screenings hasbeen gradually trending down. Breen et al. reported thatbreast cancer screening was on a decline from 2000 to 2005—with the largest drop occurring among women 50–59 yearsold.9 The mammography rates remain lowest among theuninsured (35.6 %), and low income women.8–10 Studies havealso shown that physicians tend to recommend mammogra-phy more frequently to well-educated, white women whohave annual incomes above $20,000.11 This unequal emphasismay partially explain the lower screen rates seen among the

1Department of Medicine, Johns Hopkins Bayview Medical Center, Johns Hopkins University School of Medicine, Baltimore, Maryland.2Sidney Kimmel Comprehensive Cancer Center, and 3Department of Epidemiology, Johns Hopkins University School of Medicine and

Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland.

JOURNAL OF WOMEN’S HEALTHVolume 22, Number 7, 2013ª Mary Ann Liebert, Inc.DOI: 10.1089/jwh.2012.4083

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uninsured, minorities, and low income women.8,11,12 Dailyand colleagues found that women living in disadvantagedareas were less likely to have screening mammography, evenafter adjusting for individual-level socioeconomics and accessto health care.13 Some of the well documented barriers to anoutpatient screening mammogram, including patient prefer-ences, appear to be even greater obstacles in these low so-cioeconomic areas.14,15

Breast cancer screening is traditionally offered exclusivelyin outpatient settings, however for some women having ascreening mammography while an inpatient may be a morepractical and preferable option that has not been studied. Thepurpose of this study is to identify characteristics and barriersassociated with non-adherence of mammographic screeningamong an ethnically diverse, predominantly low socioeco-nomic class of hospitalized population and evaluate their re-ceptivity to screening during their inpatient stay.

Methods

Study design and sample

All women between 50 and 75 years admitted to the generalmedical service at Johns Hopkins Bayview Medical Centerbetween October 2011 and January 2012 were approached forparticipation in this cross-sectional study. This age range wasselected in accordance with breast cancer screening recom-mendations from the United States Preventive Services TaskForce (USPSTF).16 Patients with a history of breast cancer, orcomorbidities that could either impact survival or make themineligible to have a mammogram were excluded. This in-cluded patients with current hospitalization for dementia,mental status change, acute myocardial infarction, and acutestroke. Fifty-seven percent of the study population was in-dependent, 10% were wheelchair bound, and 33% were onchronic disability. Patients who had multiple admissionsduring the study period were only enrolled on their first visit.The patients were consented during their hospitalization andsurvey data was collected via bedside interview taking ap-proximately 15 minutes to complete.

Four hundred and forty one women admitted to the med-icine service between October 2011 and January 2012 wereeligible for the study based on their age. Of these, 49 (11%)refused to participate, 43 (10%) had a prior history of breastcancer, 83 (19%) were admitted with altered mental status,and 56 (13%) women were discharged from the hospital be-fore the study coordinator could consent them, leaving astudy population of 210 women.

Protocol and measures

The survey consisted of questions regarding socio-demographic information, breast cancer risk factors includingreproductive history, history of mammographic screening,breast biopsies, and receptivity or preferences related to in-patient screening mammography. Women age 52 or abovewho reported having a mammogram within the last 2 years or24 months were classified as being adherent, and women re-porting a screening mammogram more than 2 years or 24months from the study survey were classified as being non-adherent. In our sample, there were 15 women aged 50–51years. Ten had a screening mammography within the last 24months; these women were characterized as being adherent.

The remaining 5 who had not been screened within the prior24 months were also considered to be adherent with theUSPSTF guidelines because they had 12 more months duringwhich they can be screened. We evaluated access to healthcare with the variables health insurance status and having aprimary care physician. Disease burden was characterized byassessing medical comorbidities. Several questions inquiredabout breast care during their current hospital stay, includingwhether any hospital provider had examined their breasts ortalked to them about breast cancer screening. A few questionswere also used to evaluate the women’s knowledge aboutbreast cancer screening, perceived susceptibility, and thebarriers to screening. Most of the knowledge, susceptibility,and barrier-related questions were adapted from Champion’sHealth Belief Model Scale for breast cancer screening.17 Theparticipants were then asked if they thought it was importantfor the hospital providers to discuss breast cancer screeningwith them during the hospital stay and if they would agree tohave an inpatient screening mammogram if it was due andoffered. At the end of the interview, these women were edu-cated about breast cancer and educational material was pro-vided for breast cancer screening. The risk for developingbreast cancer within the next 5 years was estimated using theNational Cancer Institute Breast Cancer Risk Tool (the Gailmodel, www.cancer.gov/bcrisktool).18–23

Pilot testing of the survey was conducted on fifteen patientsto ensure that questions were clear and not ambiguous. Thisstudy was approved by Institutional Review Board at JohnsHopkins Bayview Medical Center.

Statistical methods

Respondent characteristics are presented as proportionsand means. Unpaired t-test and Chi-square tests were used tocompare demographic and socioeconomic characteristics,barriers to screening mammography, and receptivity to in-patient mammography among women adherent and non-adherent to screening guidelines.

Results

The mean age for the total study population was 60 years;32% of the women were African American, 60% of womenreported annual household income less than $20,000, and 5%were uninsured (Table 1). Average 5-year Gail risk of breastcancer was 1.6%. One-third of the study population (32%) wasat high risk for breast cancer based on a 5-year-risk predictionof ‡ 1.7% using the Gail model. Thirty-nine percent of thehospitalized women in our study were overdue for a screen-ing mammogram (non-adherent), including 13% who hadnever had a mammogram; 28% of the non-adherent womenwere also at high risk for breast cancer (Gail score ‡ 1.7%).

Characteristics for adherent and non-adherent women areshown in Table 1. More non-adherent women had annualincomes of less than $20,000 and a history of a prior stroke.Ninety-four percent of adherent group had a primary careprovider versus 85% of the non-adherent group ( p = 0.04). Non-adherence rates were not statistically different across the agegroups (36%, 43%, and 39% in the 50–59, 60–69, and 70–75years age groups respectively [p = 0.69], as shown in Fig 1).

As shown in Table 2, the most commonly cited barrier tobreast cancer screening was ‘‘I have other problems more im-portant than getting a mammogram.’’ Several barriers to breast

638 KHALIQ ET AL.

cancer screening were perceived differently between the twogroups, including ‘‘I cannot remember to schedule a mammo-gram’’ (27% among adherent and 16% in non-adherent, p = 0.05)and ‘‘No transportation to get to the test’’ (17% among adherentand 29% in non-adherent, p = 0.04). There were no statisticaldifferences between the two groups about knowledge or per-

ceived susceptibility. The two groups were also equally awareof the benefits of screening mammography (Table 2).

In evaluation of preference for inpatient screening amonghospitalized women (Table 3), only 5% (n = 11) of women re-ported that someone had talked to them about breast cancerscreening during their inpatient stay, and 3% (n = 7) of womenreported having a clinical breast examination during that time.Almost all women (91%) believed that it is important forhealthcare providers to discuss breast cancer screening whilepatients are in the hospital. Three-quarters of the women studied(n = 159, 76%) indicated that they would agree to have an in-patient screening mammogram if it was due and it was offered.Eighty percent of the adherent women and sixty-eight percent ofthe non-adherent women ( p = 0.04), including 27% of womenwho had never had a mammogram, confirmed that they wouldbe willing to have a screening mammogram during the hospitaladmission.

Discussion

More than one-third of the hospitalized women surveyedin our study were non-adherent and therefore overdue for ascreening mammogram despite being aware of the potentialbenefit. The majority of these women responded that theywould be agreeable to breast cancer screening performedduring the hospitalization. While this study did not delve

Table 1. Characteristics of the 210 Women Studied During Their Hospitalization

at Johns Hopkins Bayview Medical Center (2011–2012)

Characteristics Adherent (N = 128) Non-adherent (N = 82) p valuea

Age ‡ 60 years, n (%) 68 (53) 48 (59) 0.44African American, n (%) 42 (33) 25 (30) 0.72Married, n (%) 45 (35) 25 (30) 0.48BMI kg/m2, mean (SD) 33.06 (10.34) 34.81 (11.49) 0.26b

High school or more years of education, n (%) 90 (70) 49 (60) 0.11

Employment statusEmployed 26 (20) 16 (20)Unemployed 11 (9) 7 (8) 0.52Retired 42 (33) 20 (24)Disabled 49 (38) 39 (48)

Insurance statusMedicare/Medicaid 57 (45) 44 (54)Private Insurance 65 (51) 33 (40) 0.33Uninsured 6 (4) 5 (6)

Annual Income less than $20,000, n (%) 67 (52) 58 (71) 0.01Has a primary care physician 120 (94) 70 (85) 0.04

ComorbiditiesCurrent smoker, n (%) 32 (25) 30 (40) 0.07Diabetes, n (%) 66 (52) 36 (44) 0.28Hypertension, n (%) 104 (81) 67 (82) 0.93Stroke, n (%) 16 (13) 21 (29) 0.01Cancer (except breast or skin), n (%) 19 (15) 6 (7) 0.1Three or more comorbidities,c n (%) 74 (58) 47 (57) 0.94

Family history of breast cancer,d n (%) 13 (10) 5 (6) 0.31High 5-year-risk for breast cancer usingGail model ‡ 1.7,e n (%) 43 (34) 23 (28) 0.40Mean length of hospital stay (days) (SD) 5 (3.91) 7 (16.68) 0.16b

aChi-Square test (Yates corrected p value where at least 20% of frequencies were < 5).bUnpaired t test statistic.cComorbidities included: diabetes, hypertension, heart disease, chronic kidney disease, stroke, congestive heart failure, chronic obstructive

pulmonary disease, and cancers other than skin or breast.dFamily history of breast cancer was defined as breast cancer in first-degree relatives like mother, sisters, or daughters.eGail score estimated using the National Cancer Institute Breast Cancer Risk Tool (www.cancer.gov/bcrisktool/).BMI, body mass index; SD, standard deviation.

FIG. 1. Percentage of adherence and non-adherence forscreening mammography by age group. *Chi-Square test–pvalue for difference in percentage of non-adherent womenbetween age groups.

CANCER SCREENING IN HOSPITALIZED WOMEN 639

Table 2. Perspectives About Breast Cancer and Screening Among Hospitalized

Women at Johns Hopkins Bayview Medical Center (2011–2012)

QuestionAll

(N = 210)Adherent(N = 128)

Non-adherent(N = 82) p valuea

Knowledge about breast cancer and screeningKnew the name of the test for breast cancer screening, n (%) 143 (68) 91 (71) 52 (63) 0.24Aware that a woman should have a mammogram every 1–2

years, n (%)175 (83) 107 (84) 68 (83) 0.9

All breast lumps are not breast cancers, agree/stronglyagree, n (%)

189 (90) 114 (89) 75 (91) 0.57

Breast cancer can be detected at an early stage,agree/strongly agree, n (%)

203 (97) 124 (97) 79 (96) 0.83b

Early detection of breast cancer improves the prognosisand chances for survival, agree/strongly agree, n (%)

202 (96) 124 (97) 78 (95) 0.52b

Perceived susceptibilityIt is likely that I will get breast cancer agree/strongly agree,

n (%)35 (17) 22 (17) 13 (16) 0.80

BenefitsMammograms find breast lumps early agree/strongly agree,

n (%)189 (90) 114 (89) 75 (91) 0.57

Mammograms decrease the chances of dying from breastcancer, agree/strongly agree, n (%)

172 (82) 105 (82) 67 (82) 0.95

BarriersI cannot remember to schedule a mammogram,

agree/strongly agree, n (%)48 (23) 35 (27) 13 (16) 0.05

I am afraid to have a mammogram because I don’tunderstand what will be done, agree/strongly agree, n (%)

5 (2) 0 (0) 5 (6) 0.01b

Lack of insurance, agree/strongly agree, n (%) 31 (15) 17 (13) 14 (17) 0.45No transportation to get to the test, agree/strongly agree,

n (%)46 (22) 22 (17) 24 (29) 0.04

I have other problems more important than getting amammogram, agree/strongly agree, n (%)

62 (30) 39 (30) 23 (28) 0.71

Not counseled by my doctor about the need to do it,agree/strongly agree, n (%)

10 (5) 3 (2) 7 (8) 0.04b

Unable to get a convenient appointment, agree/stronglyagree, n (%)

23 (11) 18 (14) 5 (6) 0.07

I am too old to need a routine mammogram, agree/stronglyagree, n (%)

8 (4) 3 (2) 5 (6) 0.17b

I am afraid to have a mammogram because I might find outsomething is wrong, agree/strongly agree, n (%)

10 (5) 3 (2) 7 (8) 0.04b

aChi-Square test.bChi-Square with Yates corrected p value where at least 20% of frequencies were < 5.

Table 3. Care Received During Admission and Preferences for Counseling and Screening

While Hospitalized at Johns Hopkins Bayview Medical Center (2011–2012)

QuestionAll

(N = 210)Adherent(N = 128)

Non-adherent(N = 82) p valuea

Someone talked to me about breast cancer screening duringthis hospitalization, n (%)

11 (5) 6 (5) 5 (6) 0.65b

A healthcare provider examined my breasts during thishospitalization, n (%)

7 (3) 3 (2) 4 (5) 0.32b

I think it is important for healthcare providers to discussbreast cancer screening while patients are in the hospital,agree/strongly agree, n (%)

192 (91) 119 (93) 73 (89) 0.32

During a hospitalization, I would agree to have an inpatientscreening mammogram, if it was due and it was offered,agree/strongly agree, n (%)

159 (76) 103 (80) 56 (68) 0.04

aChi-Square test.bChi-Square with Yates corrected p value where at least 20% of frequencies were < 5.

640 KHALIQ ET AL.

deeper into this willingness to be screened during the currenthospital admission, time in the hospital is known to promotereflection and deeper consideration of health and behaviors.24

Notwithstanding the recent change in the breast cancerscreening interval recommendations from annual to biennialby USPSTF,16 significant barriers to the screening still exist.Access to mammography during a hospital admission, whicheliminates barriers like transportation and convenience, makesthe offering of inpatient mammogram germane for increasingscreening rates.25,27 This study confirms prior reports thathave shown decreased breast cancer screening among womenfrom low socioeconomic status and those lacking primary careproviders.27–31 For hospitalized women, particularly those athigh risk of developing breast cancer, seizing the moment andperforming inpatient mammography at a time when potentialbarriers are negated seems like a judicious strategy.

Some of the barriers that women cited in our study need tobe further explored, like ‘‘I have other problems more impor-tant than getting a mammogram.’’ While ‘‘other problems’’may have been interpreted widely by patients, medical co-morbidities must have been among those at the forefront oftheir minds given the context of the hospitalization for acuteillness. Further, while it is likely that multiple comorbiditiesmay deter women from having screening tests, we did notdetect significant differences in comorbidities between adher-ent and non-adherent groups. With the evolution of hospitalmedicine over the last decade, hospitalists have affirmed theirexpertise in providing comprehensive medical care to theirpatients and partnering with outpatient provider to deliverquality. Huth et al. retrospectively reviewed breast cancerscreening practices among hospitalized women and concludedthat hospital providers failed to seize the opportunity to initiatebreast cancer screening during the hospitalization.32 In Huth’sstudy, women were hospitalized for a median of 6 days, breastcancer screening history was documented in 25% of cases,breast examination was performed on 37% of women, andmammography history was recorded in only 7.5% of hospitaladmissions.32 No prior study of which we are aware has as-sessed breast cancer risk or preferences related to breast cancerscreening among the hospitalized women. Consistent with thedata above, we found that breast examination and breastcancer screening education during the hospital stay occurredinfrequently. This is likely because breast issues were not tiedto the reason for the acute hospitalization. However, because91% of the women studied believed that it was important forhospital-based providers to discuss breast cancer screeningduring the hospitalization, the failure to do this could result ina missed opportunity for early detection of breast cancer.

A significant proportion of the non-adherent women (28%)carried a high 5-year-risk for breast cancer (using Gail model‡ 1.7%). Thus, mammography needs to be a high prioritywhenever and wherever these patients interface with thehealthcare system. Ethicists might suggest that inpatient pro-viders who are not ordering mammograms for women knownto be at very high risk for developing breast cancer and whoare overdue for the test might be failing to abide by the phy-sician charter’s principle of the primacy of patient welfare.33

One feature of accountable care will be to offer patients re-commended testing when they interface with our systems ofcare.34 It is interesting to note that some states mandate hos-pitals to offer all inpatient women over the age of 18 a Papa-nicolaou (Pap) test to screen for cervical cancer unless the

patient refuses, there is documentation of a Pap within the past12 months, or the physician orders otherwise.35 However, nosuch legislation exists for breast cancer screening.

Physician recommendations for screening have consistentlybeen shown to strongly influence patient behaviors.36 Over thecourse of several days as hospitalists forge trusting relation-ships with patients, these physicians can prompt and inspirepatients to consider, if not undergo, cancer screening that isoverdue. This time together may result in partnerships thatcan result in shared decision-making between patients andhealthcare providers around critical decisions, related both tohealth maintenance and the presenting illness.15 Currently,hospital physicians do not see prevention and screening ascritical components of their jobs or roles.24 However, if medi-cine is a public trust in which we must always put the patientfirst, expanding the role of the hospital practitioner to includemammography screening may be necessary.

Several limitations of this study should be considered. First,this study was conducted at a single hospital. Second, al-though patients’ preferences were evaluated in this study, wedid not solicit input about the potential impact of preventionand screening on hospital providers and nursing staff.Screening tests that may seem difficult to coordinate in hos-pitals today may become easier as hospitals become morepatient centered. Third, we anticipate that most women willagree to have mammograms if they were ordered. In our ex-perience caring for hospitalized patients for many years atmultiple institutions, few patients refuse tests that are re-commended by the physicians caring for them in the hospital.

Conclusion

Since early detection translates into reduced mortality, thereis a need to optimize cancer prevention for breast cancer. Itappears that women admitted to the hospital would value theopportunity to have breast cancer screening addressed duringtheir stay. Because hospitalization is a unique time duringwhich patients are a captive audience who are reflecting upontheir health, there is tremendous potential for hospitalists toprovide comprehensive care for the whole patient. This couldin turn have a major impact on public health, particularly ifthese patients share their new knowledge and perspectiveswith those in their sphere of influence—friends and family.Future studies are required to evaluate the practical aspectssuch as the feasibility and financing of prevention andscreening for breast cancer while patients are hospitalized.

Acknowledgments

Dr. Wright is a Miller-Coulson Family Scholar, and thissupport comes from the Hopkins Center for InnovativeMedicine.

Disclosure Statement

No competing financial interests exist.

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Address correspondence to:Waseem Khaliq, MD, MPH

Department of MedicineJohns Hopkins Bayview Medical Center

Johns Hopkins University School of Medicine5200 Eastern Avenue

MFL Building, West Tower, 6th FloorBaltimore, MD 21224

E-mail: wkhaliq1@jhmi.edu

642 KHALIQ ET AL.