Ethnic disparities in adherence to breast cancer survivorship surveillance care

Ethnic Disparities in Adherence to Breast Cancer SurvivorshipSurveillance Care

Pragati S. Advani, MPH1; Jun Ying, MS2; Richard Theriault, DO3; Amal Melhem-Bertrand, MD3; Stacy Moulder, MD3;

Isabelle Bedrosian, MD4; Welela Tereffe, MD, MPH5; Shon Black, MD4; Tunghi May Pini, MD, MPH6; and

Abenaa M. Brewster, MD, MHS6

BACKGROUND: Adherence to guidelines for surveillance mammography and clinic visits is an important component of breast cancer

survivorship care. Identifying ethnic disparities in adherence may lead to improved care delivery and outcomes. METHODS: Records

were evaluated for 4535 patients who were treated for stage I, II, or III breast cancer at the University of Texas MD Anderson Cancer

Center, Houston, Texas, cancer center between January 1997 and December 2006. Generalized estimating equations and Cox propor-

tional hazards analyses were used to evaluate ethnic differences in missed mammograms and clinic visits up to 4 years of follow-up

and the impact of those differences on overall survival. RESULTS: Nonadherence to guidelines for mammography (P 5.0002) and

clinic visits (P<.0001) increased over time. Hispanic and black patients were more likely to be nonadherent to guidelines for mam-

mography (odds ratio [OR] 5 1.35, 95% confidence interval [CI] 5 1.10-1.65; OR 5 1.36, 95% CI 5 1.11-1.66, respectively) and clinic visits

(OR 5 1.62, 95% CI 5 1.27-2.06; OR 5 1.45, 95% CI 5 1.13-1.86, respectively) than white patients. There was an interaction between His-

panic ethnicity and endocrine therapy on nonadherence to mammography guidelines (P 5.001). Nonadherence to mammography and

clinic visit guidelines was not associated with overall survival. CONCLUSIONS: Withdrawal from breast cancer survivorship care

increases over time, and black and Hispanic patients are more likely to be nonadherent. An understanding of the reasons for ethnic

disparities in adherence to guidelines for mammography and clinic visits is needed to improve retention in survivorship care. Cancer

2014;120:894–900. VC 2013 American Cancer Society.

KEYWORDS: breast cancer, patient adherence, survivorship, ethnicity, health care disparities, surveillance.

INTRODUCTIONPopulation-based mammography screening and innovations in breast cancer treatment over the past decade have led to adecrease in breast cancer mortality in the United States.1 Over the past 15 years, the death rate for patients with breast can-cer has declined by approximately 2.2% per year,2 and the National Cancer Institute estimated in 2013 that there wereapproximately 2.6 million breast cancer survivors in the United States.3 With the growing number of breast cancer survi-vors, surveillance for treatment-related side effects, disease recurrence, or new primary cancers (in addition to promotionof healthy lifestyles among breast cancer survivors) is an important component of the oncological clinical practice.4,5

Guidelines for the surveillance of women with a history of breast cancer have recommended that women undergo an-nual mammography and have a follow-up clinic visit every 4 to 6 months for 5 years.5,6 Previous studies evaluating adher-ence to the guidelines for breast cancer survivorship care have focused largely on understanding the predictors of the use ofsurveillance mammography. Older age at diagnosis,7-13 a lack of adequate health insurance,10-12 the presence of comor-bidities,7-10 minority ethnicities,7-13 and less education10-13 have been associated with lower adherence to the guidelinesfor surveillance mammography. There is limited information on the association between patient-related factors and adher-ence to follow-up clinic visits. Using the Surveillance, Epidemiology, and End Results (SEER)-Medicare data, Keatinget al showed that patients aged� 65 years who had fewer follow-up clinic visits with an oncologist, breast surgeon, or radi-ation oncologist were less likely to undergo surveillance mammograms.7

Corresponding author: Abenaa M. Brewster, MD, MHS, University of Texas MD Anderson Cancer Center, PO Box 301439, Houston, Texas 77230-1439; Fax: (713)

563-5746; [email protected]

1Department of Health Promotion and Behavioral Sciences, University of Texas (UT) School of Public Health, Houston, Texas; 2Department of Biostatistics, The UT

MD Anderson Cancer Center, Houston, Texas; 3Department of Breast Medical Oncology, The UT MD Anderson Cancer Center, Houston, Texas; 4Department of

Surgical Oncology, The UT MD Anderson Cancer Center, Houston, Texas; 5Department of Radiation Oncology, The UT MD Anderson Cancer Center, Houston,

Texas; 6Department of Clinical Cancer Prevention, The UT MD Anderson Cancer Center, Houston, Texas

DOI: 10.1002/cncr.28490, Received: September 23, 2013; Revised: October 17, 2013; Accepted: October 24, 2013, Published online November 20, 2013 in

Wiley Online Library (wileyonlinelibrary.com)

894 Cancer March 15, 2014

Original Article

Given the important goals of breast cancer survivor-ship care and the existing ethnic disparities in breast can-cer mortality,14 identifying disparities in adherence tosurvivorship care is critical for creating opportunities toimprove care delivery and patient outcomes. In this retro-spective study of a large, diverse (by age and ethnicity)cohort of breast cancer survivors treated at The Universityof Texas MD Anderson Cancer Center, we examined therelationship between patient characteristics and adherenceto surveillance mammography and follow-up clinic visits,and overall survival. We hypothesized that ethnic dispar-ities will exist in adherence to breast cancer survivorshipcare and negatively affect overall survival.

MATERIALS AND METHODS

Patient Selection

After we obtained approval from the Institutional ReviewBoard of The University of Texas, MD Anderson CancerCenter, we used the MD Anderson Breast Cancer Man-agement System database to identify patients who under-went treatment at MD Anderson Cancer Center for stageI, II, or III breast cancer (as defined by the American JointCommittee on Cancer Staging Manual, 5th edition, andthe American Joint Committee on Cancer Staging Man-ual, 6th edition)15,16 between January 1997 and Novem-ber 2008. Only patients who were residents of the state ofTexas were included to improve ascertainment of clinicaloutcomes. We identified 5137 patients who met the studycriteria and defined the start of follow-up in survivorshipcare as the time of the first clinic visit or mammogramthat occurred between 9 and 18 months after the start offirst treatment for breast cancer (surgery or systemic ther-apy). We excluded patients who did not have a mammo-gram or clinic visit (n 5 430) and patients whoexperienced a breast cancer event (new primary breast can-cer, recurrence, or death; n 5 172) between 9 and 18months after the start of first treatment. Those patientswere excluded to ensure that we had a disease-free cohortat the start of the study and that the goal of the mammog-raphy and clinic visits was breast cancer survivorship careand not treatment.7 The final cohort for analysis consistedof 4535 patients. We examined survivorship care thattook place up to 48 months after the follow-up startingpoint or until December 1, 2012, whichever date camefirst. To be included in analyses of a surveillance year eval-uating frequency of mammography, participants had tobe female, alive, free of breast cancer, and not have under-gone bilateral mastectomies before the end of the surveil-lance year. To be included in analyses of a surveillance

year evaluating frequency of clinic visits, patients had tobe alive and free of breast cancer before the end of the sur-veillance year.

Variables Collected

The Breast Cancer Management System database con-tains detailed information on patient demographics,breast tumor characteristics, treatment and has previouslybeen described.17 The MD Anderson Cancer Center islocated in the Houston metropolitan area, whose 10counties18 provide the majority of patient referrals to theinstitution. We therefore categorized the participants’county of residence as being within the metropolitan areaor outside the metropolitan area in order to assess theeffect of distance from home residence to the treatment fa-cility on nonadherence to survivorship care. A patient wasconsidered to have received systemic therapy if there wasdocumentation of treatment in the medical record.Follow-up information for patients listed in the BreastCancer Management System is updated every 2 years bydirect review of the medical records and linkage to theMD Anderson Tumor Registry, whose staff mail annualfollow-up letters to each registered patient known to bealive to determine the patient’s clinical status. TumorRegistry staff also check the Social Security Death Indexand the Texas Bureau of Vital Statistics data for the statusof patients who have not responded to a follow-up letter.

Metrics for Adherence to Survivorship CareGuidelines

We identified mammogram and clinic visit records byCurrent Procedural Terminology (CPT) codes obtainedfrom the MD Anderson Enterprise Warehouse Database.We included clinic visits to medical oncology, breast sur-gery, radiation oncology, and the Cancer Prevention Cen-ter at the MD Anderson Cancer Center. Patients wereconsidered nonadherent to mammogram guidelines ifthey did not have at least 1 annual mammogram duringthe survivorship follow-up period. Full adherence to clinicvisit guidelines was defined as a mean of � 2 clinic visitsper year during the survivorship follow-up period.6 Indi-viduals with a mean of < 2 and � 1 clinic visit per yearduring the survivorship follow-up period were categorizedas partially adherent, and individuals who did not have atleast 1 clinic visit per year over all years of survivorshipcare were defined as nonadherent.

Statistical Analyses

Univariable and multivariable analyses for repeatedmeasures with generalized estimating equation (GEE)models were used to estimate the association between

Disparities in Cancer Survivorship Care/Advani et al

Cancer March 15, 2014 895

nonadherence to mammography or clinic visits andpatient and clinical characteristics to model the probabil-ity of nonadherence. We used 2 comparisons to investi-gate nonadherence to clinic visit guidelines: 1)nonadherence and partial adherence versus full adherenceand 2) nonadherence versus partial and full adherencecombined. The trend of nonadherence over time was esti-mated by modeling the probability of nonadherence overyears of survivorship follow-up. Backward stepwise selec-tion was used to select main-effect models in multivariableanalyses. Variables with P< .05 for Wald statistics ofmaximum likelihood estimates were retained in multivari-able models. The interaction between endocrine therapyand ethnicity was evaluated in multivariable modelsbecause adherence to endocrine therapy has been identi-fied as suboptimal among breast cancer survivors.4 Wealso evaluated for interaction between ethnicity and edu-cation level on nonadherence to mammography and clinicvisits. Interaction terms with P< .05 for Wald statistic of

maximum likelihood estimates in any ethnicity categorywere retained in the final multivariable models. The asso-ciation between overall survival and nonadherence tomammography and clinic visit guidelines was evaluatedwith multivariable Cox proportional hazards regressionanalyses modeling the probability of nonadherence withadjustment for ethnicity as well as the statistically signifi-cant (P< .05) variables. Time to event was calculatedfrom the beginning of first treatment to the end of datacollection (December 1, 2012) or death from any cause.All P values were reported at 2-sided significance level of0.05. Data were processed and analyzed with SAS version9.3 software (SAS Institute Inc., Cary, NC).

RESULTS

Association Between Patient Characteristicsand Nonadherence to Surveillance GuidelinesOver Time

Patients included in the analysis differed significantlyfrom patients excluded from the analysis in ethnicity, age,type of health insurance, educational level and distancebetween residence and MD Anderson Cancer Center(Table 1). Of the 4535 patients included in the studyanalysis, 88 developed a new primary breast cancer, 496had a breast cancer recurrence, and 129 died during thestudy period examined.

The Spearman correlation between nonadherence tomammography guidelines and nonadherence to clinicvisit guidelines was 0.52. There was a significant trend forincreasing nonadherence to both mammography andclinic visit guidelines over time among all study partici-pants (P 5 .0002 and P< .0001, respectively) and withineach ethnic group. Approximately 20% of white patientswere nonadherent to mammography guidelines in year 4of survivorship care, compared with approximately 30%and 25% of Hispanic and black patients, respectively(Fig. 1A). Similarly, approximately 15% of white patientswere nonadherent to clinic visit guidelines in year 4 of sur-vivorship care, compared with approximately 26% and20% of Hispanic and black patients, respectively (Fig.1B).

Association Between Ethnicity andNonadherence to Surveillance Guidelines

In univariable analysis, patient characteristics associatedwith nonadherence to mammography included year ofsurvivorship care (P< .0001), older age (P 5 .002), His-panic and black ethnicity (P< .0001), type of insurance(P 5 .0004), body mass index (P 5 .05), county of resi-dence outside of metropolitan area (P< .0001) and

TABLE 1. Patient Characteristics

Characteristic

Included inAnalysisn 5 4535

(%)

ExcludedFrom

Analysis

n 5 602 (%) Pa

Ethnicity .03

White 3242 (71.5) 433 (71.9)

Hispanic 518 (11.4) 86 (14.3)

Black 541 (11.9) 64 (10.6)

Native American/Asian 234 (5.2) 19 (3.2)

Age (y) at diagnosis <.01

�50 1846 (40.7) 223 (37.0)

51-65 1849 (40.8) 229 (38.0)

>65 840 (18.5) 150 (24.9)

Body mass index (kg/m2) .28

<25 (normal/underweight) 1646 (36.3) 222 (36.9)

25-<30 (overweight) 1402 (30.9) 168 (27.9)

�30 (obese) 1487 (32.8) 212 (35.2)

Education level <.01

< High school 262 (5.8) 49 (8.1)

High or technical school 1024 (22.6) 150 (24.9)

College and above 1952 (43.0) 215 (35.7)

Missing 1297 (28.6) 188 (31.2)

Health insurance <.01

Medicaid 158 (3.5) 17 (2.8)

Medicare 563 (12.4) 105 (17.4)

Private 2885 (63.6) 336 (55.8)

Missing 929 (20.5) 144 (23.9)

Area of residence <.01

Houston metropolitan 3008 (66.3) 84 (14.0)

Other 1527 (33.7) 518 (86.0)

Cancer stage <.01

I 1863 (41.1) 291 (48.3)

II 1949 (43.0) 251 (41.7)

III 722 (15.9) 60 (10.0)

a Chi-square for the difference between the patients included in the analysis

and the patients excluded from the analysis.

Original Article


education level (P< .0001) (data not shown). In adjustedmultivariable analysis, Hispanic patients (odds ratio[OR] 5 1.35, 95% confidence interval [CI] 5 1.10-1.65)and black patients (OR 5 1.36, 95% CI 5 1.11-1.66)were more likely to be nonadherent to guidelines formammography than were white patients (Table 2). Therewas a statistically significant interaction between Hispanicethnicity and endocrine therapy in relation to nonadher-ence to mammography guidelines (P 5 .001). Comparedwith white patients who did not receive endocrine ther-apy, Hispanic patients who did not receive endocrinetherapy were more likely to be nonadherent to mammog-raphy guidelines (OR 5 2.28, 95% CI 5 1.63-3.18)(Table 2). Black patients were more likely than whitepatients to be nonadherent to mammography guidelineswhether or not they received endocrine therapy. Therewas no significant interaction between ethnicity and edu-cation level on nonadherence to mammography guide-lines (P 5 .32).

In univariable GEE analysis using the categoriesof nonadherence versus full or partial adherence toclinic visit guidelines, patient characteristics associatedwith nonadherence with clinic visits included year ofsurvivorship care (P< .0001), age at diagnosis (P 5 .005),

ethnicity (P 5 .0001), type of insurance (P 5 .005), areaof residence (P< .0001), and education level status(P< .0001) (data not shown). In adjusted multivariableanalysis, Hispanic patients (OR 5 1.62, 95% CI 5 1.27-2.06) and black patients (OR 5 1.45, 95% CI 5 1.13-1.86) were more likely to be nonadherent to clinic visitguidelines than white patients (Table 3). There was a

TABLE 2. Patient Nonadherence to SurveillanceMammography in Relation to Ethnicity and Endo-crine Therapy

Ethnicity OR (95% CI) P

Model with main effectsa

White 1.00 - -

Hispanic 1.35 (1.10-1.65) <.01

Black 1.36 (1.11-1.66) <.01

Native American/Asian 1.11 (0.81-1.52) .51

Model stratified by endocrine therapyb

Did not have endocrine therapy

White 1.00 - -

Hispanic 2.28 (1.63-3.18) <.01

Black 1.47 (1.04-2.00) .03


Had endocrine therapy

White 1.00 - -

Hispanic 1.18 (0.93-1.50) .17

Black 1.43 (1.11-1.85) <.01


a The model was adjusted for year, age at diagnosis, chemotherapy, radia-

tion therapy, endocrine therapy, area of residence, and education level.b The model was adjusted for year, age at diagnosis, chemotherapy, radia-

tion therapy, area of residence, and education level.

Abbreviations: CI, confidence interval; OR, odds ratio.

Figure 1. Graphs show nonadherence of patients with breastcancer to guidelines for (A) mammography surveillance overtime and (B) follow-up clinic visits over time.

TABLE 3. Patient Nonadherence to Clinic VisitGuidelines in Relation to Ethnicity and EndocrineTherapy

Ethnicity OR (95% CI) P

Model with main effectsa

White 1.00 - -

Hispanic 1.62 (1.27-2.06) <.01

Black 1.45 (1.13-1.86) <.01


Model stratified by endocrine therapyb

Did not have endocrine therapy

White 1.00 - -

Hispanic 2.19 (1.52-3.17) <.01

Black 1.61 (1.11-2.32) .01


Had endocrine therapy

White 1.00 - -

Hispanic 1.34 (0.98-1.84) .06

Black 1.36 (0.97-1.90) .08


a The model was adjusted for year, age at diagnosis, chemotherapy, hormo-

nal receptor status, radiation therapy, endocrine therapy, area of residence,

and education level.b The model was adjusted for year, health insurance status, age at diagnosis,

chemotherapy, radiation therapy, area of residence, and education level.

Abbreviations: CI, confidence interval; OR, odds ratio.



statistically significant interaction between Hispanic eth-nicity and endocrine therapy in relation to nonadherenceto clinic visit guidelines (P 5 .04). In adjusted multivari-able GEE model stratified by endocrine therapy use, com-pared with white patients who did not receive endocrinetherapy, Hispanic patients (OR 5 2.19, 95% CI 5 1.52-3.17) who did not receive endocrine therapy were morelikely to be nonadherent to clinic visit guidelines (Table3). There was no significant interaction between ethnicityand education level on nonadherence to clinic visit guide-lines (P 5 .13).

For clinic visits, in the adjusted multivariable GEEmodel using the combined categories of nonadherenceand partial adherence versus full adherence, there was noevidence of an interaction between ethnicity and endo-crine therapy. Hispanic patients were more likely thanwhite patients to be nonadherent or partially adherent toclinic visit guidelines (OR 5 1.22, 95% CI 5 1.02-1.47).Black patients were more likely than white patients to benonadherent or partially adherent to clinic visit guide-lines, but the association was not statistically significant(OR 5 1.12, 95% CI 5 0.94-1.34) (data not shown).

Association Between Nonadherence toSurveillance Guidelines and Overall Survival

In the adjusted multivariable Cox regression analysis,nonadherence to mammography guidelines (hazard ratio[HR] 5 0.95, 95% CI 5 0.76-1.18) and clinic visitguidelines (HR 5 1.03, 95% CI 5 0.80-1.34) were notassociated with overall survival (Table 4). However, com-pared with white patients, Hispanic patients had adecreased risk of death (HR 5 0.71, 95% CI 5 0.51 to0.98) and black patients had an increased risk of death

that bordered on statistical significance (HR 5 1.26, 95%CI 5 0.98-1.62).

DISCUSSIONWe evaluated ethnic and racial disparities in adherence tothe surveillance guidelines for breast cancer survivorshipcare (mammography and clinic visits) given the increasingrecognition of the importance of long-term follow-upcare for cancer survivors. We found that Hispanic andblack patients are more likely to be nonadherent thanwhite patients, but nonadherence increased among all eth-nicities over time. Among Hispanic patients, nonadher-ence to surveillance guidelines varied significantly inrelation to whether endocrine therapy was received. Therewas no relationship between nonadherence to the guide-lines and overall survival.

Among minority and underserved patient popula-tions, psychosocial factors including higher levels of wor-rying about health, the perceived stigma of breastcancer,19-22 and a higher financial burden11,22,23 havebeen identified as important components of the cancersurvivorship experience that may influence adherence.Having to travel a long distance to see an oncologist hasalso been described as a practical hardship affecting theadherence of many cancer patients to care guidelines.24-26

We found that distance from a patient’s residence to MDAnderson Cancer Center was significantly associated witha lack of follow-up after the completion of treatment andwith nonadherence to survivorship care guidelines. Blackand Hispanic patients were less likely than white patientsto follow up with survivorship care after the completionof treatment and were also likely to live further from MDAnderson Cancer Center than white patients. Because it isalso possible that some patients may have continued theirsurvivorship care at oncological or primary care facilitiescloser to their residences, our findings highlight the im-portance of coordination of survivorship care among dif-ferent types of providers and between providers andpatients.27-29

In a finding unique to our study, we observed a sig-nificant interaction between Hispanic ethnicity and endo-crine therapy in association with nonadherence toguidelines. Hispanic patients with breast cancer who werenot eligible for endocrine therapy or who declined or werenot offered such therapy may have had a lower incentiveto maintain a relationship with a provider, especially iflanguage barriers existed, and lack of a relationship with aprovider may have contributed to their worse adherenceto recommendations for follow-up care. An estimated30% to 50% of patients with breast cancer stop adhering

TABLE 4. Association Between Patient Nonadher-ence to Guidelines and Overall Survival

Parameter HR (95% CI) P

Mammography guidelines

Adherence 1.00 - -

Nonadherence 0.95 (0.76-1.18) .62

Clinic visit guidelines

Adherence 1.00 - -

Nonadherence 1.03 (0.80-1.34) .80

Ethnicity

White 1.00 - -

Hispanic 0.71 (0.51-0.98) .03

Black 1.26 (0.98-1.62) .07


The model was adjusted for age, stage, nuclear grade, chemotherapy, radi-

ation therapy, surgery, and education level.

Abbreviations: HR, hazard ratio; CI, confidence interval.

Original Article


to adjuvant endocrine therapy guidelines by the fifth yearof treatment.30,31 Specific educational interventions maybe needed to retain minority patients not receiving endo-crine therapy in survivorship care.

Our study enrolled patients who were alive andcancer-free 9 to 18 months after the start of first treat-ment, therefore it may have been biased toward patientswith a relatively high short-term life expectancy, forwhom a longer follow-up period would be needed todetect an association between survivorship care and over-all survival. No randomized clinical trials have been con-ducted to evaluate the impact of annual surveillancemammography on patient survival after a diagnosis ofbreast cancer. However, 3 randomized studies evaluatingreduced follow-up strategies compared to routine sched-uled clinic follow-up did not show a negative impact ofreduced follow-up on patient-reported outcomes or earlydetection of cancer.32-34 More research is needed to definethe elements of breast survivorship care that influence sur-vival and quality of life outcomes and to identify subsetsof patients most likely to derive benefit.5

The improved overall survival of Hispanic patientswith breast cancer compared to white patients has beendescribed1 and may be partially attributed to a lower prev-alence of comorbidities35 and dependent on the nativitystatus of the individual.36 Factors such as comorbidities,lifestyle factors, utilization of the health care system, andneighborhood socioeconomic conditions may have con-tributed to the survival gap between black and whitepatients with breast cancer.37-39

This study had several limitations that should beconsidered in interpreting the findings. Because the analy-ses were restricted to the information stored in the BreastCancer Management System database, we were unable toevaluate the role of other factors that can affect survivor-ship care, such as socioeconomic status,10-12 patient spo-ken language,40 acculturation,41 psychosocial variables,42-

44 and the presence of comorbidities.45,46 In addition, it ispossible that even after adjustment for known confound-ers, the multivariable GEE models with 2-way interac-tions or the Cox proportional hazards survival analyseswere affected by residual confounding.

In conclusion, ethnic disparities exist in adherencewith breast cancer surveillance guidelines, and given theimportance of survivorship care, new strategies are neededto promote adherence to care guidelines among breastcancer survivors.7,47,48 Further investigations should focuson determining the efficacy of health promotion interven-tions aimed at improving patient retention in survivorshipcare that take into account an individual’s health and

cultural beliefs, social and financial support, and ease ofaccess to survivorship care.

FUNDING SOURCESThis work was supported by Susan G. Komen Disparities CareerDevelopment Award (to Dr. Brewster), and National Cancer Insti-tute, of the National Institutes of Health, Cancer Center SupportGrant CA016672.

CONFLICT OF INTEREST DISCLOSUREThe authors made no disclosure.

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Ethnic disparities in adherence to breast cancer survivorship surveillance care