Area Deprivation Index is Associated with Variation in Quality of Life and Psychosocial Well-being Following Breast Cancer Surgery

Neighborhood-level factors have been shown to influence surgical outcomes through material deprivation, psychosocial mechanisms, health behaviors, and access to resources. To date, no study has examined the relationship between area-level deprivation (ADI) and post-mastectomy outcomes. A cross-sectional survey of adult female breast cancer patients who underwent lumpectomy or mastectomy between January 2018 to June 2019 was carried out. Patient-specific characteristics and ADI information were abstracted and correlated with postoperative global- (SF-12) and condition-specific (BREAST-Q) quality-of-life performance via multivariable regression. Patients were classified into three ADI terciles: 0–39 (low deprivation), 40–59 (moderate deprivation), and 60–100 (high deprivation). A total of 564 consecutive patients were identified, being mostly white (75%) with mean age of 60.2 ± 12.4 years, median body mass index of 27.8 [interquartile range (IQR) 24.3–32.2) kg/m2, median Charlson Comorbidity Index of 3 (IQR 2–5), and mean ADI of 42.3 ± 25.7. African American and Hispanic patients and those with high BMI were more likely to reside in highly deprived neighborhoods (p = 0.003 and p < 0.001). In adjusted models, patients in highly deprived neighborhoods had significantly lower mean SF-12 physical (44.9 [95% CI, 43.8–46.0] versus 44.9 [95% CI, 43.7–46.1] versus 46.3 [95% CI, 45.3–47.3], p = 0.03) and BREAST-Q psychosocial well-being scores (63.5 [95% CI, 59.32–67.8] versus 69.3 [95% CI, 65.1–73.6] versus 69.7 [95% CI, 66.4-73.1], p = 0.01) relative to moderate- and low-deprivation groups. Patients residing in the most deprived neighborhoods were identified to have worse psychological well-being and quality-of-life. The ADI should be incorporated into the shared decision-making process and perioperative counseling to engender value-based and personalized care, especially for vulnerable populations.

range (IQR) 24.3-32.2) kg/m 2 , median Charlson Comorbidity Index of 3 (IQR 2-5), and mean ADI of 42.3 ± 25.7. African American and Hispanic patients and those with high BMI were more likely to reside in highly deprived neighborhoods (p = 0.003 and p \ 0.001). In adjusted models, patients in highly deprived neighborhoods had significantly lower mean SF-12 physical ( 1], p = 0.01) relative to moderate-and low-deprivation groups. Conclusions. Patients residing in the most deprived neighborhoods were identified to have worse psychological well-being and quality-of-life. The ADI should be incorporated into the shared decision-making process and perioperative counseling to engender value-based and personalized care, especially for vulnerable populations.
Breast cancer health disparities have persisted in the USA despite significant advancements in cancer therapy, screening, diagnosis, and prevention. Recently, there has been growing recognition that socioeconomic factors have a significant impact on health, quality of life, and mortality. 1,2 Previous studies have demonstrated that socioeconomic risk factors may negatively impact surgical outcomes, with higher adjusted rates of mortality, surgical complications, and readmission rates. [3][4][5][6][7][8][9] Of note, the overwhelming majority of these published studies leveraged proxies for social risk such as race/ethnicity, insurance status, and income.
Broadly speaking, social determinants of health (SDoH) denote the conditions within which individuals grow up, live, work, and age that impact their health status. 10 Examples include food insecurity, poor transportation, built environment, and housing instability. [11][12][13] This relationship to health outcomes is believed to be mediated via several mechanisms such as material deprivation, psychosocial stressors, maladaptive health behaviors, and limited access to resources. 14 As US health systems increasingly adopt value-based care payment models to incentivize lower spending and improved clinical outcomes, payers and hospital administrators have acknowledged that accounting for the SDoH must be a key element of these efforts. 15,16 The area deprivation index (ADI) is a validated composite measure of neighborhood-level SDoH that offers policymakers and health service researchers a more holistic view, relative to aforementioned proxies (i.e., race, education level, and insurance status), of the drivers of health outcomes and disparities. Prior studies have shown that patients living in more deprived neighborhoods, as measured by ADI, had higher overall mortality and worse surgical outcomes. 7,17-21 However, current literature provides limited information on the impact of ADI on healthrelated quality of life (QoL) following surgical care for cancer. In the present study, we attempt to address this critical knowledge gap by evaluating the association between ADI and (global and condition-specific) QoL after breast cancer surgery. We hypothesize that patients from more deprived neighborhoods will report lower postoperative QOL and psychosocial well-being, and that certain demographic characteristics are differentially associated with ADI.

Study Design and Participants
This is a secondary analysis of a previously described single-institution, cross-sectional study of all patients who underwent lumpectomy or mastectomy, with or without reconstruction at the University of Texas MD Anderson Cancer Center over an 18-month period (January 2018 to June 2019). 22,23 Adult ([ 18 years) female patients who underwent surgery for a diagnosis of breast cancer, genetic predisposition (e.g. BRCA, Li-Fraumeni syndrome), or ductal carcinoma in situ were identified and administered the BREAST-Q 24 and 12-Item Short Form Health Survey (SF-12). 25 The BREAST-Q is a validated condition-specific patient-reported outcome measure with procedurespecific modules for assessing quality of life and satisfaction following breast surgery. 24 Items are converted to an overall score ranging from 0 to 100, with a lower score indicating a poorer outcome. The SF-12 is a global health patient-reported outcome measure that can be used as a utility measure. 26 It is a variation of the SF-36, with scores ranging from 0 to 100 for two domains, and lower scores indicating lower quality of life. It is most effective when applied to overall physical and mental health. 27 Male patients, international patients seeking treatment, and those with incomplete PRO responses or missing home address information were excluded from the analytic sample. The MD Anderson Cancer Center Institutional Review Board (IRB) approved this study, and all respondents provided consent as part of the questionnaire to have their answers linked to data obtained from our electronic medical record (EPIC; Epic Systems Corp., Verona, WI).

Survey
Our survey administration workflow has been described previously. 22,28 In brief, surveys were delivered via email in English in June 2019, within 18 months following surgery, and required approximately 15-18 min to complete. Three electronic reminders were sent in the event of nonresponse. No monetary or in-kind incentive was provided to participants. Given the sample frame and concerns about undue survey burden by the IRB committee, nonresponder analysis was not pursued. Responses were recorded in Research Electronic Data Capture (REDCap) and linked to corresponding electronic medical record for the following patient-level information: age, race/ethnicity, body mass index (BMI), insurance type, cancer stage, ablative surgery type, laterality (unilateral or bilateral), reconstruction subtype (autologous, implant-based), reconstruction timing (immediate or delayed), and receipt of chemotherapy and/ or radiotherapy.

ADI Construction
Similar to published methods, the permanent address on file for each patient was geocoded and the associated census block group was then linked to a national ADI percentile score. 29 National rather than state-level percentile scores were used to enhance the generalizability of our results. The ADI stratifies geographic areas at a granular block group level utilizing 17 American Community Survey variables from the US Census, such as poverty, housing, employment, and education. 11,20,30 Scores range from 1 to 100, with higher scores indicating greater disadvantage. 20,30 To facilitate the analysis, patients were categorized using the following previously described criteria 18,31,32 : 0-39 (low deprivation), 40-59 (moderate deprivation), and 60-100 (high deprivation).

Outcomes
Our primary aim is to investigate the independent relationship between ADI and postoperative condition-specific (BREAST-Q) and global (SF-12) QOL. To ensure uniformity throughout our patient sample, we selected one quality-of-life domain (psychosocial well-being) and two satisfaction domains (breasts and surgeon) from the BREAST-Q instrument; i.e., those who did and did not undergo breast reconstruction received similar surveys.

Statistical Analysis
Descriptive statistics and frequency/percentages were used to present the continuous and categorical variables. The normality of distribution was verified by a normal quantile-quantile plot and Shapiro-Wilk test. Chi-squared or Fisher's exact tests were used to compare the percentage of patients' characteristic among ADI groups. Continuous variables were compared using the two-sample t-test or analysis of variance (ANOVA) if data had normal distribution. Otherwise, Wilcoxon rank-sum test or Kruskal Wallis test were used alternatively. Missing values were imputed using normal distribution, Bernoulli distribution, and multinomial distribution. BREAST-Q and SF-12 were measured at least 60 days after surgery. Univariate and multiple linear regression models were used to assess the effect of ADI and patient characteristics on BREAST-Q/ SF-12. Residual plots were used for model diagnosis. Adjusted least-squares means were estimated for PROs in each ADI category, controlling for other risk factors. Parsimonious multiple regression models were fit using the stepwise selection method with least Akaike information criterion (AIC). All statistical tests were two-sided, and pvalues less than 0.05 were considered statistically significant. All analyses were performed in SAS Enterprise Guide version 9.4 (SAS Institute Inc., Cary, NC, USA).

Patient Demographics and Characteristics
Overall, 2293 consecutive patients were identified, with 647 surveys returned (28.2% response rate). Those who were male, did not have breast cancer, could not be linked to clinical records, or did not complete the BREAST-Q or SF-12 questionnaires were excluded from the study. Patients who satisfied these criteria (n = 564, 87%) composed the final analytic sample, and 361 were found to have had breast reconstruction (64%).

Area Deprivation Index and Patient Characteristics
Patients who were in the high-deprivation group had significantly higher median BMI than those who were in the moderate-and low-deprivation groups ( Table 1). While the overall proportion of African American and Hispanic patients was low (25.5%), they made up a significantly higher proportion of patients with high ADI. We found a significantly higher proportion of African American patients in the high-deprivation group than were in the moderate-and lowdeprivation groups (41% versus 25% versus 34%, p = 0.003). Similarly, we found that the high-deprivation group had a significantly higher proportion of Hispanic patients than the moderate-and low-deprivation groups (48% versus 17% versus 35%, p = 0.003). On the other hand, we found a significantly higher proportion of white patients in the lowdeprivation group than in the moderate-or high-deprivation groups (53% versus 24% versus 23%, p = 0.003).

Area Deprivation Index and PROs
Overall, the mean BREAST-Q psychosocial well-being score was 71.7 ± 20.4, mean satisfaction with breasts score was 68.3 ± 20.7, and mean satisfaction with surgeon score was 92.4 ± 14.9. The mean SF-12 physical component was 46.4 ± 6.2, and the mean mental score was 45.6 ± 6.0. Univariate models were used to examine the relationship between ADI, BREAST-Q, and SF-12 (

DISCUSSION
This study sought to examine the relationship between ADI and QoL performance following breast cancer surgery. After adjusting for competing risk factors, we found that patients from high-ADI neighborhoods had significantly lower BREAST-Q psychosocial well-being and SF-12 global physical quality of life. Given previously established minimal important difference (MID) values of BREAST-Q (4) and SF-12 (4.2), 33,34 we can infer that high ADI had a clinically important detrimental effect on only condition-specific QoL (i.e., BREAST-Q psychosocial well-being). These results suggest that prospective quality improvement initiatives in breast cancer care must strive to identify and address patient-and community-level drivers of health outcomes. This is salient because the Center for Medicare and Medicaid Services (CMS) has signaled its intent to increasingly leverage PROs to ensure meaningful health system accountability for quality improvement. 35,36 Neighborhoods are complex environments with a variety of economic, social, and physical characteristics that have a significant impact on the health of the residing individual. 37 According to some estimates, SDoH contribute [ 50% of the modifiable factors that drive health outcomes. 38,39 Our findings are consistent with previous studies examining the relationship between area-based measures of socioeconomic deprivation and patient outcomes. 18,19,[40][41][42][43][44][45] These studies have consistently found lower survival, a higher risk of adverse outcomes, and a higher likelihood of hospital readmission among patients living in deprived neighborhoods. Although not our study focus, our unadjusted results also revealed that residents of areas with high economic deprivation were likely to have high BMI and an ethnic background that was African  American or Hispanic. This latter finding is consistent with the prevailing evidence base that area deprivation is associated with obesity, 46 obesogenic growth trajectories in early life, 47 and greater ethnic/racial minority representation. 45 It has been established that barriers to care, limited screening utilization, poor health behaviors, higher comorbidity burden, inconsistent follow-up, delayed diagnosis and recognition of complications, lower likelihood of receiving standard-of-care treatment, and difficulty accessing appropriate treatment are all factors contributing to the worse outcomes among patients from disadvantaged backgrounds. 18,19,[40][41][42][43][44]48 Area-level measures of deprivation frequently capture multiple dimensions such as income, employment, education, insurance status, and housing. 49,50 While previous studies examined the impact of neighborhood deprivation on patient outcomes using indices such as the Index of Concentration at the Extremes (ICE) and the Yost index, we believe that the ADI provides a more holistic assessment of area-level deprivation by utilizing 17 variables from the US Census. Therefore, contextualizing the association between the SDoH outcomes, as represented by ADI, and health outcomes in cancer care will be of great interest to payers, physicians, patients, and policymakers.
Previous studies have also shown that unrealistic patient expectations predict adverse outcomes, such as worsening of functional status and health-related quality of life. 36 Unrealistic expectations, for example, may cause patients to become easily discouraged with postoperative therapy and nonadherent to postoperative recommendations. Patients with low expectations may also lack the motivation needed to continue with therapy, resulting in patients' not receiving the full benefit of breast cancer surgery. Therefore, measures should be taken to better understand what patients in deprived neighborhoods expect after breast cancer surgery, so that services may be provided to fulfill these needs and ensure alignment between patients and breast surgeons as they jointly work toward the same goals.
Although beyond our study scope and the expertise of our research team, we hope that our results serve to catalyze efforts to operationalize routine assessment of the SDoH in breast cancer care encounters. Pursuant to this, ADI can be used as a scalable tool for identifying populations at high risk of poor outcomes following breast cancer surgery by integrating it with the electronic medical record. A treatment plan based on this assessment might now entail a social work consult, use of patient navigators, and referrals to community-based services and financial assistance for immediate resource allocation. Furthermore, increasing the interdisciplinary care team's awareness of and engagement with SDoH will measurably enhance the patient-provider relationship. 51 This study should be viewed in light of several limitations including the single-institution, cross-sectional design. Our institution is a specialized, quaternary referral center, and results may not be generalizable to all practice settings. The study was designed to included only a population of insured women undergoing breast cancer surgery, yet ADI was still associated with patient-reported outcomes. This only strengthens our findings; effect sizes are expected to be magnified in the general population with worse socioeconomic characteristics, particularly among those without baseline insurance coverage. The outcomes were measured at a single point in time and do not demonstrate a causal relationship. We minimized reporting bias by using objective data from patient medical records, employing validated patient-reported outcome measures, and administering the survey within 18 months of surgery. In addition, by including only consecutive patients, we were also able to minimize selection bias. Factors other than ADI, SDoH, and financial hardship may contribute to differences in patient-reported outcomes but were not quantifiable in this study. Future studies should address the limitations of the current study, ideally in the form of prospective, multicenter studies that encompass a more representative patient population and allow for the detection of variation in QoL, from baseline, attributable to ADI. Furthermore, case-control studies examining the beneficial effects, if any, of community-based interventions designed to alleviate ADI on postoperative outcomes will significantly expand the knowledge base.

CONCLUSIONS
Patients residing in neighborhoods that have been marginalized or made vulnerable, characterized by high ADI, who underwent breast cancer surgery were more likely to have worse psychological well-being and quality of life. Patients of color (i.e., African American and Hispanic) and those with high BMI were also likely to come from an economic background characterized by high deprivation. These data suggest that ADI is an important driver of quality of life and psychosocial wellbeing after breast cancer surgery, and advocate for the incorporation of this metric in a ''patient-centric'' approach to facilitate personalized care, especially for vulnerable populations.
AUTHOR CONTRIBUTIONS All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Abbas M. Hassan, Huan T. Nguyen and Jun Liu. The first draft of the manuscript was written by Abbas M. Hassan, Anaeze C. Offodile, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
FUNDING The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
DATA AVAILABILITY The datasets generated during and/or analyzed during the current study are not publicly available due to institutional policies but are available from the corresponding author on reasonable request. ETHICS APPROVAL All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
CONSENT TO PARTICIPATE This is an observational study, and The University of Texas MD Anderson Cancer waived informed consent.