Race, Stress, and Breast Cancer: A Scoping Review

doi:10.21203/rs.3.rs-5166029/v1

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Race, Stress, and Breast Cancer: A Scoping Review

https://doi.org/10.21203/rs.3.rs-5166029/v1

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Objective

Toxic stress may influence breast cancer (BC) risk and progression through various physiological and biological pathways, potentially differing based on racial categories. We systematically reviewed the literature on the relationship between race, stress, and BC.

Methods

We searched PubMed (prior to August 2023), Embase, Web of Science, PsycINFO, and Scopus (prior November 2023) to identify relevant peer-reviewed studies. Two independent reviewers screened titles, abstracts, and full text, with disagreements resolved by discussion or a third reviewer. Data extraction and thematic synthesis were conducted independently.

Results

We identified 30 articles, including 21 original observational studies and 9 reviews. Primary studies explored biological markers including measures of allostatic load (AL), epigenetic changes, and social determinants of health. Studies explored biological marker, AL, epigenetic changes, and social determinants of health. Black women with BC exhibited higher AL and shorter telomeres compared to White women. Epigenetic modifications were associated with social determinants, potentially influencing BC risk and aggressiveness. Significant associations were found between neighborhood disadvantage, social support, and psychosocial stress among women of color with BC.

Conclusion

This review provides a landscape view of the current evidence on the complex interplay between social stressors, biological responses, and racial and ethnic disparities in BC outcomes. Findings highlight the significant role of chronic psychosocial stress in the disproportionate burden of breast cancer faced by marginalized groups. Further research is needed to explore mechanisms and evaluate multilevel interventions addressing individual stress management, neighborhood resources, and societal-level policies to improve breast cancer prevention, detection, and management.

allostatic load

biological stress

health disparities

psychosocial stress

toxic stress

Stress is described as a biological state of the body or a generalized psychological alert in response to threatening agents.¹ Stressors, as defined by Wheaton and Montazer, refer to conditions of threat, challenge, demands, or structural constraints that, because of their occurrence or existence, call into question the operating integrity of the organism.² When an individual experiences an event or environmental shift that causes stress, toxic effects may ensue depending on the reactive biological and psychological mechanisms that are triggered, and the duration of the stress reaction. For the purposes of this review, we will describe prolonged and adverse biological and psychological effects of exposure to stressors as “toxic stress”. The significance of stress and stressful life events in influencing the risk of developing breast cancer and breast cancer outcomes has been established in scientific literature, as reflected by a recent systematic review and meta-analysis showed that a history of stressful life events is related to a moderate increase in breast cancer risk.³

Toxic stress likely exerts its effects on cancer behavior at least partially through neuroendocrine regulation. A study investigating the role of neuroendocrine activation in breast cancer progression in mouse models, found that stress (i.e., restraining mouse in a confined space and preventing it from moving freely) resulted in a substantial 30-fold increase in distant metastasis.⁴ Stressful life events and stressors exert their influence on health behaviors and neuroendocrine regulation by triggering psychological processes that may contribute to anxiety, depression, and decreased psychological well-being.⁵ This impact extends to biological dysregulation, leading to elevated levels of stress hormones, circulating cytokines, and other inflammatory markers, as well as a potential for increased risky health behaviors and reduced healthcare-seeking behaviors.^5,6 Additionally, the physiological effects of stress hormones, such as cortisol, influence mammary gland development, estrogen activity, and intracellular pathways.^6,7 In summary, these studies highlight multiple pathways through which toxic stress exerts a biologic impact on patients.

Although individual experiences can be stressors for any person, significant racial and ethnic differences in exposure and response to stress exist at the population level in part because of structural and systemic inequalities, early life stressors, and environmental exposures faced by many individuals from marginalized racial and ethnic groups. These individuals also tend to live in disadvantaged neighborhoods characterized by structural dilapidation, poverty, a disparate number of female-headed households, limited employment opportunities, and lower educational attainment.^8–10 Black or African American (henceforth referred to as Black) and Hispanic individuals who report poorer health are more likely to have experienced stressors related to finances, relationships, employment, and lifetime discrimination compared to White individuals.⁹ The psychological and biological responses to these stressors are influenced by the nature of the stressor, including its frequency, intensity, and timing of exposure.^5,11,12

The cumulative impact of stress on the body can be estimated using a physiological indicator of dysregulation termed allostatic load (AL).¹³ AL is estimated as an index measure including multiple markers of physiological dysregulation influenced by the social and physical environment, such as cortisol, epinephrine, norepinephrine, dehydroepiandrosterone sulfate (DHEA), diastolic (DBP) and systolic blood pressure (SBP), waist-hip ratio, total cholesterol, and glycated hemoglobin (HgA1C). ^14,15 Other markers sometimes included in AL are insulin-like growth factor-1, body mass index (BMI), and C-reactive protein (CRP). While several formulas have been offered for calculation of allostatic load, the most frequently utilized are markers of cardiovascular, metabolic and neuroendocrine dysregulation. AL is particularly useful in understanding and estimating racial disparities in breast cancer.¹⁶ As a link between exposure to environmental stressors and tertiary health impacts, AL is a useful concept to integrate into studies of cancer health disparities.

From a psychological standpoint, stress can be examined through a stimulus perspective arising from the characteristics and external circumstances a person encounters or a response perspective defined as complex reactions to adaptive demands forced by environmental challenges.¹² Validated instruments and questionnaires that assess stress exist, however, evaluating the severity of stress through patient-reported instruments has limitations. Individual factors, such as reliance and socioeconomic status, influence responses to stress and, these existing assessments often fail to capture the intricate and multiplicative interactions among these factors,^12,17 particularly in the context of racial and ethnic disparities. This necessitates a deeper exploration of the literature to understand the complex interactions between stress, social determinants of health, and racial disparities in breast cancer. To this end, we systematically reviewed the relationship between race, stress (psychological and biological), and breast cancer. This knowledge can guide the development of culturally sensitive assessment tools such as AL measures, thereby promoting more accurate diagnoses, personalized treatment plans, and improved outcomes for all patients.

Search Strategy and Study Selection

This review focused on the relationship between race, ethnicity, and stress in women with breast cancer. We used the databases PubMed prior to August 2023 and Embase, Web of Science, PsycINFO, and Scopus prior to November 2023 to identify relevant peer-reviewed literature. The search terms were categorized into three groups: breast cancer, race and ethnicity, and stress. A detailed list of the search terms is provided in Table 1.

Table 1

Definition and implementation of search terms
Category	Term criteria
Breast cancer	"breast cancer” OR "breast neoplasm*"
Race and ethnicity	Black OR "African American" OR White OR Caucasian OR Hispanic OR Latin* OR "Asian American" OR "Native Hawaiian OR "Pacific Islander" OR AAPI
Stress	stress OR distress* OR "allostatic load" OR "multi-systemic biological risk” OR “Multi-Systemic Biological Risk" OR "AL overload"

Articles describing concepts related to stress in women with breast cancer within one or multiple racial or ethnic groups were included. Interventional and animal studies were excluded to focus on observational studies that capture existing contextual disparities. The focus of our review were descriptive and observational studies to minimize the influence of confounding factors. Abstracts or poster presentations and gray literature without peer-reviewed validation, studies conducted outside the US (considering that the relationship between race or ethnicity, stress, and breast cancer may not align with that in the US), publications in languages other than English, studies involving individuals with different cancer types, and studies involving individuals at risk for breast cancer but without breast cancer were also excluded. Furthermore, studies focusing on quality of life, physical concerns, symptoms, distress, or burden were excluded as they fell outside the scope of the review’s primary objectives.

Analysis

References were imported into Covidence, an online software that streamlines the production of systematic reviews. Two reviewers, NE and KH independently assessed the titles and abstracts for relevance and eligibility for the full-text review. Subsequently, NE and FA thoroughly reviewed the remaining articles to determine eligibility for data extraction. Conflicts were resolved through discussion or consultation with a third reviewer, GR. Data extraction involved the identification of specific findings corresponding to the inclusion criteria using a data extraction form. NE and FA independently extracted information about each included study, including title, author, year of publication, aim, study design, methodology, study sample and setting, participant inclusion and exclusion criteria, and study outcomes. After careful review, key findings and topics were systematically extracted and discussed to reach a consensus. Summaries were consolidated by overarching themes and are presented in Table 2, with a brief overview of each study.

Table 2

Summary of original studies included in this review (N = 21).
Study ID	Title	Aim(s)	Population	Study design/Follow up period for longitudinal	Outcomes of the study:	Variables	Summary of findings
Shen 2020	Biological Aging Marker p16INK4a in T Cells and BC Risk	To conduct a two-stage study that assesses and validates the relationship between p16INK4a mRNA expression in T cells and risk of BC.	From a 2012 BC case-control study at The University of Texas, M. D. Anderson Cancer Center, N = 945	Case-control	BC risk	Socio-economic/ Psychosocial/ Lifestyle: age, race, marital status, annual income, smoking Epigenetic: p16INK4a mRNA expression in T cells (a marker of cellular senescence)	Higher pre-treatment p16INK4a mRNA expression is associated with a 1.4 times greater increase in BC risk. Higher levels of p16INK4a mRNA expression are associated with breast tumors that are aggressive, larger in size, and have poor differentiation. Statistically significant variations in expression of p16INK4a mRNA based on age (< 51 years: OR 4.72 vs ≥ 51 years: OR 2.02, p < 0.001), race (Black: OR 3.79 vs White: OR 3.08, p = 0.021), family history (positive: OR 4.90 vs negative: OR 3.11, p < 0.001), and marital status (married: OR 4.92 vs unmarried: OR 4.27, p = 0.029) exists. Other significant variations included annual income, and smoking status.
Chen 2023	The Implications of Racialized Economic Segregation and Allostatic Load on Mortality in Patients with BC	To understand the relationship between racialized economic segregation, measured through ICE* and allostatic load. Additionally, to understand the relationship between ICE and overall mortality, and assess the influence of AL on the link between ICE and all-cause mortality in patients with BC.	Ohio State University Cancer Registry, N = 4296	Cross-sectional	All-cause mortality, allostatic load, racialized economic segregation using the Index of Concentration at the Extremes (ICE)	Socio-economic/ Psychosocial/ Lifestyle: Medicaid, marital status, smoking, neighborhood segregation Cancer-related: All-cause mortality Inflammatory Biomarkers: AL [i.e., ALP, albumin, creatinine serum, heart rate, WBCC, BMI, SBP, DBP, BUN, and glucose; high AL was defined as a total AL score (range 0–10) greater than the median]	Higher AL was associated with lower ICE values (i.e., more deprived and segregated). Living in highly segregated neighborhoods is associated with 55% higher odds (OR 1.55, 95% CI 1.36–1.76) of having a high AL even after adjusting for demographic and clinical characteristics (adjusted OR 1.40, 95% CI 1.21 − 1.61). Higher racialized economic segregation was linked to being Black, having Medicaid insurance, being single/widowed/divorced, smoking, and having TNBC. Patients living in highly racially segregated neighborhoods had a 63% higher risk of all-cause mortality.
Parente 2013	Association between BC and allostatic load by race: National Health and Nutrition Examination Survey 1999–2008	(1) To investigate the association of BC with AL scores, by comparing AL scores of those with a history of BC to those without, stratified by race. (2) To evaluate whether the interaction between race and BC predicts elevated AL levels.	National Health and Nutrition Examination Survey (NHANES) 1999–2008, N = 4875	Cross-sectional	AL	Socio-economic/ Psychosocial/ Lifestyle: Black versus White women Inflammatory markers: Allostatic load [i.e., nine components and their corresponding cutoffs: SBP ≥ 140 mmHg, DBP ≥ 90 mmHg, heart rate ≥ 90 bpm, total cholesterol level ≥ 240 mg/dL, (v) HDL < 50 mg/dL, BMI ≥ 30 HbA1C ≥ 6.4%, CRP > 3 mg/ L, and albumin < 4 g/dL]	The study found a positive association between AL and BC risk in Black women (OR 2.08, 95% CI 1.02 − 4.22), but not in White women. Black women with a history of BC had a 16.4% greater likelihood of having higher AL compared to White women. In Black women having a history of BC was associated with an increased CRP and low LDL cholesterol.
Shen 2022	Neighborhood disadvantage and biological aging biomarkers among BC patients	To evaluate the relationship between neighborhood disadvantage and AL, TL, and global DNA methylation in leukocytes among women with BC.	From a 2012 BC epidemiological study at The University of Texas, M. D. Anderson Cancer Center, N = 906	Cross-sectional	AL, TL, and telomerase activity in leukocytes, global DNA methylation in leukocytes	Socio-economic/ Psychosocial/ Lifestyle: Neighborhood disadvantage, BMI, physical activity, alcohol consumption, and tobacco use Inflammatory markers: AL [i.e., SBP, DBP, HDL, LDL, total cholesterol, triglycerides, waist circumference, BMI, glucose, HbA1C, albumin, eGFR, creatinine, CRP, IL-6, rest heart rate, and the history of taking medication to control metabolic diseases and hypertension Epigenetic: TL, telomerase activity in leukocytes, global DNA methylation in leukocytes	Patients from higher disadvantaged neighborhoods (which also had a higher proportion of non-Hispanic Black individuals) had significantly higher median AL levels (OR 1.35, 95%CI 1.09–1.74) and lower median global DNA methylation levels (OR 0.40, 95%CI 0.27–0.60), however no significant association was found between ADI and TL. These associations were significant even after adjusting for demographic variables and BMI, physical activity, alcohol consumption, and tobacco use (AL: OR 1.20, 95% CI 1.02–1.87; global DNA methylation: OR 0.49, 95% CI 0.33–0.65).
Zhao 2021	Allostatic score and its associations with demographics, healthy behaviors, tumor characteristics, and mitochondrial DNA among BC patients	To explore the associations between the AL score at the time of diagnosis and patient demographics, healthy behaviors, and aggressive breast tumor characteristics	Participants from an ongoing BC study at the University of Texas M. D. Anderson Cancer Center, N = 472	Cross-sectional	Aggressive breast tumor characteristics based on (1) ER status (2) tumor stage: late (III) vs early (I&II); (3) tumor grade: poorly (grade 3) vs moderately and well differentiated (grade 1/2); (4) tumor size: large (≥ 2 cm) vs small (< 2 cm); and mitochondrial DNA copy number	Socio-economic/ Psychosocial/ Lifestyle: Black versus non-Hispanic White women Cancer-related: Aggressive breast tumor characteristics	AL was higher in Black and Hispanic women, those with lower levels of physical activity and those with greater alcohol consumption. Higher AL was found to be significantly associated with an increased odds of having poorly differentiated tumors (OR 1.40, 95% CI 1.28–1.62) and ER- BC in Black (OR 1.56, 95% CI 1.02–2.36). Certain mitochondrial DNA variants were also associated with greater AL.
Aghaee 2022	Everyday discrimination and TL in a multiethnic cohort of BCSs	To explore the relationship between two variables everyday discrimination and TL.	Equality in BC Care study (identified from the population-based Greater Bay Area Cancer Registry (GBACR, part of the NCI SEER program and the California Cancer Registry), N = 58	Cross-sectional	Race-Related Differentially Expressed Genes in XIAP-Driven ASR Gene Set	Socio-economic/ Psychosocial/ Lifestyle: marital status, education, above poverty level income, experiences of discrimination Epigenetic: race-related differentially expressed genes	Compared to their reference categories, patients who experienced higher levels of discrimination were more likely to be married, have at least a high school diploma, be above the federal poverty level, have stage II or HER2 + BC. Higher discrimination levels were associated with longer TLs (regression coefficient = 1.04, 95% CI 1.01–1.07). The shortest telomere length was found in AA women (43% shorter compared to non-Hispanic Whites). Significant predictors of TL were discrimination, BC subtype, and race.
Chen 2023	An epigenome-wide analysis of SEP and tumor DNA methylation in BC patients	To conduct an epigenome-wide analysis of two of the commonly assessed SEP factors, total household income and educational attainment, using tumor DNA methylation data.	Women's Circle of Health Study (WCHS) recruited from Mount Sinai School of Medicine (MSSM) in New York, and The Cancer Institute of New Jersey (CINJ), N = 694	Cross-sectional	DNA methylation using CpG sites	Socio-economic/ Psychosocial/ Lifestyle: income Epigenetic: DNA Methylation	This study found 25 CpG sites in the genome of differing significance linked to household income and consistent across different racial groups and estrogen receptor status, however none were linked to educational attainment. The two most important CpG sites were in genes involved in stress response, inflammation, and immune function. Higher income was linked to lower methylation of these sites, suggesting a potential association between socioeconomic factors and gene expression.
Sánchez-Díaz 2021	What mediates the racial/ethnic disparity in psychosocial stress among BC patients?	Consider the stress of female authority in managerial occupations and the stress of caring in professional occupations as gendered stress processes that can increase BC risk via prolonged exposure of breast tissue to the antiapoptotic and proliferative effects of chronically elevated cortisol (in White women)	The BC Care in Chicago (BCCC), a population-based, cross-sectional study of newly diagnosed BC patients, N = 989	Cross-sectional	Psychosocial stress (Cohen Perceived Stress Subscale), loneliness (UCLA Felt Loneliness Scale), psychological Consequences (Cockburn Psychological Consequences Scale), SEP, and social support	Socio-economic/ Psychosocial/ Lifestyle: SEP and social support Stress: Psychosocial stress, loneliness, psychological consequences, SEP, and social support	Patients who were younger, Hispanic, or non-Hispanic Black, and of low SEPs, reported higher rates of psychosocial stress. Later stage at diagnosis was linked to greater perceived stress and psychological consequences. Additionally, having greater unmet support needs was associated with higher psychosocial stress. The association with race/ethnicity was reduced or eliminated when controlling for SES, and path models revealed the racial disparities in psychosocial stress can be attributed to SES.
Sheppard 2014	The importance of contextual factors and age in association with anxiety and depression in Black BC patients	To identify contextual and healthcare process of care factors associated with anxiety and depression levels in newly diagnosed Black patients with BC to aide providers in identifying and addressing women who require the greatest support.	AA/Black women from clinic sites with invasive non-metastatic BC, N = 82	Cross-sectional	Symptoms of anxiety and depression were measured using the Hospital Anxiety and Depression Scale (HADS), contextual factors, process of care factors	Socio-economic/ Psychosocial/ Lifestyle: Age, medical mistrust, barriers to care Depression/Anxiety: Hospital Anxiety and Depression Scale (HADS)	In this sample of Black women, roughly 12% and 10% of women had clinically significant levels of anxiety, and significant depression levels, respectively. A third of women had borderline significant levels of depression or anxiety. Higher depression and anxiety were associated with more medical mistrust and greater barriers to care. Medical mistrust, age, and a positive attitude were significant predictors for both depression and anxiety.
Vin-Raviv 2013	Racial Disparities in Posttraumatic Stress After Diagnosis of Localized BC: The BQUAL Study	To investigate the prevalence, racial disparities, and potential risk factors of PTSD symptoms among women with BC,	BC Quality of Care Study (BQUAL), N = 1479	Cross-sectional	PTSD symptoms assessed at three time points using the Impact of Event Scale (IES)	Socio-economic/ Psychosocial/ Lifestyle: PTSD symptoms: recurrent thoughts, nightmares about the cancer diagnosis, avoidance of reminders of cancer, and feelings of hyperarousal Stress: IES	This study found that almost 25% of patients reported symptoms consistent with PTSD shortly after diagnosis. Black (OR 1.48 vs White, 95% CI 1.04–2.10) and Asian OR 1.69 vs White, 95% CI 1.10–2.59), as well as younger women more likely to experience PTSD compared to White women and women who were older. The most common symptoms reported included recurrent thoughts, nightmares about the cancer diagnosis, avoidance of reminders of cancer, and feelings of hyperarousal.
Armour-Burton 2020	Black Feminist Thought A Paradigm to Examine BC Disparities	To describe the essence of life within intersectionality between identities of race, gender, and social class among a group of AA women with BC, and to investigate the impact of this intersectionality in psychological well-being.	AA women recruited from support groups, churches, and nursing organizations across the US, N = 10	Cross-sectional, Qualitative	N/A	Socio-economic/ Psychosocial/ Lifestyle: altruism, marginalization (oppressive behavior leading to decreased access and feeling powerless), existential invisibility (feeling ignored despite being vitally important), and silent strength (a need for strength driven by historical struggle)	In this qualitative study of AA women with BC, four main themes emerged: altruism, marginalization (oppressive behavior leading to decreased access and feeling powerless), existential invisibility (feeling ignored despite being vitally important), and silent strength (a need for strength driven by historical struggle).
Mollica 2015	Transition From Patient to Survivor in AA BCSs	To examine the experience of AA women as they transition from BC patient to survivor.	Community-based AA women aged 35 to 75 years in Charleston, South Carolina, and Buffalo, New York, who had completed treatment for primary BC between 6 and 18 months prior, N = 15	Cross-sectional, Qualitative	N/A	Socio-economic/ Psychosocial/ Lifestyle: faith, emotional needs, physical function, guidance needs after treatment	This qualitative study identified four main themes: perseverance through struggles supported by reliance on faith, persistent physical issues, anticipatory guidance needed after treatment, and emotional needs as important as physical
Madison 2021	Distress Trajectories in Black and White BCSs: From Diagnosis to Survivorship	To examine distress trajectories after diagnosis of breast through survivorship in Black and White women	Ohio State University cancer clinics from a parent study, N = 195	Longitudinal Cohort, Follow up = 6- and 18-months post-treatment	Perceived stress (Perceived Stress Scale short form), anxiety and depressive symptoms (CES-D scale), Beck Anxiety Inventory, Inflammation assay: CRP, TNF-α, IL-6, IL-1β, IL-8	Socio-economic/ Psychosocial/ Lifestyle: Black compared to white patients Depression/Anxiety: Anxiety and depressive symptoms Stress: Perceived stress Inflammatory markers: CRP, TNF-α, IL-6, IL-1β, IL-8	This study found that perceived stress trajectories differed by race, with Black patients not experiencing improvements and instead having high psychological distress over time even after months of recovery and completing treatment. There were no significant differences in overall levels or trajectories of inflammatory markers like CRP level between Black and White patients.
Crane 2019	Trajectories of Depression and Anxiety in Latina BCSs	To identify subgroups of Latina BCSs with unique trajectories of depression and anxiety and examine predictors associated with these subgroups	Latina women receiving treatment for BC and their designated informal cancer caregivers recruited for participation in three RCTs, N = 293	Longitudinal Cohort, Follow up = 16 weeks	Depression [CES-D scale] and anxiety [Spielberger State-Trait Anxiety Inventory (STAI) and PROMIS-Anxiety scale]	Socio-economic/ Psychosocial/ Lifestyle: Sociodemographic characteristics (i.e., age, rurality, income, employment, marital status, education level) social well-being (sub-scale of the QOL Instrument–BC) Depression/Anxiety: CES-D, STAI, PROMIS-Anxiety	This study identified three depression trajectories in Latina BCSs: 78% with low/moderate stable depression, 7% with high-improving depression, and 15% with high-stable depression. Age, social, well-being, chemotherapy, and baseline depression were significant predictors of depression trajectories Additionally, three anxiety trajectories were identified: 73% with low-stable anxiety, 18% with high-improving anxiety, and 9% with high-worsening anxiety, with baseline anxiety being the only significant predictor.
Pudrovska 2013	Higher-status occupations and BC: A life-course stress approach	To explore the effect of occupation on BC incidence and while considering the stress of female authority in managerial occupations, the stress of caring in professional occupations, and gendered stress processes.	The Wisconsin Longitudinal Study (WLS) who participated in 1975, 1993, and 2004, and women who died of BC any time after 1975, N = 3682	Longitudinal Cohort, Follow up = 54 years (1957–2011)	BC incidence	Socio-economic/ Psychosocial/ Lifestyle: professional status/attainment Cancer-related: BC incidence Inflammatory markers: cortisol	This study found that women in professional and managerial occupations had a significantly higher risk of developing BC (HR 1.57, 95% CI: 1.12–2.18) compared to women in lower-status occupations and housewives likely due to demanding work environments that lead to hormonal dysregulation and increased exposure to stress hormones like cortisol.
Xing 2020	Pre-diagnostic AL as a Predictor of Poorly Differentiated and Larger Sized BCs among Black Women in the Women's Circle of Health Follow-Up Study	To explore the association of pre-diagnostic AL measures with several unfavorable tumor clinicopathologic features, namely invasive tumor behavior, higher tumor grade, larger tumor size, and ER- among women with BC	AA/Black Women from the Women's Circle of Health Follow-Up Study (WCHFS) and New Jersey State Cancer Registry, N = 638	Prospective Cohort, Follow up = 2- and 3-year post-diagnosis	Unfavorable tumor characteristics defined based on four clinicopathologic features: (i) tumor behavior [invasive (stages I, II, and III) vs. noninvasive (stage 0 or DCIS)]; (ii) tumor grade [poorly differentiated (grade 3) vs. well and moderately differentiated (grades 1 and 2)]; (iii) tumor size (2 cm vs. <2 cm); and (iv) ER status	Cancer-related: Unfavorable tumor characteristics	This study found that Black women with higher AL before their diagnosis were more likely to develop poorly differentiated, faster growing, and larger sized breast tumors; this relationship remained significant even after adjusting for other known risk factors for BC.
Slattery 2014	Diet and lifestyle factors interact with MAPK genes to influence survival: the BC Health Disparities Study	To examine the association between variants in MAPK genes and survival after diagnosis with BC in NHW and US Hispanic/NA women, a genetically admixed population. Hypothesized that certain diet and lifestyle factors associated with activation of this signaling pathway would interact with genetic variation in MAPK genes to alter survival in women diagnosed with BC.	4-Corners BC Study (4-CBCS) and the San Francisco Bay Area BC Study (SFBCS), N = 2337	Retrospective Case-Control, time = 1997–2004	Survival (in months)	Socio-economic/ Psychosocial/ Lifestyle: age, disease stage, diabetes, smoking, vitamin C intake, alcohol consumption, menopausal status Cancer-related: Survival Epigenetic: MAPK genes, NA ancestry	Women with low Native-American ancestry exhibited several MAPK genes associated with both BC-specific and all-cause mortality. Even after adjusting for disease stage, diet and lifestyle factors influenced survival across all ethnic groups specifically greater age, advanced disease stage, a history of diabetes, and lower vitamin C intake for both NHW and Hispanic/NA women; cigarette smoking and higher BMI for NHW women's and premenopausal status and long-term alcohol consumption affected Hispanic/NA women. Genetic and lifestyle interactions, particularly with MAPK genes like MAP2K1, MAP3K9, and MAPK12, played a role in mortality risks, with stronger associations in women with low NA ancestry
Lawrence 2023	Stressful Life Events, Social Support, and Incident BC by ER Status	To investigate the relationship between stressful life events and BC incidence by ER status in postmenopausal women and to understand the link between chronic psychosocial stress and incident BC vary by ER status.	Women's Health Initiative Observational Study enrolled from 40 different clinic sites (WHI-OS), N = 76,951	Prospective Cohort, follow up = 15–20 years depending on when each participant enrolled.	Incident BC	Socio-economic/ Psychosocial/ Lifestyle: stressful life events Stress: number of stressful life events (questionnaire adapted from the Beta-Blocker Heart Attack Trial) Cancer-related: BC incidence	This study found no independent association between the number of stressful life events and overall risk of developing cancer. However, it did find that women who experienced higher number of stressful like events had higher risk (Quartile 4 vs. Quartile 1; HR 1.30; 95% CI, 1.01–1.68; P_trend = 0.050) of developing ER- BC.
Barber 2021	Neighborhood disadvantage and individual-level life stressors in relation to BC incidence in US Black women	To investigate the association of individual-level and neighborhood-level psychosocial stress factors with risk of ER+, ER- and TNBC in Black women.	Black Women's Health Study (BWHS), a prospective cohort study of women from across the US who self-identified as Black, N = 57,442	Prospective Cohort, Follow up = every 2 years	Incident invasive BC	Socio-economic/ Psychosocial/ Lifestyle: neighborhood characteristics, early life stress/abuse, education Cancer-related: BC incidence	Certain individual and neighborhood- level factors are associated with increased risk of BC, these include marital status, education level, and neighborhood SES. Black women who live in disadvantaged neighborhoods have a greater risk of ER- BC (HR 1.26 95 CI 1.00-1.58) compared to those living in higher advantaged neighborhoods. Early life stressors such as childhood sexual abuse (sexual assault ≥ 4 times vs. no abuse: HR 1.35, 95% CI 1.01–1.79) and marital status (married/living together vs. single: HR 1.29, 95% CI 1.08–1.53) were linked to an increased risk of ER + BC but did not show a significant association with ER- BC.
Obeng-Gyasi 2023	Association of AL With All-Cause Mortality in Patients with BC	To examine the association between AL and all-cause mortality in patients with BC.	Ohio State University Cancer Registry, N = 2869	Retrospective cohort, time = 2012–2020	All-cause mortality	Socio-economic/ Psychosocial/ Lifestyle: marital status, insurance coverage Cancer-related: All-cause mortality	Higher AL was observed in patients who were older, single, government insured (Medicaid aRR 1.14; 95% CI, 1.07–1.21; Medicare aRR 1.11, 95% CI 1.03–1.19) non-Hispanic Black (aRR 1.11, 95% CI 1.04–1.18), and with fewer comorbidities. Furthermore, higher AL was linked to increased risk of all-cause mortality even after adjusting for covariates (HR 1.46, 95% CI 1.11–1.93).
AlAbo 2022	ASR genes associated with BC subtypes and survival outcomes reveal race-related differences	To investigate the expression profile of the XIAP-driven ASR gene set in BC subtypes, identify race-related differentially expressed genes within this gene set, and determine associations between ASR gene expression and poor survival outcomes.	Data generated by the Cancer Genome Atlas Program (TCGA) Research Network, N = 1222	Retrospective cohort, time = up to 2021	BC subtypes	Cancer-related: BC subtypes	This article focuses on the ASR pathways and their potential as biomarkers for treatment strategies to attenuate the racial disparities in BC outcomes. It suggests that disparities in BC outcomes, particularly in self-identified AA women, may be associated with factors inducing chronic stress at various levels, including societal, neighborhood, institutional, and possibly individual levels.
*aRR: adjusted relative ratio; AA: African American; ADI: area deprivation index; ALP: alkaline phosphatase; ASR: adaptive stress response; BC: breast cancer; BCS: breast cancer survivor; BMI: body mass index; BUN: blood urea nitrogen; bpm: beats per minute; CES-D: Center for Epidemiologic Studies-Depression; CI: Confidence Interval; CRP: C-reactive protein; DCIS: ductal carcinoma in situ; DBP: diastolic blood pressure; eGFR: estimated glomerular filtration rate; ER: estrogen receptor; HbA1C: glycosylated hemoglobin; HDL: high density lipoprotein; HR: hazard ratio; ICE: index of concentration at the extremes; IL: interleukin; NA: Native American; NHW: non-Hispanic White; OR: Odds Ratio; PTSD: posttraumatic stress disorder; QOL: quality of life; RCT: randomized controlled trial; SBP: systolic blood pressure; SEER: Surveillance Epidemiology End Results; SEP: socioeconomic position; TL: telomere length; TNBC: triple-negative breast cancer; WBCC: white blood cell count

Study Characteristics

The initial search yielded 1256 Embase, 463 PubMed, 424 Web of Science, 231 PsycINFO, 64 Scopus, and 60 Cochrane references. After removing 1058 duplicates, 1440 titles and abstracts were screened, and 148 references were included for full-article review. After applying the inclusion and exclusion criteria, 30 articles remained for comprehensive analysis (Fig. 1). Among the 30 articles reviewed, 21 were observational and largely employed cross-sectional or cohort study designs that utilized data from population-based registries, clinical registries, clinic settings, and cancer registries (summarized in Table 2). The remaining nine were reviews published between 2013 and 2023 (summarized in Table 3).

Table 3

Summary of review articles included in this review (N = 8)
Study ID	Title	Aims	Inclusion criteria	Number of studies included	Study design	Summary of findings
Colon-Otero 2020	The Biology of BC Disparities in Hispanics: Current Knowledge, Gaps, and Research Opportunities	To explore BC outcomes among the Hispanic population in the U.S. and provide an overview of the current knowledge regarding BC in Hispanics	N/A	N/A	Narrative review	This review suggests Hispanic women have a lower incidence of BC, are diagnosed at younger ages and with more aggressive tumor subtypes, and higher mortality compared to non-Hispanic white women. Contributing factors include low SES impacting healthcare access and lifestyle choices, genetic factors that are less established, and epigenetic factors such as early-life and environmental exposures that influence gene expression. Other proposed mechanisms are chronic stress and inflammation, as well as childhood obesity, which is more common in Hispanics.
Joshi 2022	Epigenetic Determinants of Racial Disparity in BC: Looking Beyond Genetic Alterations	To discuss the current state of knowledge in epigenetic differences between Black and White women with BC and describe environmental factors that contribute to these epigenetic changes.	N/A	N/A	Narrative review	This review highlights differences in epigenetic patterns between Black and European American women and the potential impact these patterns have on racial disparities in BC incidence and outcomes. The review highlights the abundance of research that has explored DNA methylation differences and the lack of research in histone modification patterns. It also discusses the higher basal found epigenetic changes in Black women and explores the dietary habits, exposure to pollutants, and psychosocial stress, which contribute to epigenetic changes and mediate racial disparities in BC outcomes, as well as stresses the importance of systemic changes to address structural inequalities.
Linnenbringer 2017	Black-White Disparities in BC Subtype: The Intersection of Socially Patterned Stress and Genetic Expression	To elucidate disparities in BC subtype using weathering hypothesis, review existing literature on BC risk, and present recent evidence on structural and neighborhood factors.	Peer-reviewed studies that focused on stress biology, BC epidemiology, and health disparity, specifically racially patterned structural, residential, and individual exposures that are theoretically or empirically linked to ER- BC risk factor	N = 14	Systematic review	This review emphasizes the influence of social stressors, including perceived social isolation, segregation, and racial discrimination, on HR- BC risk. The conceptual model proposed by the authors refocuses attention from genetic risk factors to instead highlight the impact of structurally embedded chronic stressors on HR- BC risk. The review also examines the relationship between BC risk and psychological stress, physiological responses, behavioral modifications, and genetic alterations.
Obeng-Gyasi 2021	AL: a framework to understand BC outcomes in Black women	To develop a framework using AL to understand and measure BC disparities from diagnosis through survivorship.	N/A	N/A	Commentary	This commentary focuses on disparities in BC outcomes in Black patients. The authors developed a conceptual framework to understand these disparities using AL. It highlights the impact of systemic inequality on clinical outcomes and the chronic stressors that may contribute to physiological dysregulation.
Obeng-Gyasi 2022	AL and BC: a Systematic Review of the Literature	To review and present the literature on AL among BC patients, identify the gaps in current research, and highlight opportunities for future research.	Empirical studies available in English focused on BC and AL in the US and internationally	N = 8 (n = 3 included in our review)	Systematic review	Most studies were in the USA, particularly focused on Black women, with various outcomes including AL, tumor characteristics, mitochondrial DNA copies, patient-reported outcomes, and factors affecting metastatic BC. Among women with a history of BC, high AL is associated with poorly differentiated tumors and being Black. For AL, the most used cardiac physiologic biomarkers were SBP and DBP. BMI was the most used metabolic biomarker, and CRP was the most used immune biomarker.
Saini 2019	Disadvantaged neighborhoods and racial disparity in BC outcomes: the biological link	This review sheds light on the probable biological links between neighborhood disadvantage and BC risk, emphasizing stress reactivity and inflammation, epigenetics, and telomere length in response to adverse neighborhood conditions.	N/A	N/A	Narrative review	This review discusses the influence of chronic stress caused by neighborhood disadvantage on inflammation and its association with BC risk. It discusses the biological responses to stress, such as hormones that suppress cellular immune responses and proinflammatory cytokines released during stress, such as CRP and IL-6, that encourage tumor initiation and progression. The review also discusses environmental and behavioral factors such as poor diet and air pollution that are associated with disadvantaged neighborhoods. Lastly, the review expands on telomere length as a promising biomarker for BC risk in individuals living in disadvantaged neighborhoods.
Tsai 2020	Systematic review of depressive, anxiety, and post-traumatic stress symptoms among Asian American BCS	This review examines psychopathology symptoms in Asian American BCSs, exploring the prevalence, contributing factors, and effective interventions.	Empirical, peer-reviewed papers in English that included studies with women ≥ 18 who have Asian heritage living with BC in the USA BC focused on psychopathology symptoms (e.g., depressive symptoms, anxiety symptoms, post-traumatic stress symptoms)	N = 16	Systematic review and meta-analysis	This review examined the literature for studies on mental health symptoms among Asian American BCSs. It found that these women have moderate to elevated levels of depression, anxiety, and post-traumatic stress symptoms. Additionally, higher levels of acculturation are generally associated with lower levels of depression and anxiety in these women. Higher levels of intrusive thought and more mental health symptoms were associated with greater social constraints.
Williams 2016	Understanding and Effectively Addressing BC in Black Women: Unpacking the Social Context	To review social factors like SES and stress throughout a woman's life and the interaction with biological factors and how they contribute to racial disparities in BC.	N/A	N/A	Narrative review	This review highlights the higher incidence of BC that is more aggressive before age 40 in Black women and their risk for lower survival rates compared to White women. It also emphasizes that these disparities are not only explained by biological factors but are influenced by SES, systemic racism, chronic stress, unhealthy behaviors, and limited access to resources. This impact starts from early childhood and continues through adulthood.
Yap 2023	Outcomes in BC - does ethnicity matter?	To summarize the BC outcomes among different ethnicities or populations reported in the literature, as well as the drivers of these disparities, focusing on the latest and the larger studies.	N/A	N/A	Narrative/ review	In determining BC outcomes, ethnicity matters. Other drivers of cancer, including the ability to evade the immune system, promote tumor-inducing inflammation, disrupt cellular metabolism, undergo epigenetic changes, and exhibit diverse microbiomes, may also be contributing to disparities in BC outcomes. However, due to the complex interplay between host, tumor biology, and socioeconomic determinants, it is challenging to differentiate between internal and external drivers of BC, which also explains why this remains poorly understood.
AL: allostatic load; BC: breast cancer; BCS: breast cancer survivor; CRP: C-reactive protein; HR: hormone receptor; IL: interleukin; PTSS: posttraumatic stress symptoms; SES: socioeconomic status; TL: telomere length

Allostatic Load: The Biological Marker of Stress

Eight studies explored AL as a biological marker of stress in patients with breast cancer from different racial groups. Chen et al.¹⁸ found that higher AL scores, calculated using biomarkers that were routinely collected as part of preoperative work-up for breast cancer surgery and included heart rate, SBP and DBP, BMI, alkaline phosphate (ALP), glucose, albumin, white blood count, blood urea nitrogen (BUN), and creatinine, were associated with lower index of concentration extremes (ICE) values. Their results suggest that high AL is associated with living in more deprived neighborhoods. Additionally, women from segregated neighborhoods which is linked to Black race, underinsurance, single marital status, and smoking had greater odds of high AL. The association between AL and racialized economic segregation remained statistically significant, even after adjusting for demographic, clinical, and treatment characteristics.¹⁸ Obeng-Gyasi et al¹⁹ used the same method for calculating AL scores in women with breast cancer and found that women with higher AL were more likely to be older, single, underinsured, and non-Hispanic Black. Women with high AL also experienced increased all-cause mortality.¹⁹ Several other studies using AL observed that Black women with breast cancer tend to have higher AL scores compared to their White counterparts, even after adjusting for lifestyle factors.^19–21 Moreover, Black women with higher AL before diagnosis were likely to exhibit unfavorable tumor characteristics, including poor differentiation, rapid growth, and large size.²²

Epigenetics and Genetics: A Potential Contributor to Racial Disparities in Breast Cancer

The second group of studies identified in our review highlighted DNA modifications that influence gene expression may contribute to racial disparities in breast cancer. Notably, Black women tend to exhibit higher basal epigenetic changes that are potentially influenced by environmental factors, such as diet, pollutants, and psychosocial stress, predisposing them to aggressive breast cancer and poor outcomes.²³ Variations in methylation at CpG sites link stress response and immune function to socioeconomic factors, such as household income.²⁴ Furthermore, Aghaee et al²⁵ found a correlation between social stressors (e.g., discrimination) and an increased risk of aggressive breast cancer.²⁵ Moreover, Black women with breast cancer demonstrate shorter telomere lengths, a marker of cellular aging, compared to Hispanic and White women.²⁵ This study found that for every one-unit increase in Everyday Discrimination Score (EDS), telomeres were 4% longer, and Black women had an average telomere length that was 43% shorter than those of non-Hispanic White women.²⁵ Chronic stress, systemic racism, unhealthy behaviors, and limited access to resources that start from early childhood also contribute to a higher incidence of aggressive breast cancer and lower survival rates in Black women compared to White women.²⁶ The influence of chronic stressors at institutional, societal, and individual levels is evident in the expression of adaptive stress response (ASR) genes. One of these genes involved in the ASR pathway, MAPK (specifically MAP2K1, MAPK3K9, and MAPK12), was associated with breast cancer-specific and all-cause mortality among women with low Native American genetic background.²⁷ Exploring the complex interplay between differential DNA methylation, other epigenetic alterations, genetics, and biological markers of aging (e.g., telomere length) that exist across different racial and ethnic groups is important for establishing personalized biomarkers to improve breast cancer diagnosis and prevent progression.²³

Social Determinants of Health and Psychosocial Patterns

A third group of studies identified in our review focused on self-reported exposure to stressors and breast cancer outcomes among women of different races. Investigating the social context of women with breast cancer revealed an intricate interplay between social determinants of health and psychosocial experiences. Although one study did not find an independent association between overall life stress and breast cancer risk, it identified a specific link between high life stress and increased risk of developing estrogen receptor-negative breast cancer. ²⁸ This finding suggests a potential role for hormonal dysregulation due to chronic life stress in the development of aggressive breast cancer subtypes. In this study, the degree of social support did not modify the relationship between stressful life events and breast cancer risk.²⁸ Moreover, data from Barber, et al.¹⁰ demonstrated that Black women who resided in disadvantaged neighborhoods had a greater risk of estrogen receptor-negative breast cancer. However, in contrast to the prior study, early life stressors such as childhood abuse and marital status did not show significant associations with estrogen receptor-negative breast cancer.¹⁰

Psychosocial stress disproportionately affects women from minoritized racial and ethnic groups who are more likely to live in disadvantaged neighborhoods, be younger and of lower socioeconomic positions.²⁰ Women diagnosed at advanced stages reported higher perceived stress and psychological consequences, which were linked to greater unmet support needs, including emotional, financial, informational, practical, and spiritual needs. Unmet financial and practical needs played an extensive role in mediating racial and ethnic disparities in psychosocial stress.²⁹ Furthermore, age, social well-being, and baseline mental health predicted depression trajectory in a study of Latina breast cancer survivors with distinct depression and anxiety trajectories.³⁰ Black women with breast cancer also reported higher clinically significant levels of depression and anxiety; however, these psychological challenges were linked to increased medical mistrust and greater barriers to accessing care.³¹ Asian American breast cancer survivors reported experiencing moderate to high levels of depression, anxiety, and post-traumatic stress, and those with higher acculturation and social support generally reported lower levels of depression.³² These findings collectively highlight the interrelatedness of psychosocial experiences within the broader context of societal and individual-level factors in understanding racial and ethnic disparities in breast cancer outcomes.

This review synthesized the current literature on the relationship between race, stress, and breast cancer. Individual-level stressors, neighborhood-level stressors, and societal factors interact and influence breast cancer outcomes in racially and ethnically diverse populations. The findings of our review highlight the complex interplay between these multilevel factors, emphasizing the need for a comprehensive approach to understand and address racial disparities in breast cancer.

One of the key takeaways is the underappreciated role of chronic psychosocial stress in breast cancer. Studies explored conceptual models, such as stress exposure and weathering frameworks, to illustrate how social determinants of health can lead to chronic stress and influence biological processes. For instance, research suggests that AL is significantly higher in Black women than in White women even after adjusting for lifestyle factors,^19–21 pointing to a potential biological link between social stress and racial disparities in breast cancer outcomes.

Furthermore, epigenetic modifications and telomere length have emerged as potential contributing factors to the interplay between social stress and breast cancer. Studies demonstrated higher epigenetic changes^23,24 and shorter telomeres²⁵ in Black women than in White women. These biological markers may be influenced by social and societal stressors, including discrimination and limited access to resources, potentially increasing susceptibility to aggressive breast cancer subtypes²⁹ and poor outcomes.²⁶

Implications

Our review highlights the need for multilevel interventions that target stress across individual, neighborhood, and societal levels. Potential strategies include individual-level stress management techniques, such as mindful meditation and resilience coaching, and neighborhood-level improvements to community resources. At the societal level, interventions should address policies and practices that perpetuate racial discrimination, poverty, and limited access to healthcare services.

Future research would benefit from inclusion of standardized outcome measures, such as stress perception and quality of life assessments, alongside clear metrics for breast cancer incidence and population-specific tools to appropriately capture social determinants of health. Standardizing AL assessment protocols is essential and can be achieved by optimizing the sets of biomarkers included and the methods used to quantify AL. Rigorous validation of AL tools in diverse populations is also needed. Prioritizing equitable access to breast screening tools and appropriate insurance coverage will be essential. These approaches acknowledge the realities and unique experiences of diverse populations while maintaining consistency to allow for meaningful comparisons across studies. Longitudinal studies are needed to investigate how social and environmental stressors dynamically alter epigenetic, telomere-related, and adaptive stress mechanisms over the course of life. Future studies should also assess the utility of epigenetic and telomere markers as predictive and prognostic biomarkers for breast cancer outcomes. In addition, exploring the possibility of targeting stress response pathways is necessary to develop novel therapies that could improve treatment outcomes.

Limitations

This review has limitations, including the exclusion of literature published in languages other than English and studies conducted outside the US. This may have excluded relevant studies published in other languages and countries, potentially introducing publication bias. Our review focused on observational studies (which cannot support causation) and included various methodologies, limiting our ability to directly compare findings across studies. Additionally, most studies have focused on comparisons between Black and White women with breast cancer, with less emphasis on other racial and ethnic groups. Because this review focused on breast cancer, the findings may not be generalizable to different cancer types, as the relationship between stress and other cancers may differ. Lastly, measures of systemic racism were not consistently utilized or fully incorporated into the reviewed studies, making it difficult to assess its independent contribution to breast cancer disparities.

Although AL can be used as a framework to understand racial disparities in breast cancer outcomes, its application faces several limitations. The operationalization of AL across studies has been inconsistent because of a lack of consensus on the optimal biomarkers to be included in AL assessments. Second, the methods to quantify AL [also inconsistent, and even when studies used similar biomarker components, they applied different weights or thresholds to define high versus low AL.^33,34 Lastly, a lack of optimization and validation of AL among diverse populations poses a significant challenge hindering generalizability and comparison across studies.³³

This review provides a comprehensive overview of the current evidence on the complex interplay between social stressors, biological responses, and racial and ethnic disparities in breast cancer outcomes. The findings highlight the significant, yet often overlooked, role of chronic psychosocial stress in the disproportionate burden of breast cancer faced by marginalized racial and ethnic groups. Further exploration and evaluation of multilevel, targeted interventions and personalized biomarkers are needed to inform more effective and equitable approaches to breast cancer prevention.

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Availability of data and materials

This review article does not include any new data generated by the authors. All data discussed in this manuscript are derived from publicly available sources and previously published studies, which are cited appropriately in the references section.

Competing Interests

The authors declare that they have no competing interests.

Funding

Dr. Eltoum is supported by grant T32HS013852 from the Agency for Healthcare Research and Quality (AHRQ). Dr. Rocque is supported by Daiichi Sankyo.

Acknowledgements

Not applicable

Clinical trial number: not applicable.

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Race, Stress, and Breast Cancer: A Scoping Review

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Abstract

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Background

Methods

Search Strategy and Study Selection

Analysis

Results

Study Characteristics

Allostatic Load: The Biological Marker of Stress

Epigenetics and Genetics: A Potential Contributor to Racial Disparities in Breast Cancer

Social Determinants of Health and Psychosocial Patterns

Discussion

Implications

Limitations

Conclusion

Declarations

References

Additional Declarations

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