Healthcare Factors for Obtaining a Mammogram in Latinas With a Variable Mammography History

Breast cancer is the leading cause of cancer death for Latinas, and Latinas are more likely than non-Latina Caucasians to be diagnosed with breast cancer at a later stage and to die from the disease (American Cancer Society [ACS], 2015; DeSantis, Ma, Bryan, & Jemal, 2014). The causes of this disparity in late-stage diagnosis have many origins; however, Latinas’ lower adherence to screening mammography guidelines compared to other races and ethnicities remains a major contributing factor (ACS, 2015). Healthcare factors, such as having health insurance and a usual source of care, appear to be important and may contribute to behavioral disparities (Gonzalez et al., 2012; Jerome-D’Emilia & Suplee, 2015; Nuño, Castle, Harris, Estrada, & Garcia, 2011). The impact of healthcare factors on women’s thoughts about mammograms may underlie these associations, based on psychosocial research concerning conscious thought and behavior (Baumeister, Masicampo, & Vohs, 2011). However, despite interventions to address these factors, nonadherence to guidelines persists (Terán, Baezconde-Garbanati, Márquez, Castellanos, & Belkic, 2007).

One of the issues limiting the impact of interventions to improve adherence to screening mammography guidelines among Latinas is how previous research informing these interventions compares groups at different stages of screening mammography adoption (never, initiation, maintenance). Although previous studies have shown that Latinas with a prior history of obtaining a mammogram are more likely to think about and plan to obtain a mammogram in the future, the barriers and facilitators at each stage may be different (Gonzalez et al., 2012; Schueler, Chu, & Smith-Bindman, 2008). For example, knowledge barriers to initiating screening mammography may include not knowing one’s breast cancer risk, whereas knowledge barriers to maintaining screening mammography may include not knowing that a lifetime history of one mammogram is insufficient to detect all breast cancer during one’s life (Austin, Ahmad, McNally, & Stewart, 2002). However, previous research typically only compares women with a lifetime history (ever) to women without a lifetime history of screening mammography (never) to study initiation of screening mammography or compares women with a history of a mammogram in the past two years (recent) to women with a mammogram more remote than the past two years (not recent) to study maintenance of screening mammography (Cronan et al., 2008; Kapp, Walker, Haneuse, & Yankaskas, 2011; Lopez-McKee, McNeill, Bader, & Morales, 2008). Most studies do not compare all three groups (never, not recent, recent) simultaneously to understand how mammography history relates to obtaining future mammograms. Therefore, interventions to improve adherence to screening mammography guidelines among Latinas need to consider the barriers at different stages separately.

The relationship between past and future mammography thoughts, plans, and behavior is mediated by a complex combination of sociodemographic, intrapersonal, and interpersonal factors. The majority of theory and empirical interventions for Latinas has focused primarily on sociodemographic, intrapersonal, and interpersonal factors outside the healthcare context (Jerome-D’Emilia, 2015). However, healthcare factors, operationalized as access and experience, may also influence the relationship between past and future mammography behavior (Gierisch, Earp, Brewer, & Rimer, 2010; Zorogastua, Erwin, Thelemaque, Pulley, & Jandorf, 2016). For example, women reporting adherence to screening mammography guidelines are more likely to also report greater healthcare access, including having health insurance and a regular provider, and experiences with their providers, including having had a clinical breast examination (CBE) and a provider recommendation (Nuño et al., 2011; Watson-Johnson et al., 2011). Despite extant empirical work documenting these patterns, to the authors’ knowledge, no extant theory or framework has addressed if or how health care influences longitudinal mammography patterns. In addition, this is the first study that has quantified the mediating effects of healthcare factors on relationships between past mammography behavior and future thoughts, intentions, and behavior. Therefore, the current study will provide preliminary evidence to inform adaptation of extant theories and conceptual frameworks regarding longitudinal mammography use, such as the Transtheoretical Model and Theory of Planned Behavior, to incorporate the mediating roles of healthcare factors more explicitly.

The Role of Nurses in Health Equities

Nurses serve a major role in promoting equity in early breast cancer detection. Nurses operate across the spectrum of healthcare delivery and can translate research into improved patient experiences, awareness, and receipt of screening mammography (Shackelford, Weyhenmeyer, & Mabus, 2014). Nurses may be better able to provide culturally appropriate care to Latinas, given that they are more likely than physicians to be similar sociodemographically (e.g., female, Spanish speaker, Latina ethnicity, socioeconomic background) (Association of American Medical Colleges, 2014). As the U.S. population becomes older and more racially diverse, nurses and nurse practitioners are ideally suited to eliminate disparities in adherence to screening mammography guidelines (Yeo, Phillips, Delengowski, Griffiths, & Purnell, 2011), particularly as these guidelines change.

Nurse researchers, particularly oncology nurse researchers, serve as pivotal stakeholders in addressing cancer inequities. Oncology nurse researchers have conceptualized the importance of patients’ interactions with the healthcare system and other factors associated with optimal breast cancer care in terms of access and experience (Downey & Happ, 2013; Kennedy Sheldon, 2005; Traeger et al., 2013), particularly among underserved ethnic minority communities (Jerome-D’Emilia, Suplee, & Akincigil, 2015; Mott-Coles, 2014; Royak-Schaler et al., 2008; Russell, Perkins, Zollinger, & Champion, 2006). These researchers have further indicated the importance of nurses in addressing barriers to healthcare access and positive experiences with their providers by women from marginalized groups (Giger et al., 2007; Larsen & Reif, 2011). Therefore, the current article seeks to address gaps in the literature and identify possible ways to improve the health and well-being of Latinas across the breast cancer continuum.

Methods

To understand the relationship between mammography history and current thoughts about obtaining a mammogram among Latinas, the mediation effects of several healthcare factors were examined. First, the authors assessed differences in hypothesized healthcare factor mechanisms (e.g., health insurance status, regular provider, CBE, provider recommendation) by mammography history. Second, they examined if mammography history and healthcare factors were associated with thoughts about obtaining a mammogram. Finally, the authors conducted a formal analysis to directly test the mediating effects of healthcare factors in the relationship between mammography history and thoughts about obtaining a mammogram.

Procedures

Recruitment: The current study used baseline data from a multi-clinic randomized, controlled trial (¡Fortaleza Latina!) that involved partnerships among the Fred Hutchinson Cancer Research Center, the University of Washington, the Seattle Cancer Care Alliance, and Sea Mar, a federally qualified health center (FQHC) with multiple clinic sites (Coronado et al., 2014; Molina et al., 2015). The primary aim of ¡Fortaleza Latina! is to increase participation in breast cancer screening among Latinas. The institutional review boards of all institutions approved the study. Baseline data were collected from 2012–2014 and analyzed in 2014. The recruitment and interview procedures have been reported previously (Coronado et al., 2014). The electronic health records (EHRs) from the four clinics of the FQHC identified potential participants. Enrollment criteria consisted of: (a) identified as Latina or Hispanic in the EHR and confirmed during in-person interviews; (b) aged from 42–74 years; and (c) received care from one of the four clinics within the past five years. FQHC staff invited, screened, and consented patients for the study. Patients signed a Health Insurance Portability and Accountability Act waiver to be contacted by project staff to participate (Coronado et al., 2014).

Interviews: The methodology used to translate and validate the survey and train the promotores was described previously (Coronado et al., 2014). After obtaining consent to participate in ¡Fortaleza Latina!, staff contacted participants by telephone to schedule an interview, and promotores conducted these in-person baseline interviews. Five promotores were trained to consistently obtain consent and interview participants to reduce bias and to support the validity and reliability of the survey results. The 161-item baseline survey was developed from previous instruments addressing breast cancer screening in Latinas (Byrd et al., 2013; Gallo et al., 2014; Puschel et al., 2010). Participants completed the survey in their preferred language (English or Spanish).

Data entry: Trained operators at the Fred Hutchinson Cancer Research Center Collaborative Data Services performed data entry using DatStat Illume. Data were then exported to SAS®, version 9.0, for analysis.

Measures

Sociodemographic information: Sociodemographic questions assessed information at the time of the survey. Women also gave information regarding their country of birth, the year they arrived in the United States, and their language of preference. Finally, women were asked how many of their primary relatives (mother, sisters, daughters) ever had breast cancer.

Mammography history: Figure 1 illustrates how the mammography history groups for the current study were derived from ¡Fortaleza Latina!. Women self-reported their lifetime mammography history and number of years since their last mammogram. Self-report of recent mammogram was substantiated with the relevant provider’s medical record. Discrepancies were resolved by confirming mammograms at the appropriate institutions. In cases for which screening mammograms could not be confirmed, the participant was considered not to have had a mammogram. Women were categorized as never had a mammogram (never), had a mammogram more than two years before study enrollment (not recent), and had a mammogram two years or less before study enrollment (recent). Women obtaining a diagnostic mammogram (non-screening) as their most recent mammogram were excluded.

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Women were asked if they had thought or were thinking about getting a or another mammogram; if they had health insurance coverage at the time of taking the survey; if they had a personal doctor or medical provider who was their main provider; if they had a provider examine their breasts within the past year; and if a doctor, nurse, or other healthcare professional (provider) had recommended a mammogram within the past year (0 = no, 1 = yes).

Statistical Analysis

Simple bivariate analyses identified potential sociodemographic covariates for thoughts about obtaining a mammogram. First, four multivariable logistic regression models were conducted to examine if health insurance status, having a regular provider, having a CBE performed, and receiving a provider recommendation varied across mammography history (four separate coefficients “a”). Next, the authors conducted a multivariable logistic regression model to examine the direct associations of mammography history on thoughts about obtaining a mammogram (coefficient “c”). Another multivariable logistic regression model examined the relationship between healthcare factors and thoughts about obtaining a mammogram. It yielded four separate coefficients “b.” Finally, two mediation models were conducted using Preacher and Hayes methods (using 5,000 samples) (Hayes & Preacher, 2014; Preacher & Hayes, 2008). To determine the mediating effect, 95% confidence intervals (CIs) were calculated and the percentage mediated was calculated as a function of the indirect effect (a*b) divided by the sum of the direct effect and indirect effect ([a*b]/[a*b+c^1]). Women with a recent history were used as the referent group, and dummy coded variables were included in accordance with recommendations for analyses with categorical predictors (Hayes & Preacher, 2014; Preacher & Hayes, 2008). This method allows models to retain all information about how the three groups differ from one another while focusing on one specific comparison (e.g., recent versus never, recent versus not recent).

Results

Sample Characteristics

Table 1 provides sociodemographic factors across mammography history. Less than 1% of women had missing data for each variable of interest, except income (15% of women did not report income). Women with a never history of a mammogram were younger than women with not recent and recent mammography histories. Women with a recent history of mammography reported greater household income relative to other groups; however, the proportion of missing data for income varied across mammography history (p = 0.05). Consequently, analyses always included age as a covariate; given differences in the amount of missing data across mammography history, models with and without income as a covariate were conducted.

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Healthcare Variables

Table 2 provides descriptive characteristics and results from multivariable logistic regression models for each mammography history. Age was included as a covariate because of its significant association with mammography history. Relative to women with a recent history, women with a never and not recent mammography history were less likely to be insured, have a regular provider, have had a CBE performed within the past year, and have received a provider recommendation to have a mammogram within the past year. Associations did not differ when including age and income or when including only age as covariates.

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Thoughts About Obtaining a Mammogram

Table 3 provides unadjusted descriptive characteristics and results from multivariable logistic regression models using mammography history, health insurance status, having a regular provider, having had a CBE performed within the past year, and receipt of a provider recommendation. After adjusting for age, mammography history was significantly associated with thoughts about obtaining a mammogram. Relative to women with a recent history, women with never and not recent histories were less likely to state that they had thoughts about obtaining a mammogram. When including age and income as covariates, women with a never history were still less likely than women with a recent history to report thoughts about obtaining a mammogram (odds ratio [OR] = 0.2, 95% CI [0.1, 0.7], p = 0.003). Differences were attenuated when including income between women with recent and not recent histories (OR = 0.7, 95% CI [0.2, 1.5], p = 0.28). After adjusting for age, having a CBE performed and receipt of a provider recommendation were associated with thoughts about obtaining a mammogram but not health insurance status or having a regular provider. These patterns persisted, even when including income as a covariate. Given these findings, having a CBE performed and receiving a provider recommendation were identified as potential mediators, but health insurance status or having a regular provider were not.

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Mediation Model

Prior to mediation models, the authors assessed the potential moderating effects of healthcare factors. Multivariable logistic regression models revealed no significant interaction terms (p = 0.44–0.99). The mediating effects of having a CBE performed and receiving a provider recommendation within the past year on differences in thoughts about obtaining a mammogram were explored among women with never and recent histories (see Figure 2). Evidence existed of full mediation effect, which was driven by having a CBE performed (70% mediated, mediated effect = –0.94, 95% CI [–1.9, –0.35]). One reason contributing to the lower thoughts about obtaining a mammogram among women with a never history, relative to women with a recent history, was their lower odds of having a CBE performed. Similar patterns were observed when including or excluding income as a covariate. Second, the mediating effects of these variables among women with not recent and recent were explored (see Figure 3). This model did not include income as a covariate, given findings discussed previously. Full mediation was also suggested for this model and appeared to be driven by receipt of a provider recommendation (54% mediated, mediated effect = –0.58, 95% CI [–1.2, –0.1]). One reason contributing to the lower thoughts among women with a not recent history, relative to women with a recent history, was their lower odds of receiving a provider recommendation.

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Discussion

Because the U.S. healthcare system focuses more on performance, preventive care, and increasing access, providers need to understand how to increase the proportion of women adhering to screening mammography guidelines (Albright et al., 2011; Moy et al., 2011). In the current study, the authors showed that Latinas with a recent mammography history were more likely to have thoughts about obtaining a mammogram than members of the other two groups (never and not recent). The findings also suggest that healthcare factors vary by past behavior and future thoughts. Finally, findings emphasize the value that Latinas place on the relationship with their providers regarding adhering to screening mammography guidelines.

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A major gap in the literature addressed by the current study was a more comprehensive assessment of healthcare factors across different mammography histories. A previous study of Latinas demonstrated significant differences in healthcare factors across different mammography histories (Castañeda et al., 2014). However, Castañeda et al. (2014) categorized their population into recent and not recent/never because too few women reported a not recent mammography history (n = 16, 8%). The current authors’ work extends this understanding by simultaneously assessing Latinas with different mammography histories, including women with never, not recent, and recent histories. The current study found that Latinas with a never or not recent history had less healthcare access (medical insurance, regular provider) and use (CBE, provider recommendation) relative to Latinas with a recent history. Previous cross-sectional research has largely attributed differences in mammography histories to be a result of past healthcare factors (González & Borrayo, 2011); however, the current study shows that past mammography history predicts current healthcare factors.

The authors hypothesize that both of these relationships were longitudinal, such that continuous healthcare access and use resulted in adherence to screening mammography guidelines. In this case, Latinas with a recent history may have had greater healthcare access and positive experiences with their providers (influencing their receipt of mammography) and may continue to have greater healthcare access and positive experiences (influencing their future use) relative to Latinas with a never and not recent history. Consistently, different healthcare factors mediated the relationship between mammography history and thoughts. Latinas with a recent history of mammography had greater thoughts about obtaining a mammogram relative to Latinas with a never history of mammography, in part because they were more likely to have a CBE performed in the past year. Simultaneously, they had greater thoughts about obtaining a mammogram relative to Latinas with a not recent mammography history, in part because they were more likely to have received a provider recommendation in the past year. The current authors’ work indicates the importance of additional research that quantifies these longitudinal patterns and examines the role of continuous healthcare access and use.

Of note, the current findings suggest that experiences with their providers during healthcare visits (CBE, provider recommendation) were more strongly associated with thoughts about obtaining a mammogram than healthcare access variables (insurance, regular provider). A previous meta-analysis of 195 studies on screening mammography use demonstrated that a woman’s previous screening behaviors (breast, cervical, and colon cancer) and a physician’s recommendation were the strongest predictors of recent mammography use (Schueler et al., 2008). However, this meta-analysis included insufficient Latinas for a subanalysis of factors associated with mammography history. Also, the studies used in this meta-analysis focus on a physician’s recommendation. This narrow focus on physicians ignores other healthcare professionals providing health education and recommendations, particularly nurses. The authors asked a more inclusive question (“Has any doctor, nurse, or other health professional recommended a mammogram within the past year?”) to account for changes in healthcare delivery. The authors’ work suggests that any provider recommending a mammogram increases adherence in Latinas with a not recent mammography history; this emphasizes a need to include other healthcare professionals when assessing impact of recommendations.

Although Latinas’ experiences with their providers appeared to serve as mediators (e.g., CBE, provider recommendation), the current study also suggests that the mediators for the relationship between mammography history and thoughts are different for Latinas with not recent and never histories. A need exists for more qualitative and quantitative research to understand these effects. One potential explanation is that these factors are associated with different intrapersonal factors unique to women’s mammography history. For example, lower levels of knowledge and psychocultural attitudes about mammography have been found among Latinas with a never mammography history (Madadi, Zhang, Yeary, & Henderson, 2014). Conversely, women with a not recent and recent mammography history have overcome these barriers to obtain their first mammogram. A provider recommendation among women with a history of mammography use may differ from those given to women with a never history and involve more discussion about the need for regular mammography. This type of tailored recommendation would address the lower levels of knowledge among Latinas with a not recent history (González & Borrayo, 2011; Hall, Hall, Pfriemer, Wimberley, & Jones, 2007). Alternatively, provider recommendations may serve as a reminder to women with a recent mammography history.

Limitations

The current study is limited by several factors. First, previous studies have used different definitions for recent and not recent mammography history, some using the previous American Cancer Society definition (Smith, Cokkinides, Brooks, Saslow, & Brawley, 2010) of one year or less for recent and others using the U.S. Preventive Services Task Force ([USPSTF], 2009) definition of two years or less for recent. During the current study, the USPSTF changed its recommendations to every two years and advised that routine screening begin at age 50 years (Siu, 2016). Because this was a recent change, the current authors included women aged 42 years and older but considered women adherent if they had a mammogram within two years. Second, the authors used thoughts about obtaining a mammogram, rather than obtaining a mammogram, as one of the outcome variables. Previous research typically used thoughts or intentions to obtain a mammogram as a surrogate measure for obtaining one in the future because it can be measured immediately after an intervention (Madadi et al., 2014). Although current thoughts about obtaining a mammogram do not imply that one will obtain a future mammogram, they are a prerequisite because a woman who does not think about obtaining a mammogram is unlikely to obtain one. Third, the current analysis relies on cross-sectional data. However, the operationalization of mammography history, current healthcare factors, and thoughts about obtaining a mammogram approximate a temporal sequence. Fourth, differences in missing data on income limited the authors’ ability to understand the role of income on screening intention. Finally, although insurance status was collected at the time of the survey, changes in insurance status may have occurred.

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Conclusion

To the authors’ knowledge, this is the first study to quantify healthcare factors as potential mechanisms underlying past and future mammography use. Additional research on the role of provider visits and the patient–provider relationship is needed to understand why mammography history predicts future screening behavior. The current results suggest that, although a referral for a mammogram is not necessarily needed, providers maintain a key role in Latinas’ breast cancer screening practices.

Implications for Nursing

The current study has important implications for the high impact of nursing interventions for Latinas across different mammography history groups. Specifically, nurses often interact with patients when providing health communications and are more frequently from similar sociodemographic groups (e.g., gender, ethnicity, language) and, therefore, more likely to recognize and address health needs (e.g., barriers to obtaining a mammogram) (Cottrell et al., 2012; Eggenberger, Grassley, & Restrepo, 2006; Engelman et al., 2011). Therefore, nurses may improve Latinas’ adherence to screening mammography guidelines through their role as health communicators in the clinic, as well as medical experts within their racial and ethnic communities. CBE may be a unique opportunity within the patient–provider interaction for providers to discuss breast cancer and the importance of screening mammography. Latinas may be more comfortable asking questions about sensitive topics, such as breast health, with females from their community. Nurses operating as health educators or primary care providers need to discuss screening mammography with their patients (Hall et al., 2007; Shackelford et al., 2014; Tupper & Holm, 2014). Although CBE is no longer recommended by the USPSTF for breast cancer screening, the National Comprehensive Cancer Network continues to recommend CBEs, and both organizations recognize the importance of breast cancer awareness (National Comprehensive Cancer Network, 2016; USPSTF, 2009). Nurse providers should recognize that, in addition to their potential to screen for breast cancer, CBEs may provide an important opportunity for delivering education on screening mammography to Latinas.

In addition, the current study provides important information for oncology nursing researchers. As noted previously, many conceptual models that articulate factors affecting the relationship between past and future mammography behavior focus on sociodemographic, intrapersonal, and interpersonal factors (Jerome-D’Emilia, 2015). Simultaneously, oncology nursing researchers have emphasized the importance of healthcare factors, including access and experiences with their providers, for patients’ health and well-being (Downey & Happ, 2013; Kennedy Sheldon, 2005; Traeger et al., 2013). The current study provides evidence for the need of oncology nursing researchers in expansion of extant conceptual frameworks, particularly regarding inclusion of healthcare access and experience factors.

The authors gratefully acknowledge Gaytri P. Scheel, MD, and Catherine O’Donnell, MA, for their careful review of this manuscript. In addition, they gratefully acknowledge the dedicated efforts of the ¡Fortaleza Latina! participants and of key affiliated investigators and staff throughout the project.

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About the Author(s)

Scheel is an assistant professor in the Department of Radiology at the University of Washington in Seattle; Molina is an assistant professor in the School of Public Health and Community Health Sciences Division at the University of Illinois in Chicago; Coronado is a senior investigator in health disaprities research at the Kaiser Permanente Center for Health Research in Portland, OR; Bishop is a program manager in the Division of Public Health Sciences at the Fred Hutchinson Cancer Research Center in Seattle; Doty is a health education program coordinator and Jimenez is a medical director, both at Sea Mar Community Health Centers; Thompson is a researcher in the Cancer Prevention Program at the Fred Hutchinson Cancer Research Center; Lehman is the director of breast imaging in the Department of Radiology at Massachusetts General Hospital in Boston; and Beresford is a professor and senior associate dean in the Department of Epidemiology at the University of Washington in Seattle. This research was funded by grants from the National Cancer Institute (R25 CA92408) and the Center for Population Health and Health Disparities (5 P50 CA148143) and by a Safeway Foundation Breast Cancer Research Award. All of the authors contributed to the conceptualization and design and completed the data collection. Scheel and Molina provided statistical support and analysis. Scheel, Molina, Coronado, Thompson, Lehman, and Beresford contributed to the manuscript preparation. Scheel can be reached at jrs4yg@uw.edu, with copy to editor at ONFEditor@ons.org. Submitted August 2015. Accepted for publication April 19, 2016.