https://orcid.org/0000-0002-2716-9469
Abstract
Background
Major restructuring of surveillance after breast cancer treatment with less follow-up consultations may result in insecurity and fear of recurrence (FCR) among the less resourceful breast cancer patients. We investigate the association between breast cancer patients’ education and FCR and if self-efficacy mediates the associations between education and FCR.
Material and methods
A questionnaire survey was conducted from 2017 to 2019, among 1773 breast cancer patients shortly after having their follow-up switched from regular outpatient visits with an oncologist to either nurse-led or patient-initiated follow-up, with a subsequent questionnaire after 12 months. Data on disease and treatment characteristics were extracted from medical records and the Danish Breast Cancer Group Database. Logistic regression analyses were used to examine the association between education and FCR. Separate analyses were conducted for patients ≤ and >5 years since diagnosis and all models were adjusted for age and cohabitation status. To explore potential mediation by self-efficacy, we conducted regression analyses on education and FCR further adjusting for self-efficacy.
Results
The participation rate was 57%, and after the exclusion of patients due to missing data, 917 were included in analyses. Patients with long education had significantly less FCR compared to patients with short education (OR (95% CI) 0.71 (0.51;0,99)). When separated by time since diagnosis, there was no association among patients >5 years since diagnosis while the OR was 0.51 (95% CI, 0.30;0.85) for patients ≤5 years since diagnosis. Further adjusting for self-efficacy among patients <5 years since diagnosis resulted in an OR of 0.56 (95% CI, 0.33;0.95) among patients with long compared to short education.
Conclusion
Up to 5 years after diagnosis, breast cancer patients with long education are less likely to experience FCR than patients with short education. Self-efficacy mediated only a very small part of this association, indicating that other factors play a role in socioeconomic differences in FCR among breast cancer patients.
Background
Fear of cancer recurrence (FCR), defined as ‘fear, worry or concern about cancer returning or progressing’ [Citation1] is one of the most commonly reported symptoms amongst cancer patients. A systematic review found that 22–87% of patients across cancer types report moderate to high FCR and up to 15% report high levels of FCR [Citation2]. FCR has been associated with depression, poor quality of life, and impaired functioning [Citation3,Citation4]. Further, it has been indicated that patients with FCR may on the one hand overuse medical services, and on the other hand, avoid participation in tests to identify recurrence in follow-up surveillance [Citation5]. Such results point to self-efficacy, a construct associated with health behavior and the use of health services [Citation6] which may influence FCR.
Self-efficacy is the belief in one’s ability to perform relevant self-care behaviors in particular situations [Citation6,Citation7]. Previous studies found that a higher degree of self-efficacy among breast cancer patients was associated with better mental well-being, increased quality of life, and less fatigue [Citation8–10]. Thus, higher levels of self-efficacy may be associated with better self-care and help-seeking behaviors and management of symptoms like FCR during treatment and subsequent follow-up.
Recently introduced Danish national guidelines for follow-up after breast cancer have reduced the number of regular outpatient visits, favoring an individual and needs-based approach as described by Karlsen et al. [Citation11]. However, such changes in the follow-up program put a higher demand on the individual breast cancer survivor’s own ability to interpret and react to symptoms of recurrence, to treatment-related side effects, as well as psychosocial needs, which may include FCR. Changes toward increasing patient-initiated follow-up care thus may imply a risk that some patients with less resources will not receive adequate and timely management of symptoms and may thus introduce social inequality in the follow-up of cancer and potentially also in FCR.
Socioeconomic inequality has been documented in breast cancer patients, including socioeconomic differences in stage at diagnosis and access to treatment [Citation12–16], in return to work after treatment [Citation17], and in survival [Citation14–16]. We, however, still know little about socioeconomic differences in breast cancer- and treatment-related symptoms and late effects. To the best of our knowledge, socioeconomic differences in FCR and the role that self-efficacy may play in this association have not been investigated before. In a prospective questionnaire study among patients in follow-up after breast cancer treatment, we investigated the association between educational level and the clinically relevant level of FCR and if self-efficacy played a role in this association. The hypothesis was that patients with short education would have a higher level of FCR than patients with a long education and that this may be mediated partly by lower self-efficacy in these patients compared with patients with long education.
Material and methods
Population and data collection
The study was conducted at the Department of Clinical Oncology and Palliative Care, Zealand University Hospital, Denmark, which provides all oncological breast cancer treatment and follow-up in the Danish Region Zealand (approximately 850,000 citizens). Region Zealand implemented the change in follow-up program during the period from July 2016 to May 2017 and successively changed the follow-up from oncologist-led to either nurse-led or patient-initiated follow-up in all breast cancer patients with low or intermediate risk of recurrence (>40 years at diagnosis, no known BRCA mutation, stage I–II and no recurrent breast cancer). Patients 1–5 years after diagnosis could choose between nurse-led or patient-initiated follow-up, whereas patients 5–10 years after diagnosis were allocated only to patient-initiated follow-up. Follow-up of breast cancer patients with a very low or high risk of recurrence was unchanged. In order to examine the symptom burden over time after the implementation of the new follow-up program and in order to identify vulnerable patient groups that may otherwise not be identified in a less intensive follow-up program, we sent out a baseline questionnaire 0–6 months after transition to the new follow-up program, and a follow-up questionnaire 12 months later. Both questionnaires included a series of validated scales, and the baseline questionnaire additionally included study-specific questions on education and cohabitation status. FCR and self-efficacy were obtained from the follow-up questionnaire.
In addition, we obtained data on tumor characteristics and adjuvant treatment received from the database of the Danish Breast Cancer Group (DBCG) [Citation18]. Through medical records, we identified and excluded patients who experienced breast cancer recurrence or a new cancer diagnosis between baseline and follow-up. Data from this cohort study has also been used to investigate the association between socioeconomic position and HRQOL and self-management 12 months after implementation of the new follow-up program has also been examined [Citation11]. The study was approved by the Danish Data Protection Agency Jr. no. 2016-41-4769 and registered in the Danish Cancer Society Research Database (2018-DCRC-0011). No permission from the Ethical Committee System was required. The study is reported according to the STROBE guidelines [Citation19].
Exposure
Educational level was used to define participants’ socioeconomic position. Education reflects a person’s attained knowledge, cognitive function, and skills and is highly associated with understanding of health information and access to health services [Citation20]. It is a relatively stable indicator over the adult life course and thus can be considered valid as a self-reported measure. We categorized education into short (mandatory school, 7–9 years), medium (senior high school or vocational education, 9–12 years), and long (higher education, ≥13 years).
Descriptive characteristics and covariates
For descriptive purposes, clinical variables on tumor size (0–20 mm, 21–50 mm, >50 mm), tumor positive lymph nodes (0, 1–3, 4+), estrogen receptor (ER) status (positive, negative), human epidermal growth factor receptor 2 (HER2) status (positive, negative), and treatment variables on surgery (mastectomy, lumpectomy) and chemotherapy, radiation therapy, endocrine therapy and HER2 therapy (yes/no variables) were created. Potential confounders included age (as linear) and cohabitation status (living with a partner (married, cohabiting) or living alone (single, widow, divorced) and time since diagnosis was categorized as ≤ or >5 years since diagnosis.
Outcomes
FCR was measured by the Concerns About Recurrence Questionnaire (CARQ-4) [Citation4].
The CARQ-4 scale score ranges from 0 to 40 points, zero indicating no fear of recurrence and 40 indicating the highest possible fear of recurrence. Points were calculated according to the scoring manual, and we applied a cut-point of 11 for clinically relevant FCR [Citation4]. The average score was used to replace missing responses if a participant responded to ≥50% of the questions. Participants responding to <50% of the questions were excluded from the analyses.
Self-efficacy was measured by the General Self-Efficacy scale (GSE) [Citation21]. The GSE scale score ranges from 10 to 40 points with a higher score indicating higher self-efficacy. As the developers of the GSE scale do not recommend using a cut-point between high and low self-efficacy, we analyzed self-efficacy as a continuous variable. Missing responses were replaced by the average score if the participant responded to more than 7 out of 10 questions [Citation22].
Statistical analyses
We used logistic regression analysis to examine the association between education and clinically relevant fear of recurrence adjusting for age and cohabitation status. Preplanned separate analyses among patients ≤ or >5 years since diagnosis explored the association between education and FCR amongst short-term and long-term BC survivors.
Using the traditional mediation approach as suggested by Baron and Kenny [Citation23] and VanderWeele [Citation24] we explored the potential mediation of self-efficacy on the association between education and FCR in regression models with and without adjusting for self-efficacy. Using the difference method, a change in parameter estimate is taken as mediation [Citation23,Citation24].The statistical software STATA IC version 14.2 was used for statistical analyses.
Results
Among 1773 breast cancer patients who were invited to participate in the study, 1011 responded to both the baseline and the follow-up questionnaire (57%).
We excluded patients who had a recurrence or new cancer between baseline and follow-up (n = 18, 2%) and further, patients with missing exposure data, outcomes, and confounder variables (n = 76, 8%) leaving 917 patients for analysis.
Patients with long education were younger (mean age 65.7), and more frequently living with a partner (70%) compared with patients with short education (mean age 70.1 and 59%) (). About 40% of the patients were ≤ 5 years since diagnosis with only small differences across educational groups. When comparing disease and treatment characteristics by education only a few differences were observed (). Descriptively, 35% of breast cancer patients with short education scored in the clinical range of fear of recurrence compared with 30% of participants with long education, while mean self-efficacy scores ranged from 29.6 (SD 7.3; short education) to 30.9 (SD 6.9; long education) (Online Table S1).
Table 1. Descriptive sociodemographic characteristics among 917 women in follow-up after breast cancer who had follow-up changed from oncologist-led to nurse-led or patient-initiated follow-up, Region Zealand, Denmark, 2016–17.
Overall, the adjusted OR for clinically relevant FCR diminished stepwise with the increasing length of education and was 0.71 (95% CI, 0.51;0.99) for patients with long compared with short education. Among patients who were ≤5 years after diagnosis, the OR for clinically relevant FCR was 0.51 (95% CI, 0.30;0.85) among patients with long compared with short education and 0.81 (0.44;1.51) for medium compared with short education. No statistically significant associations between education and FCR was found among patients >5 years after diagnosis (). Due to these results, we only explored the potential mediating effect of self-efficacy among patients ≤5 years after diagnosis.
Table 2. Associations between education and clinically relevant fear of recurrence among 917 women in follow-up after breast cancer who had follow-up changed from oncologist-led to nurse-led or patient-initiated follow-up, Region Zealand, Denmark, 2016–17.
There was a tendency towards higher self-efficacy with longer education, albeit not statistically significant (Online Table S2). Conversely, FCR decreased with increasing self-efficacy, with an adjusted OR of 0.93 (95% CI, 0.90;0.96) per 1-point self-efficacy score and a score of 0.69 (95% CI, 0.59;0.80) per 5-point self-efficacy. With adjustment for self-efficacy, the OR for clinically relevant FCR changed slightly from 0.81 (95% CI, 0.44;1.51) () to 0.84 (95% CI, 0.44;1.60) (Online Table S2) in patients with medium, and from 0.51 (95% CI, 0.30;0.85) () to 0.56 (95% CI, 0.33;0.95) (Online Table S2) in patients with long compared with short education, respectively.
Discussion
Our findings suggest that within the first five years after diagnosis, breast cancer patients with short education are at higher risk of reporting clinically relevant FCR than patients with long education. Further, self-efficacy only influenced the association between education and FCR to a very low degree.
In this population of patients in follow-up after breast cancer, we found educational differences in clinically relevant FCR, but only among patients ≤5 years since breast cancer diagnosis. Although some studies find that FCR is stable over time [Citation2], FCR has also been found to be the strongest short time after diagnosis and decrease over time [Citation25,Citation26].
A recent systematic review and meta-analysis demonstrate that psychological interventions are efficacious in reducing FCR [Citation27]. Thus, when implementing such interventions in clinical practice, it is important to ensure that all patients independent of education are included if they have FCR at a clinically relevant level.
Although self-efficacy increased with the level of education, and FCR decreased with increasing self-efficacy as also found previously [Citation7], our results indicate that self-efficacy only mediate a very small part, if any, of the association between education and FCR. To the best of our knowledge, this association has not been explored in previous studies. As we used general self-efficacy as a measure of self-efficacy rather than a more specific cancer-related or survivorship-related self-efficacy measure, this may be a reason for the only weak and probably not clinically relevant associations between education, FCR, and self-efficacy.
Strengths and limitations
The population-based and longitudinal nature of the study and the combination of self-reported outcomes, clinical, and treatment characteristics strengthen the study findings.
Participation in both the baseline and the follow-up questionnaire was 57% and may be considered fairly high. Although misclassification may occur, education is generally considered a stable and feasible measure for self-report [Citation20]. It is however, likely that patients with low education or with FCR may be more likely to not respond to the follow-up questionnaire [Citation28–30], which may affect the generalizability of results. Exploration of potential mediation of self-efficacy is a strength of the study, however, future studies may consider to apply a more advanced mediation approach. Further, our use of a general self-efficacy measure may have hampered our ability to explore the potential role of self-efficacy on the association between education and FCR in this population.
Conclusion
We demonstrate an educational inequality in FCR among breast cancer patients in follow-up up to five years after diagnosis; where patients with short education are more likely to experience clinically relevant FCR than patients with long education. This was only to a very small degree explained by self-efficacy, and thus, more knowledge is needed on factors driving the association between SEP and clinically relevant FCR, like cancer-specific self-efficacy, health literacy, or symptom burden.
Supplemental Material
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Data availability
The data that supports the findings of this study are available from the last author (SD) upon reasonable request.
Additional information
Funding
References
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