It’s not an easy fix: Adherence to adjuvant endocrine therapy after breast cancer

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Editor note: The manuscript was written based on the Clinical Lectureship Award lecture provided at the Annual Conference of the Canadian Association of Nurses in Oncology held in Winnipeg, October, 2019.

It’s not an easy fix: Adherence to adjuvant endocrine therapy after breast cancer

by Leah K. Lambert, Lynda G. Balneaves, and A. Fuchsia Howard

ABSTRACT

Adjuvant endocrine therapy (AET) is a highly efficacious treatment that signifi- cantly reduces breast cancer recurrence and mortality for women with hormone-re- ceptor positive breast cancer. Yet, many women do not adhere to prescribed AET.

The overarching aim of this research was to gain a better understanding of why a sig- nificant number of women diagnosed with breast cancer have suboptimal adherence to AET. A mixed-methods approach was used to explore the personal, social, and struc- tural factors influencing breast cancer sur- vivors’ AET adherence, including: (1) an integrative review of patient-reported fac- tors associated with AET adherence; and (2) interviews with breast cancer survivors prescribed AET. In this paper, we summa- rize and discuss the key contributions of both phases of this research, implication for clinical practice, and how we might lever- age the expertise of nurses in practicing to full scope to address the complex needs of breast cancer survivors prescribed AET.

INTRODUCTION

A

s the leading cause of cancer in Canadian women, breast cancer is expected to be diagnosed in approximately 27,400, or 1 in every 8, women in 2020 (Brenner et al., 2020). From 1980 though the early 1990s, we saw an upward trend in the number of women diagnosed with breast cancer due to improved early detection of breast malignancies using mammography screening (Canadian Cancer Society’s Steering Committee, 2010). Since the 1980s, mortality from breast cancer has substantially declined due, in part, to advancements in treatment options including adjuvant endocrine therapy (AET) (Berry et al., 2005; Canadian Cancer Society’s Steering Committee, 2010).

AET is a treatment (e.g., tamoxifen, aromatase inhibitors) for breast cancer that significantly reduces the risk of recurrence and mortality for women with early-stage, hormone receptor-positive (HR+) breast cancer, if taken as prescribed for the recommended treatment period (Burstein et al., 2019; Hershman et al., 2011). For example, tamoxifen reduces the risk of recurrence by almost half in the first 10 years after diagnosis and improves disease-free survival by approximately a third in the first 15 years after diagnosis in women with early-stage breast cancer (Early Breast Cancer Trialists’ Collaborative Group, 2011). Until 2010, AET was prescribed for five years after initial treatment for women diagnosed with HR+ breast cancer. In 2010, the American Society of Clinical Oncology published clinical practice guidelines recommending AET for up to 10 years in eligible women (Burstein et al., 2010).

Unfortunately, adherence to AET is suboptimal and less than half (49%) of

women diagnosed with breast cancer take the recommended dose of AET for the full duration of therapy (Hershman et al., 2010). Evidence suggests that the benefits of AET are greatest when women adhere to therapy for the prescribed treatment period. Women who adhere to AET for less than five years have a significantly higher rate of breast cancer recurrence (Burstein et al., 2010;

Hershman et al., 2011). AET non-adherence and early discontinuation are also associated with an increased risk of mortality (49% and 26%, respectively) (Hershman et al., 2011). The connec- tion between adherence and survival outcomes highlights the importance of identifying the reasons why women do not use these medications as prescribed.

Historically, the majority of research on AET adherence focused on identifying demographic and clinical predictors of AET non-adherence, with very little known about the personal (e.g., beliefs and values), social (e.g., social support, patient-healthcare provider [HCP] relationships) and structural factors in the healthcare system (e.g., continuity of care) that may influence women’s decisions and behaviours related to AET adherence. These gaps in the literature and the relative lack of attention to social and structural factors led me to wonder why researchers had not talked directly with breast cancer survivors to understand what was happen- ing in their everyday lives to support their adherence to AET. If innovative, patient-centred adherence interventions are to be developed, knowledge about people’s experiences and prefer- ences related to AET, and their moti- vations associated with adherence to these potentially life conserving thera- pies are needed. As such, in my doctoral research, I decided to use qualitative

AUTHOR NOTES

Leah K. Lambert, School of Nursing, University of British Columbia, T201-2211 Wesbrook Mall, Vancouver, BC V6T 2B5; British Columbia Cancer, 600 W 10th Ave, Vancouver, BC V5Z 4E6

Lynda G. Balneaves, College of Nursing, Rady Faculty of Health Sciences, University of Manitoba, 89 Curry Place, Helen Glass Centre for Nursing, Winnipeg, MB R3T 2N2

A. Fuchsia Howard, School of Nursing, University of British Columbia, T201-2211 Wesbrook Mall, Vancouver, BC V6T 2B5

Corresponding author contact: Leah K. Lambert, PhD, RN

Email: Leah.Lambert@ubc.ca

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methodology to interview breast cancer survivors to better understand why women engage in medication-taking behaviours that could potentially cause them harm. I wanted to delve into women’s stories to uncover how complex psychosocial issues, including beliefs, values, relationship issues, work chal- lenges, and attributes of the healthcare system and service delivery influence AET adherence.

The overarching aim of our research was to gain a better understanding of why a significant number of women diagnosed with breast cancer have suboptimal adherence to AET. The spe- cific research objectives that guided this study were:

1. Identify the patient-reported factors in the literature that were found to be associated with non-adherence in breast cancer survivors;

2. Explore breast cancer survivors’

experiences and perspectives related to AET adherence using a qualitative approach.

In this paper, we summarize and discuss the key contributions of both phases of this research, implications for clinical practice, and how we might leverage the expertise of nurses in practicing to full scope to address the complex needs of breast cancer survivors prescribed AET.

SUMMARY AND KEY CONTRIBUTIONS OF FINDINGS

Integrative Review

To address the first research objec- tive, we conducted an integrative review (Lambert, Balneaves, Howard, & Gotay, 2018) to: (1) identify what was known quantitatively about the patient-reported factors associated with breast cancer survivors’ AET adherence; and (2) explore the qualitative literature on the barriers and facilitators to AET adherence. Side effects of AET, women’s beliefs about the necessity of treatment, their self-efficacy in taking AET and communicating with HCPs, the quality of patient-HCP relationships, social support, and a lack of continuity of follow-up care were all found in previous research to influence AET

adherence. These findings are consistent with the results of two previous systematic reviews that synthesized the psychosocial and healthcare factors associated with AET adherence (Moon et al., 2017; Van Liew et al., 2014). What was unique about our review was the focus on patient-reported factors in a way that paid particular attention to social and structural factors, as well as the inclusion of qualitative data. We also identified additional factors, including women’s misconceptions about the hormonal nature of AET and concerns about premature aging, that were absent from previous research.

Despite the unique perspective presented in our integrative review, the quantitative nature of most studies included in our review, coupled with the small number of qualitative studies, provided limited insight into the nuances of women’s real-world experiences with AET and other socio-structural factors influencing their decisions around adherence. In addition, our review identified features of AET non-adherence that required further investigation. For instance, more information was needed to understand how factors, such as women’s medication beliefs, perceived need for AET, social relationships, and the healthcare context shape breast cancer survivors’ beliefs about AET and their adherence behaviour.

Breast Cancer Survivors’ Experiences and Perspectives

In the next phase of our research, we wanted to talk with women to find out more about their real-world experiences in using AET. We conducted a qualitative study, using interpretive description methodology and the the- oretical lens of relational autonomy, wherein we interviewed 22 breast cancer survivors prescribed AET (Lambert, Balneaves, Howard, Chia, et al., 2018a).

One of the most important contributions of our study is the voice it gave to women’s experiences with AET, offering a more person-centred perspective on factors that influenced their AET adherence. It is important to note that women revealed how persistence with AET, not adherence, was a challenge. It was not a matter of women forgetting to take

their medication or changing the dose of AET; rather, they experienced chal- lenges in continuing to take AET for the prescribed duration.

Some women described genuinely struggling to persist with AET and shared the profound impact side effects had on their QOL. Physical side effects, such as joint pain, muscle cramps, and hot flashes, kept some women awake all night and made activities of daily liv- ing difficult. Physical symptoms also prevented some women from doing activities they enjoyed before breast cancer (e.g., hiking) that were an integral part of their social connectedness with others.

Side effects also took an emo- tional and psychological toll on some women, compromising their personal relationships, confidence in social sit- uations, and occupational roles. The latter work-related changes also altered women’s sense of identity and finan- cially impacted their family. Quite sim- ply, these were not just bothersome side effects – these were life-altering effects that many women endured on a daily basis and not surprisingly, largely con- tributed to some women discontinuing AET.

In our study, some women’s determination to persist with AET and over- come the difficult aspects of therapy was largely influenced by their beliefs about the necessity of AET, their perceived susceptibility of being diagnosed with breast cancer again, and ultimately, their fear of dying. This finding is supported by quantitative research, which suggests women who hold positive beliefs about AET and its outcomes are more likely to persist with treatment (Bright et al., 2016; Hershman et al., 2016; Stanton et al., 2014). Our research and those of others (Brauer et al., 2016;

Cahir, Dombrowski, et al., 2015; Harrow et al., 2014), found that how women cog- nitively framed their AET experience directly impacted their attitude toward AET and, in turn, their motivation to continue with treatment.

In our study, although women’s beliefs had a substantial influence on their persistence, they were also embed- ded in relationships with HCPs and faced with healthcare access issues that

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shaped their ability to persist with AET.

HCPs, including nurses, were influential in some women’s decisions about AET, which is consistent with previous research that has also found that clinical support, guidance, and information from HCPs can impact women’s self-efficacy and ability to continue with AET (Cahir, Dombrowski, et al., 2015; Farias et al., 2017; Harrow et al., 2014; Humphries et al., 2018; Wells et al., 2016). Women in our study who had access to a knowledgeable HCP, including nurses, who validated their symptoms and provided options to alleviate side effects felt supported in persist- ing with AET. Other women, however, described that a lack of timely access to a knowledgeable HCP or the perceived inability of their family physician to manage their AET-related follow-up care influenced their decision to stop treatment early.

Some women who were persistent with AET also had a difficult time with therapy – so what differentiated them from non-persistent women? The answer is not simple. Women’s persistence with AET was influenced by a complex interaction of personal factors (e.g., beliefs and values) and also broader contextual aspects (e.g., interactions with HCPs and access to care). For many women, AET persistence became a bal- ancing act over the course of their treatment and the value these women placed on certain factors shifted over time and, ultimately, tipped the scales toward persistence or non-persistence (See Fig. 2 in Lambert, Balneaves, Howard, Chia, et al., 2018b). The continued reappraisal of AET benefits and risks suggests that while side effects are often a primary reason for non-adherence (Cahir, Guinan, et al., 2015; Humphries et al., 2018; Lambert, Balneaves, Howard, &

Gotay, 2018; Moon et al., 2017; Murphy et al., 2012), there are other factors, that might also be highly influential in women’s adherence decisions and behaviours.

Thus, one of the most important findings of our study was the powerful impact of the broader socio-structural context on shaping breast cancer survivors’ willingness and ability to persist with AET by either enabling or constrain- ing their agency.

Relational Autonomy Lens

A final unique contribution of our research was the application of a relational autonomy lens, which illumi- nated how personal and socio-structural factors interacted to influence breast cancer survivors’ AET experiences and adherence. Autonomy is generally understood as an individual’s capacity for self-determination and self-gov- ernance to make decisions about their own life (Mackenzie & Stoljar, 2000).

In reaction to the more traditional and individualistic understanding of patient autonomy, which views patients as free and independent individuals, feminist scholars proposed a relational understanding of autonomy that takes into account the impact of social, political, and economic conditions on the lives of individuals (Donchin, 1995; Sherwin, 1998).

In our research, a relational autonomy lens helped to uncover elements of the healthcare environment that were problematic for women, including ineq- uities in the provision of follow-up care.

Limited access to timely care, a break- down in the patient-HCP relationship, and a lack of symptom management options were three examples that limited women in their capacity to continue AET. Applying a relational autonomy lens also led us to identify new factors not previously known to influence AET adherence, such as concerns about the structure and delivery of care, which could foreseeably be modified within the healthcare system. This includes improving transitions in care and increasing the frequency of communication with women during the initial AET treatment period.

What we found was that women’s own agency was not consistently supported by the healthcare system; even those women who wanted to benefit from AET were not always receiving the support, the advice, and the follow-up care they required. This illustrates the need to look beyond the notion that women are solely responsible for their AET adherence. We need to recognize that how care is provided also influences what women believe, what they understand, and how well they can manage the impact of AET on their QOL.

IMPLICATIONS FOR PRACTICE

Clinical practice guidelines regard- ing the optimal duration of AET have emphasized the importance of identifying strategies to improve AET adherence, particularly given recom- mendations for longer durations of AET that can last up to 10 years (Burstein et al., 2014). Medication adherence, however, is a long-standing issue in chronic disease populations that has not proven to be amenable to simple interventions.

It is not surprising that AET is no dif- ferent. To date, no interventions have demonstrated statistically significant improvements in breast cancer survivors’ AET use (Ekinci et al., 2018).

Furthermore, the evidence on interventions aimed at enhancing adherence to oral anticancer agents is limited and inconsistent (Mathes et al., 2014).

In fact, the most effective methods for improving medication adherence in any chronic disease population remain unclear (Nieuwlaat et al., 2014). The results of this research suggest that interventions to improve AET adherence will likely take more than a one-di- mensional approach to provide women with the information, support, and access to appropriate resources and care.

Nursing Engagement in AET-Related Care

Some of the breast cancer survivors we talked with in our study advo- cated for further engagement of nurses in education initiatives and follow-up care related to AET. Although few nurses were involved in the provision of AET care in this population, some breast cancer survivors named them as a trusted and, sometimes, more acces- sible resource. A growing body of evidence supports optimizing advanced practice nurses (i.e., nurse practitioners (NPs), clinical nurse specialists (CNSs) and registered nurses (RNs) with advanced training and graduate education) to deliver high-quality, sus- tainable care in a number of contexts, including oncology (Canadian Nurses Association, 2008). Several systematic reviews have demonstrated the care provided by advanced practice nurses

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results in equivalent or improved care and patient outcomes (DiCenso et al., 2014; Horrocks et al., 2002; Martin- Misener et al., 2015; Newhouse et al., 2011). In 2017, an expert panel endorsed Cancer Care Ontario guidelines regard- ing recommended models of care for cancer survivorship, which indicated the discharge of breast cancer survivors from specialist-led care to nurse-led care in an institutional setting is a reason- able option for women with no ongo- ing treatment issues (Sussman et al., 2017). In terms of AET, other researchers have also suggested that utilizing nurses in the delivery of AET-related care might provide breast cancer survivors with timely access to the care and support they need to remain adherent to AET for the full duration of treatment (Albert et al., 2011; Murphy et al., 2012;

Wengstrom, 2008).

The Canadian healthcare system, however, has yet to optimize the expertise of advanced practice nurses in healthcare, particularly in oncology (Bryant-Lukosius et al., 2015). Coupled with increasing cancer incidence and demonstrated gaps in care, this suggests that an opportunity exists to increase engagement of nurses in cancer care by optimizing and expanding exist- ing nursing roles to improve access, quality of care, and patient outcomes (Bryant-Lukosius et al., 2015). In British Columbia, a NP-led clinic for women undergoing AET was piloted in 2018 to serve the complex needs of women prescribed AET, increase capacity in medical oncology clinics in acute care settings and facilitate the successful tran- sition of care back to primary care pro- viders in the community. One of the primary objectives of this clinic is to identify and address women’s symptoms to improve their quality of life and potentially AET adherence. Pilot data dem- onstrates that women presented with a significant burden of physical, sexual, and psychosocial health symptoms that affected their quality of life (Shenkier et al., 2019). Further investigation is needed, however, to determine how to best engage oncology nurses in practicing to their full scope when providing care to women taking AET.

Patient education. Enhancing patient education is one approach that has shown some effectiveness in increasing medication adherence. A recent systematic review of adherence interventions found that patient education that was personalized and repeated resulted in improved adherence to medications for chronic diseases (Kini & Ho, 2018). In relation to AET, there is begin- ning evidence to suggest that women who do not take AET as prescribed lack knowledge about AET and information on associated side effects (Cahir, Dombrowski, et al., 2015). Clinical practice guidelines have also suggested that addressing women’s beliefs about AET, helping them understand the rationale for treatment, and informing them of the high likelihood of side effects might lead to improved adherence (Burstein et al., 2014). Our integrative review also indicated that women who were aware and knowledgeable about potential side effects before initiating AET were more likely to adhere (Lambert, Balneaves, Howard, & Gotay, 2018). Furthermore, our study with breast cancer survivors suggests that when HCPs acknowl- edge the presence and severity of side effects and offer options for alleviat- ing symptoms, some women feel better supported and more able to persist with AET (Lambert, Balneaves, Howard, Chia, et al., 2018b). This highlights the important role patient education and shared decision making can play in women’s experiences with care and AET adherence.

Nurse-led group visits. Another approach is to offer nurse-led group visits to women starting AET aimed at enhancing their treatment understanding, setting realistic expectations and addressing questions and concerns that often arise in the early phases of AET use. Sessions could offer education and supportive care in a group environment by providing a full overview of AET, including information on side effects and symptom management; interactive discussions; and the option to speak with a nurse one-on-one. Preliminary research suggests group medical appointments, facilitated in part by a NP, in which breast cancer survivors

learn about AET options, are a feasi- ble and acceptable alternative to individual physician appointments (Trotter

& Schneider, 2012; Vlahadamis et al., 2013). Furthermore, meta-analyses in other chronic disease populations (e.g., diabetes) suggest group medical visits can have a positive effect on clinical and patient-reported outcomes (Housden et al., 2013). There is also some suggestion that group medical visits have the potential to result in increased health system efficiencies, timely access to care, and decreased healthcare costs (Trento et al., 2005; Vlahadamis et al., 2013).

REFLECTION FOR ONCOLOGY NURSES

The experience of taking AET is per- sonally challenging for many women not only because of the physical effects of treatment, but because of its impact on their quality of life – emotionally, physically and psychologically. The complex needs of this population often requires focused care and time from a healthcare provider with expertise in breast cancer and knowledge of how to support patients in managing complex symptoms. Our Canadian healthcare system is under tremendous pressure with limited resources and cost con- straints. Given these limitations, it is not realistic, nor is it effective or sus- tainable, to expect oncologists to provide specialized care to women on long-term AET. We need to start think- ing ‘outside the box’ in terms of developing novel and innovative models of care, such as NP-led clinics, that more effectively use human and healthcare resources to address the complex needs of this population and support women to reap the full benefits of AET. Not only do we need to develop supportive care strategies to assist women undergoing AET, we also need to develop and eval- uate interventions that will better manage the range of symptoms experienced by women.

Nurses are well positioned to take the lead in providing supportive care to women undergoing AET as members of the larger healthcare team. Oncology nurses have a critical role to play in advancing the delivery of high-quality

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breast cancer survivorship care, facil- itating collaboration among multidis- ciplinary teams and advocating for women and their experiences. We are leaders in quality improvements and developing innovative approaches to care and treatment. Improving adherence to AET is an opportunity for nurses to also be leaders in shifting how we view non-adherence and creat- ing new ways of providing education, support, and care. It is well within our scope of practice as oncology nurses to raise awareness about the importance of taking these medications, help women to manage their symptoms, and meet them where they are at in order to

provide the support needed to cope with the reality of long-term AET.

Addressing non-adherence to AET is not going to be an easy fix. It will require looking beyond the personal reasons women do not adhere to how the system fails to adequately support them. Conceptualizing AET adherence as situated in, and determined by, socio-structural conditions presents an opportunity to attend to the contextual factors that either enable or constrain women’s adherence; rather than isolat- ing the responsibility for change at the level of the individual (Sherwin, 2011).

Going forward, we will need to develop novel ways of addressing

current gaps in the healthcare system to optimize survivorship care, AET adherence, and also empower and enable nurses across care settings to deliver optimal AET-related care that is responsive and patient-centred. Women need timely access to care that is evidence-in- formed and responsive, which also means that as nurses we will need the knowledge, tools, and time to provide this level of care. AET adherence is not only the responsibility of breast cancer survivors; women’s adherence is a prod- uct of the environment in which care is provided and, therefore, is also the responsibility of the larger healthcare system.

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