Survivorship Care of Older Adults With Cancer: Priority Areas for Clinical Practice, Training, Research, and Policy

INTRODUCTION

Older adults represent a growing number of all cancer survivors. In the United States, an estimated two thirds of cancers survivors—more than 10.7 million adults—are 65 years of age and older.^1,2 Adults older than 85 years of age are the fastest growing age group of survivors.³ An increasing population of older adults, earlier detection of cancer, and more effective, life-prolonging treatments contribute to a larger population of older cancer survivors. The probability of developing invasive cancer also increases with age, jumping from one in 16 for survivors of age 50-59 years to one in eight for men and one in 10 for women of age 60-69 years.⁴ Cancer is most prevalent among those older than 65 years; however, disproportionately fewer funded research studies focus on survivorship care for older adults.⁵

CONTEXT

• Key Objective

• The growing number of older adults living with cancer are a population in need of improved integration of oncology and primary care. We provide a conceptual review of topics critical and contemporary for cancer survivorship care of older adults.

• Knowledge Generated

• We begin with a review with recent frameworks for cancer survivorship care and current topics in clinical oncology for older adults to provide context and impetus. We provide a conceptual evidence-based review of the current state of cancer survivorship care of older adults (age ≥ 65 years) focused on four key domains for consideration: the integration of geriatric assessment into survivorship care, care coordination, patient and family caregiver engagement, and health equity considerations for geriatric oncology.

• Relevance

• To maintain and improve upon our ability to provide patient-centered, responsive, and equitable cancer care, our care delivery systems must adapt to the growing number of older adults living with cancer.

Although individuals are considered survivors from the point of cancer diagnosis through the remainder of their lives, cancer follow-up care generally begins after active treatment concludes. The successful development of many therapeutics has enabled survivors to live long, often decades, after diagnosis; thus, survivorship care encompasses individuals with wide ranges in time since treatment concluded. In addition, many survivors are treated with oral therapies to maintain remission, and in these cases, survivorship overlaps with the active treatment phase.

Cancer is one of several chronic conditions that affect the overall health and functioning of older adults. Multimorbidity is common and consequential in older cancer survivors; its impact on survivorship begins early in the disease course and is linked to poorer physical functioning in survivorship.⁶ Because the presence of comorbidities is associated with lower trial access and participation, multimorbid survivors are underrepresented in clinical trial research.^7,8 Yet, clinical trials set standards for clinical care—including older adults.⁹ The participation of patients of age ≥ 65 years enrolled in cancer clinical trials (approximately 32%) is disproportionate to the percentage of those diagnosed with incident cancers (approximately 61%).¹⁰ Key stakeholders, including the ASCO, Friends of Cancer Research, and the US Food and Drug Administration, recently established working groups to examine the potential to modify clinical trial eligibility to ensure that trials reflect real-world patient populations and improve clinical trial access and participation.

The purpose of this paper is to provide a conceptual evidence-based review of the current state of survivorship care of older adults with cancer (ages ≥ 65), focusing on the following four areas: integration of geriatric assessment (GA) into oncology care for survivors, care coordination, patient and family caregiver engagement, and health equity considerations. We first provide a review of recent frameworks for cancer survivorship and current topics in survivorship care for older adults.

SURVIVORSHIP IN OLDER ADULTS: RECENT FRAMEWORKS

Over the past 15 years, several cancer survivorship frameworks have been developed to inform care. In 2005, the Institute of Medicine, now the National Academies of Medicine, published their landmark report, From Cancer Patient to Cancer Survivor: Lost in transition. This report marked the first key set of priorities for cancer survivors after treatment and identified fundamental components of survivorship care, including prevention and surveillance, management of late and long-term effects, and health promotion.¹¹ Notably, the report introduced the use of a survivorship care plan, which was envisioned as a tool to coordinate the components of survivors' care after treatment. More recently, policy makers and researchers developed the Quality of Cancer Survivorship Care Framework to guide both the assessment and delivery of quality cancer survivorship care.¹² This framework addresses five key domains of survivorship care: (1) prevention and surveillance for recurrence and new cancers, (2) surveillance and management of physical effects, (3) surveillance and management of psychosocial effects, (4) health promotion and disease prevention, and (5) surveillance and management of chronic medical conditions. Although the Quality of Cancer Survivorship Care Framework provides a comprehensive overview for the delivery of quality survivorship care, recommendations include tailoring care to the needs of specific survivors. Care for the older adult with multiple chronic conditions within this framework is necessary, particularly for the surveillance and management of chronic conditions care domain.⁶

Several consensus reports expanded the 2005 Institute of Medicine survivorship care recommendations by focusing on the specific needs of older adults.^13-15 The reports emphasized that the effects of cancer and its treatment are often exacerbated by comorbidities prevalent in older adults, and that clinicians must consider acute, late, and chronic side effects from cancer treatment in developing survivorship plans to mitigate physical sequelae.¹³ A subsequent report noted concern that implementing survivorship care plans alone may have little impact on outcomes for older adults.¹⁴ The report instead recommends shifting to a tailored survivorship care planning process, which includes five key components: (1) a GA of survivorship needs, (2) development and initiation of a survivorship care plan by an interprofessional team and tailored based on GA, (3) identification of key members of the interprofessional team needed for specific components of care, (4) systematic tracking of care plan goals, and (5) assessment of a change in needs, which would stimulate a subsequent adjustment of the care plan. This report also brought attention to common long-term effects of cancer in older adults, including fatigue, cognitive impairment, chemotherapy-induced peripheral neuropathy, physical function, and osteoporosis.¹⁴

New care delivery approaches have emerged to address older adults' needs, including multidisciplinary geriatric oncology clinics¹⁶ or distributed subspecialty expertise, such as services in psycho-oncology,¹⁷ cardio-oncology,¹⁸ and other fields at the intersection of cancer and multimorbidity. Palliative care approaches, once exclusively administered in end-of-life care, are increasingly offered to survivors to manage symptoms and address psychosocial concerns, ultimately affecting quality of life.¹⁹ An important challenge for the field will be to coordinate specialized services for older adult cancer survivors that are stratified, tiered, and tailored to individual needs. At the same time, new care delivery approaches should minimize disruption for older adults who are in the process of transitioning beyond active treatment.

Any care delivery model must, however, address the complex interplay between an already overburdened oncology workforce²⁰ and the projected growth of this population.¹ The complex survivorship needs of older adults warrant innovative models of survivorship care that use risk-stratified care tailored to individual needs.²¹ This personalized approach triages survivors to distinct care pathways based on their specific needs, ability to manage their own care, types of providers that their care requires, and level of social support. Research is needed in this area, including methodological innovations to inform risk stratification and enhance efficiency of care allocation for older adults with cancer.²²

CLINICAL CARE DELIVERY FOR OLDER ADULT CANCER SURVIVORS

As the number of older adult cancer survivors increases, new challenges and opportunities to deliver high-quality, comprehensive survivorship care have also emerged. Contributors to this changing population and these new opportunities include contemporary cancer treatment strategies newly available to older adults, availability of data that directly reflect the experiences and outcomes of older adults with cancer, and the emergence of new delivery models that promise better ways to deliver high-quality survivorship care.

An increasing number of older cancer survivors receive concurrent therapies, each with their own unique toxicity profiles, whether for chronically controlled malignancies (eg, Bruton tyrosine kinase inhibitors²³ in chronic lymphocytic leukemia or tyrosine kinase inhibitors²⁴ in chronic myeloid leukemia), advanced or metastatic disease (eg, immune checkpoint inhibitors²⁵ in melanoma and lung cancer), or maintenance therapies (eg, immunomodulators in multiple myeloma²⁶). As a result, a growing number of cancer survivors include individuals cycling on and off or continuously receiving cancer-directed therapies, with an increasing number receiving oral medications.²⁷ These treatments may cause, exacerbate, or otherwise interact with other comorbidities frequently found in older adults. For example, atrial fibrillation is commonly seen in individuals treated with Bruton tyrosine kinase inhibitors.²⁸ Other treatments may stimulate secondary malignancies, necessitating increased vigilance in older cancer survivors. Toxicity of cancer treatment, particularly radiation and anthracycline, on the cardiovascular system remains an important research area.²⁹

The benefits of advances in treatment are increasingly available to older adults with cancer, but these opportunities also introduce new questions for survivorship care. The late and long-term effects of complex cancer treatment strategies remain poorly understood in older adults.³⁰ For example, the advent of reduced-intensity conditioning facilitated the extension of allogenic hematopoietic cell transplantation to adults up to age of 80 years with acute myeloid leukemia and other hematologic conditions.³¹ Chimeric antigen receptor T-cell therapy has been delivered to adults in their mid-80s,³² with initial use in non-Hodgkin lymphoma but expanding indications. The Bone Marrow Transplant Clinical Trials Network 1704 CHARM study³³ and other efforts are determining the ability of older adults to tolerate intensive treatment. Although newer therapies show promise and impact on survival and other outcomes, more work is needed to elucidate their toxicities and long-term effects on older adult cancer survivors.

Tools to help providers determine how older patients feel and function during and after cancer treatment are moving from research to routine clinical practice. Advances in the development and implementation of comprehensive GAs,³⁴ ePROs³⁵, and wearable sensors^36-38 have facilitated a better understanding of the impact of cancer and its treatment upon function and quality of life in older adults.³⁹ Furthermore, accumulating evidence recognizes the role of physical activity to improve lifespan,^40,41 mitigate the effects of cancer upon physical and mental health, prevent new or exacerbated comorbidities induced by cancer therapy, and reduce the risk for developing primary disease recurrence and possibly secondary cancers.⁴² Wearable sensors and electronic patient reported outcomes can be integrated into programs that promote physical activity or help older adults with cancer transition to healthy survivorship. These programs include health coaching⁴³ and cancer rehabilitation.^44,45 Increasingly, multicomponent interventions for symptom management among older adults are being tested, including adaptive trial designs to further tailor interventions for individual survivors.⁴⁶

CRITICAL AREAS OF FOCUS AND RECOMMENDATIONS FOR IMPROVING SURVIVORSHIP CARE OF OLDER CANCER SURVIVORS

The next sections outline four major areas of importance for the survivorship care of older adults (Fig 1): (1) use of GA to tailor care planning, (2) innovative models to improve care coordination, (3) patient and caregiver engagement, and (4) health equity considerations. Table 1 provides a list of clinical practice, education and training, research, and policy recommendations in each of these areas guided by the research to date.

FIG 1.

Critical areas of focus for older adult cancer survivorship care.

TABLE 1.

Clinical, Education and Training, Research, and Policy Recommendations for Older Adult Cancer Survivorship Care

Integrate GA to Tailor Care Planning

GA can be used to meet the unique needs of older adult cancer survivors.¹⁴ Given the toxicities of many cancer therapies, GA can be used to guide treatment decision making, adjust treatment plans,³⁰ and incorporate advance care planning within the context of survivorship care planning.⁴⁷ In 2018, ASCO issued a formal guideline recommending that GA be used to identify vulnerabilities not routinely captured in standard oncology assessments⁴⁸; however, limited awareness and barriers to implementing GA, including lack of time and staff, persist.³⁴ The International Society of Geriatric Oncology published detailed recommendations on how to perform brief GA using various measures and tools,⁴⁹ including the Geriatric 8—a scale that takes a few minutes to deliver and that covers age, body mass index, nutritional intake, weight loss, mobility, cognitive problems, use of prescription medications, and health status—a screening tool with high sensitivity for predicting the need for further assessment.⁵⁰ Screening tools like the Geriatric 8 can be deployed at several points across the survivorship care continuum to monitor for changes in health status and onset of frailty. Recently, International Society of Geriatric Oncology recommended incorporating GA to aid cancer treatment decision making amid the COVID-19 pandemic and deploying select geriatric screening tools remotely to overcome access barriers and identify patients with cancer needing more comprehensive assessment.⁵¹ Similarly, using personalized risk-stratified cancer follow-up care models may ensure better health outcomes for survivors and more efficient health care resource use.²¹ Some of these models may be informed by multiple data sources that could benefit from new modeling approaches, such as natural language processing methods and machine learning, to maximize prediction precision with existing data inputs.⁵²

Several groups, for example, the Cancer and Aging Research Group, provide resources and guidance on integrating GA into survivorship care planning.¹⁵ Flexible approaches to GA implementation will likely be needed since geriatricians have limited involvement in routine practice.⁴⁶ Multidisciplinary team members, including social workers, physical and occupational therapists, and nurses, may be effective at implementing geriatric management interventions.⁴⁶ The Association of Community Cancer Centers also offers resources to enhance geriatric oncology care.⁵³ Organizations can complete the Geriatric Oncology Gap Assessment to determine gaps in care and resources; tools are shared supporting the improvement plan. These areas include, but are not limited to, functional status, cognition, comorbidities, and screening. Using validated, simple GA tools like the Geriatric Oncology Gap Assessment can facilitate routine assessment for older adults with a history of cancer. The value of GA to older adult survivorship care suggests a role for its inclusion in quality measurement.

Innovate Models of Care Coordination

The complex needs of older adult cancer survivors necessitate coordination of care between providers, patients, and caregivers. For older adults with cancer and chronic conditions, care coordination requires information exchange, including efficient electronic health record data sharing and sequencing treatment and follow-up care to ensure that survivors' needs are met. In fact, one study demonstrated that among older cancer survivors, perceived care coordination is worse with increasing age.⁵⁴ Older adults may experience unmet needs in care coordination for several reasons, including difficulties navigating health care systems, challenges managing polypharmacy, and lack of social support. Care fragmentation is associated with poor outcomes, including worse symptom control, medication errors, adverse events, and underutilization and overutilization of care.⁵⁵ Effective care coordination for older adult cancer survivors will therefore require innovative models of survivorship care.

The term model of survivorship care refers to the delivery of follow-up care, including the type of care delivered, when this care is delivered, and by whom. Several models have been suggested to coordinate care for cancer survivors, including shared care, risk-stratified care, and multidisciplinary survivorship clinics.⁵⁶ Regardless of the model, care coordination for older adults requires engagement of primary care providers. As such, it is critical to train primary care providers, including advanced practice practitioners, in the care of older adults who are survivors and also integrate them as members of the survivorship team.⁵⁷ A key limitation of this approach is the need to sustain a robust, effective, and resilient supply of clinicians to support cancer survivors.²⁰ Similar to oncology, primary care and geriatric medicine also face an inadequate workforce supply paired with chronic overwork among providers. Recognizing these challenges, in 2019, the National Academies of Medicine proceedings, Developing and Sustaining an Effective and Resilient Oncology Careforce, provided recommendations to rapidly increase the oncology workforce. Successful models of survivorship care coordination for older adults will therefore need to accommodate these workforce shortages.

Two promising intervention strategies to enhance care coordination may particularly benefit older adult cancer survivors. A systematic review of care coordination studies found that patient navigation and home telehealth interventions improve care coordination for patients with cancer.⁵⁵ Although patient navigation has focused largely on follow-up after abnormal screening and reducing barriers to receiving treatment, a growing number of interventions evaluated the role of navigators for cancer survivors. For older adults, patient navigators could help survivors and their caregivers coordinate care and treatments among providers. Navigators could focus on assessing for medication interactions and ensuring management of chronic conditions and surveillance for recurrence and subsequent cancers. Hub-and-spoke models of collaborative learning, including Extension for Community Healthcare Outcomes and Extension for Community Healthcare Outcomes-like models,⁵⁸ can expand to include geriatric oncology survivorship care. New partnerships with long-term care facilities, many of which care for older adults with a history of cancer, can also be fostered. Finally, tools to assist remote monitoring and aging-in-place could be informative for cancer symptom management and surveillance of late and long-term effects.

Telehealth has become a primary mode of communication and coordination of oncology and survivorship care during the COVID-19 pandemic; notable benefits include reduced travel burden for survivors, which allows for more timely discussion of needs and modification of care plans.⁵⁹ However, older adults may experience increased challenges including broadband accessibility and capability, digital literacy, limited English proficiency, and access to quality devices. As telehealth becomes a model of care to expand reach to cancer survivors, ensuring equitable access and training for all older adult cancer survivors must be a priority. Such disruptive and promising technological changes must be guided by partnerships with community-based and patient advocacy organizations.

Engage Survivors and Caregivers as Part of the Care Team

At the center of improving care coordination is engaging survivors and their informal caregivers. During active treatment, caregiver engagement can lead to better adherence to therapy, optimized care utilization, lower distress, improved clinical trial recruitment and retention, and better health outcomes among patients.^60-62 For research programs, one example is the Stakeholders for Care in Oncology and Research for our Elders board. With funding from the Patient-Centered Outcomes Research Center, a research team created Stakeholders for Care in Oncology and Research for our Elders board as a patient or caregiver stakeholder group that provided feedback and recommendations to the research team to elevate care, support service, and improve outcomes for patients ≥ 65 years of age with cancer and their caregivers.⁶³ Findings included the need for creating effective mission statements, holding regular meetings with flexible formats and accessible materials, providing administrative support, and collaborating authentically with the principal investigator and research team.⁶³ Establishing a patient or caregiver group with these components may ultimately yield more patient-centered care delivery.

As older adults transition from active treatment into survivorship, caregivers serve as a critical link between clinicians and survivors, as well as the coordinators of survivors' health care providers. Family caregivers are the individuals most likely to help older cancer survivors arrange services, manage long-term symptoms and side effects, and monitor adherence to maintenance therapies.⁶⁴ The family caregivers' presence in cancer clinical encounters lengthens visit time and improves patient-centeredness, particularly in patient-provider race-discordant encounters.⁶⁵ Poorer caregiver well-being is linked to worse perceived quality of care,⁶⁶ yet caregivers often have unmet needs. One cohort study found that more than one third of caregivers reported unmet psychosocial needs 5 years after the diagnosis of their care recipient.⁶⁷ Innovative ways to meet needs and engage caregivers in survivorship care, including providing personalized materials that can be accessed flexibly (ie, when needed), are called for.⁶⁸ In addition, caregivers should be connected to information about long-term service and supportive resources for older cancer survivors.

Despite widespread appreciation of the invaluable work performed by caregivers, there is high state-to-state variability in the quality of long-term services and supports for older adults and their family caregivers.⁶⁹ The Caregiver Advise Record Enable act has been passed in most states to help standardize practice for communicating with caregivers of hospitalized patients⁷⁰; however, there is no analogous policy for the caregivers of cancer survivors who receive care in outpatient settings. The Recognize, Assist, Include, Support and Engage Act was passed in 2018 to establish a US national family caregiver strategy to address assessment and service planning, supports for caregivers (including respite options), and financial and employment issues.⁷¹ As of this writing, the plan remains under development, and attention to how it could affect older cancer caregivers specifically is warranted.⁷² Among cancer survivors, hospitalization is more common in older-aged adults; this legislation will greatly affect caregiving norms for all hospitalized cancer survivors, particularly for older adults.

Integrating patient- and caregiver-reported outcomes into cancer clinical trials⁷³ and routine clinical practice may enhance engagement,^74,75 and incorporating these assessments is on the rise. More research is warranted to ensure patient safety and value over burden.

Apply a Health Equity Lens

Advances in diagnostic, treatment, and survivorship care for older adults are not always available to all survivors, and age is one attribute that intersects survivor characteristics and identities linked to equity. Health disparities present as downstream consequences of accumulated stressors influenced by multilevel social determinants, including structural inequities and social injustices.⁷⁶ Persistent, stalled, and sometimes worsening racial or ethnic, urban or rural, and LGBTQ disparities exist in cancer survivorship outcomes for older adults. Survivorship cohorts consisting of diverse older adult patient and caregiver post-treatment populations are limited. Kilbourne's Disparities Research Framework categorizes studies as detecting, understanding, and/or intervening upon disparities to contribute to a collective synthesis and scientific agenda; thus, it is useful for conceptualizing health equity research on older cancer survivors. The National Cancer Institute's recent portfolio analysis of health care delivery research grants demonstrates that most studies focus on the detection and intervention phases of the Kilbourne's research continuum, with far fewer focused on understanding causes of disparities.⁷⁷

Regarding detection of health disparities, several examples exist of the persistence of disparities in cancer outcomes post-treatment among older survivors. Racial or ethnic disparities in mental health among older adults with a history of cancer have been increasing since the late 1990s.⁷⁸ Older rural cancer survivors report lower vitality and social functioning in addition to emotional and physical role limitations after cancer than urban survivors.⁷⁹ Rural colorectal cancer survivors report higher treatment-related financial hardship and nonadherence to surveillance colonoscopy than urban survivors.⁸⁰ In addition, rural survivors may need more intense interventions to promote health-promoting behaviors, including high fruit and vegetable and low saturated fat consumption.⁸¹

Inequities in cancer survivorship outcomes among older adults may be considered within the broader context of the social determinants of health.⁷⁶ Constraints on health information flow, including limitations on health-related internet use among cancer survivors, are more common among older, rural, and ethnic minority survivors.⁸² A recent review details several biological mechanisms for how social determinants and structural racism specifically are embodied by and lead to cancer health disparities among Black women.⁸³ Black, female cancer survivors face challenges in both detecting and managing late effects of cancer treatment⁸⁴ and surveillance mammography.⁸⁵ Patient navigation, however, has been shown to have beneficial effects in both Black and White older cancer survivors.⁸⁶ The lack of systematic surveillance of sexual orientation and gender identity in cancer registry data,⁸⁷ which stems from lack of implementation of standardized documentation in electronic health records,⁸⁸ challenges progress on understanding and intervening upon barriers to quality health care among LGBTQ survivors. A recurring challenge stems from care fragmentation and lack of sufficient expertise in the late and long-term effects of cancer, particularly in community oncology settings. Better integration of primary care providers trained to recognize late and long-term effects in older adults could help improve care quality for populations with already limited access.⁵⁷

Interventions to address cancer health disparities among older adults are emerging and show promise but will require multilevel and multisector engagement, particularly with community-based patient advocacy organizations. Recognizing how social determinants manifest as social needs that critically disrupt access to care is fundamental to adequately addressing cancer health disparities. Recently, the COVID-19 pandemic has highlighted how gaps in broadband internet service presents barriers to access telehealth, an increasingly important delivery model for survivorship care. A recent plan by the American Cancer Society to understand and address social determinants to advance cancer health equity presents bold recommendations to address structural inequities, institutional barriers, and living environments.⁷⁶ The plan calls for making explicit provisions in all public policies for disadvantaged older adults with cancer to narrow resultant health and racial or ethnic disparities. Achieving equity for older cancer survivors will require improvements in all three domains.

In conclusion, our ability to provide patient-centered, responsive, and equitable cancer care will require adapting to the growing number of older adults living with cancer. Current observational research and corresponding interventions have predominantly focused on the emotional well-being and physical health of survivors; however, less attention has been paid to research on both the patterns of and quality of care provided to older adult survivors.⁸⁹ Continuous clinical quality improvement includes an emphasis on integrating GA and creating new models to enhance care coordination. Collectively, we can build on lessons learned from integrating survivorship care planning and our experiences in expanding telehealth during the COVID-19 pandemic to carry forward into the future. Centering health equity must remain or in some cases become a priority in older adult cancer survivorship care and research. Better integration of family caregivers into care teams holds potential for improving care quality and patient-centered communication. Finally, older adult cancer survivors can thrive when we engage multidisciplinary clinicians, researchers, funders, policymakers, advocates, and survivors and their caregivers in cancer care.

AUTHOR CONTRIBUTIONS

Conception and design: All authors

Collection and assembly of data: Erin E. Kent, Michelle A. Mollica

Data analysis and interpretation: Erin E. Kent, Michelle A. Mollica

Manuscript writing: All authors

Final approval of manuscript: All authors

Accountable for all aspects of the work: All authors

AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

Survivorship Care of Older Adults With Cancer: Priority Areas for Clinical Practice, Training, Research, and Policy

The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated unless otherwise noted. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO's conflict of interest policy, please refer to www.asco.org/rwc or ascopubs.org/jco/authors/author-center.

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