key: cord-1013176-ww229ahy
authors: Jones, Jennifer M; Saeed, Hina; Katz, Matthew S; Lustberg, Maryam B; Forster, Victoria J; Nekhlyudov, Larissa
title: Re-Addressing the Needs of Cancer Survivors during COVID-19: A Path Forward
date: 2020-12-26
journal: J Natl Cancer Inst
DOI: 10.1093/jnci/djaa200
sha: 637a6d075b30219479c72d2df2a4df19de9f9082
doc_id: 1013176
cord_uid: ww229ahy

The growing number of cancer survivors along with the high prevalence of cancer-related physical and psychosocial effects pose important and pressing challenges to health systems. The coronavirus disease 2019 (COVID-19) pandemic has led to further stressors on cancer survivors and the healthcare systems. As the pandemic continues to have substantial impact on the world, it is critical to focus attention on the healthcare needs of cancer survivors. In this commentary, we propose an adoption of essential steps that should be part of a continuous adaptive approach to promote effective cancer survivorship care during ongoing COVID-19 waves and beyond.

Over 17 million individuals are living with a personal history of cancer in North America 1 and millions more around the world. 2, 3 Prior to coronavirus disease 2019 , the growing number of cancer survivors along with the high prevalence of cancer-related side effects posed important and pressing challenges to health systems. The pandemic has led to further stressors on cancer survivors and the healthcare systems. [4] [5] [6] Earlier in the pandemic, several editorials were written to highlight the potential effects of COVID-19 on the health and healthcare of cancer survivors. 4, 6, 7 While suspected yet unconfirmed at the time, recent studies identified cancer diagnosis to be a risk factor for acquiring COVID-19 8 and for its associated negative outcomes including morbidity and mortality. [9] [10] [11] [12] Specifically, people at risk are older, currently receiving chemotherapy, have lung cancer or haematological malignancies, and those who have completed therapy within 5 years. [11] [12] [13] [14] After the initial disruptions and delays in routine cancer treatment and follow-up 9, 15, 16 , there have been implementation of strategies to reduce risk of exposure and minimize in-person visits 15, 17 along with the development of pandemic-focused priority care guidelines. 18, 19 While necessary, the potential negative consequences of these changes in healthcare delivery are concerning. These concerns were highlighted in a recent editorial by Norman Sharpless, Director of the US National Cancer Institute, in which he noted a substantial drop in screening tests resulting in delayed diagnosis and suboptimal care for people with cancer since the start of the pandemic, which will likely have an impact on cancer mortality. 20 Further, a recent paper that examined the impact of COVID-19 on cancer care across the globe found 88% of centers faced challenges in providing usual cancer care and up to 80% of patients in some centers had exposure to potential harm. 15 Survivors have also reported negative consequences of COVID-19 on cancer care and follow up. 21, 22 As the duration and course of the pandemic is uncertain, it is crucial that attention be placed on resumption of services along the cancer care continuum when safe and feasible. 20, 23 In this commentary, we go beyond the previously published perspectives to propose the adoption of essential steps that should be part of a continuous adaptive approach to find the optimal balance between minimizing the negative impact of the fluctuating COVID-19 pandemic while promoting effective cancer survivorship care (see Figure 1 ). Our approach is based on a previously published model for cancer diagnostic services. 24

In guiding this commentary, we sought to capture the rapidly evolving evidence and to include perspectives of multiple stakeholders. First, we reviewed numerous sources, including relevant literature and national and international guidance statements (i.e. American Society of Clinical Oncology (ASCO), European Society of Medical Oncology (ESMO), American Society of Therapeutic Radiation Oncology, Cancer Australia), advocacy group recommendations (e.g. National Coalition of Cancer Survivorship (NCCS), American Cancer Society). Second, we drew insights from two Twitter chats focused on COVID-19 and its impact on cancer survivors. The first was hosted by Cancer Survivor Social Media (#CSSMchat) on April 15 th , 2020; the second was hosted on May 16-17 th , 2020 by the Radiation Oncology Journal Club (#radonc #jc). Both events included participation by the authors, patients/advocates and colleagues around the globe and discussions were based around the themes of potential impact on survivors and need for action to mitigate the impact.

With the global pandemic marked by ongoing temporal and spatial variation, the development of appropriate policy and healthcare delivery planning requires projections of possible COVID-19 scenarios at the community, regional and national levels. 25 The use of consistent measurements of objective and comparable data is vital in order to assess the effectiveness of mitigation strategies and inform ongoing efforts. 26 As the prevalence of COVID-19 is critical in driving decisions, collaboration and sharing of accurate data amongst healthcare providers and public health agencies is paramount. This, in turn, results in a risk-based triaging of available resources and an assessment of care capacity for cancer survivors.

COVID-19 has led to decreased utilization of healthcare services with priority placed on initial cancer diagnosis and treatment. 15 Cancer survivors may have also been fearful of coming into healthcare settings due to concerns about susceptibility, leaving them to manage physical and practical issues and worries on their own. 5, [27] [28] [29] While there have been recent public messaging advising patients to report unusual symptoms, these have not focused on those with prior cancers. Effective outreach involves collaboration on a local, regional and national level, targeted to both patients and caregivers, and must be a priority across the cancer care continuum. Although patient education is an important aspect of delivering quality oncologic care, it is now even more important to educate patients to monitor and report any suspicious symptoms indicative of new, recurrent or progressive disease. Public health agencies, cancer societies, charitable organizations, and academic centers should develop and disseminate information specifically tailored for those patients with prior cancer.

Post-treatment follow-up care of cancer survivors has dramatically changed as a result of COVID-19, and many surveillance visits and imaging have been delayed or cancelled 5 . While majority of the guidelines provide specific frequency ranges for surveillance testing (such as every three to six months), most are based on consensus, rather than evidence. As such, it maybe be reasonable to delay surveillance during COVID-19 surges based on medical providers' consideration for individual factors, including disease type, treatment exposures, as well as COVID-19 risk factors. Symptom-based monitoring, which may be remote, may offer benefits over routine, "traditional" surveillance. 30 It is important that in considering surveillance modifications, medical providers take caution in that some patients might perceive this as lack of standard care and thus experience anxiety. Sensitivity toward and adjustment of surveillance modalities to patient preference may be needed. Patient resources regarding the impact of COVID-19 on cancer care have been developed and can be helpful in preparing patients and their family understand how the pandemic will affect care provision (i.e. ESMO, ASCO Cancer.Net).

Telemedicine with bi-directional messaging to facilitate self-reported monitoring of cancer patients with COVID-19 including any disease specific or social concerns 31, 32 can play a meaningful role for cancer survivors. Although telemedicine is not new, its accelerated dissemination was precipitated by the pandemic 33 and is poised to become an important pillar of cancer care. 34 However, while secure telemedicine with its incorporation of risk benefit balance has been a useful and important tool to deliver care since the onset of the pandemic, it is not in itself the solution. 35 Efficient and meaningful telemedicine requires training for patients, caregivers and clinicians as well as having the "right" technology, appropriate infrastructure and private space for the virtual visits. Impaired hearing and vision, linguistic barriers, cultural limitations and cognitive deficits in patients pose further challenges necessitating a more personalized virtual approach. Often there are digital inequalities or disparities in both the ability to access and to use telemedicine, within local, regional, national, and global populations. 36, 37 In such cases, alternative route of communication such as telephone conversation can be potentially helpful. Communication guides that may assist clinicians with oncology-specific language to respond to patient questions about changes in delivery of cancer care during the pandemic are available online. 38, 39 There continues to be widespread issues with regulations regarding financial incentives and reimbursement associated with telemedicine. To address this evolving situation, ASCO recently issued an interim position statement on telemedicine in cancer care which included recommendations on federal and state coverage, health equity, patient education, and research. 40 With the current crisis posing additional challenges to communities that have traditionally faced barriers to healthcare access, sole reliance on telemedicine is not advised and appropriate triaging considering the risk of COVID-19, the urgency of the patient needs, and patient preferences should dictate the route of communication 4 . Moving forward, it is important that healthcare organizations expand beyond the traditional center walls to leverage multidisciplinary community-based care to serve those for whom virtual care is inappropriate or inaccessible. 41

While remote monitoring using telemedicine may be adopted; when requires, physical examination should not be avoided. 42 There has been a rapid reorganization of cancer systems in order to ensure timely and essential cancer care while at the same time minimizing risk of exposure to COVID-19. 23 Recent guidance from organizations such as ASCO provides immediate and short-term recommendations that cancer centers and oncology practices can adopt. 19 It is important to emphasize that there is no "one size fits all" approach to delivering cancer care during the COVID-19 surges and individualized treatment decisions must be made. Priority should be given to those whose treatments and testing have been delayed during "shutdown" and driven by benefit versus risk analysis as well as therapeutic intent. [43] [44] [45] In case where faceto-face clinical encounters are warranted, safety should be optimized through patient outreach and education. Patients should be given practical advice and instructions to encourage safe behaviour when coming in for routine checks or other follow up care. Healthcare facilities can promote adaptation to "new normal" by delivering "care with caution", following standard COVID-19 precautions.

Recognizing the challenges of telemedicine, an opportunity to empower patients is provided by availability of real-time online access to electronic records, including encounter notes written by clinicians (referred to as "open notes") through patient portals. 46 Such practice exists in Nordic countries as well as several institutions in the United States and continues to grow worldwide. [47] [48] [49] Encouragingly, new federal laws in the United States (US) mandate that providers must extend open notes to all patients starting from November 2nd, 2020. 50 While there is concern that patients' access to their oncology notes will trigger anxiety or confusion, research to date suggests that patients find this access to be useful, report improved understanding about their diagnosis, treatment risks and side-effects, and learn important information that they had missed during clinical visits. [51] [52] [53] [54] Accessibility to open notes has been cited as crucial for patients' mental wellbeing. 46 The use of open notes is highlighted by the pandemic and has the potential to serve patients in the future.

Adoption of evidence-based, innovative models of care, including shared follow-up and survivorship care along with streamlined collaborative workflows amongst primary care and oncology services was insufficient in the pre-COVID era. The need for such a workflow has been intensified by the pandemic and can facilitate timely evaluation of potential cancer symptoms as well as divert COVID-19 evaluations for cancer patients to non-oncologic settings, thus decreasing risk of transmissions amongst this vulnerable cohort. The fundamental role of primary care may also be well-poised to identify cancer survivors at risk of suboptimal or delayed surveillance due to non-compliance. Further, optimization of primary care with efficient use of triage-based telemedicine or personal interaction may support cancer patient follow up and assist in sustaining their physical (i.e. management of chronic medical conditions) and mental health. In order to support this, it is important to establish and embed processes and infrastructure that encourages the development and sharing of patient follow-up care plans between multidisciplinary health professionals who are providing survivorship care.

Resources and education of multidisciplinary healthcare providers to support delivery of person-centred and evidence-based models of follow-up and survivorship care is needed 42 .

Development and use of standardised templates to support care coordination and agreement of alternative follow-up shared care arrangements has been proposed. 42 Further, processes to support rapid communication between primary and tertiary care settings for clinical issues requiring cancer specialist consultation or advice needs to be established. 42

The United Nations has warned of a global mental health crisis due to Cancer survivors already face uncertainty and are at higher risk of depression and anxiety compared to the general population. [56] [57] [58] COVID-19 has likely exacerbated this due to lack of access to screening and recommended care coupled with worry over increased susceptibility to contracting COVID -19. 7, 59 Physical distancing protocols, which continue in most areas of world has the potential to amplify anxiety, distress and depression. Additionally, socioeconomic and sociopolitical disparities can further exacerbate psychological morbidity in cancer patients. [60] [61] [62] Proactive steps can be taken to address psychosocial needs of cancer survivors. 63 To begin, it is important to validate the anxiety that individuals are feeling; compassion and valuebased approaches may be beneficial. 64 Next steps involve identifying those who need extra support can be facilitated through simple screening tools (i.e. distress thermometer) as well as emerging tools to assess fear related to COVID-19. 65 Moving forward, it is critical that expansion of mental health services is prioritized to increase the capacity to address the challenges caused by the pandemic. The use of triaging and stepped care approaches 66 will require systems that are well designed to screen, identify and deliver this care. Initiatives such as Helplines (i.e.

Cancer Support Community Helpline) and peer "check in" could make a difference in the early stages of social isolation. 67 Further, the use of telemedicine and other technology platforms can be vital components of stepped care for acute mental health crisis management as well as nonurgent care and support. 63

For many, COVID-19 and the need to self-isolate or quarantine has had a very negative impact on lifestyle behaviors including physical activity, diet, sleep, and alcohol consumption. [68] [69] [70] [71] [72] [73] [74] Given the importance of promoting physical and mental health and overall wellbeing 75 , scientific and medical organizations including the World Health Organization (WHO) have released recommendations to promote physical activity at home during the COVID-19 pandemic. The recovery and quality of life of cancer survivors can be at risk with surges of COVID-19 and cancer survivors may be particularly vulnerable to the impact of the pandemic on lifestyle behaviors. Physical inactivity, sedentary behavior, and poor nutrition are already highly prevalent in cancer survivors both during and after treatment 76 and are associated with chronic medical conditions, as well as overall poor physical and mental health and increased mortality risk. [77] [78] [79] [80] With limited access to gyms and exercise programs along with the need to enact more strict physical distancing measures, participation in healthy behaviors among cancer survivors is likely to further decline. At the same time, social distancing may present an opening to make lifestyle changes as some typical barriers that interfere with an active lifestyle adoption (e.g., lack of time, work, traffic) have been removed. 81 Clinicians and other health-care practitioners should proactively prescribe physical activity to their patients during the pandemic and encourage other healthy strategies such as sleep hygiene and nutrition. 7 Verbal coaching, brochures and pamphlets as well as effective use of social media platforms can assist with promoting healthy behaviors. Remotely supported home-based exercise programs that integrate safe and simple exercises may be recommended. 82 Cancer survivors who are exercisenaïve or who have pre-existing health problems and/or exercise contraindications should consult with their primary care provider, oncologist and/or an exercise professional before starting any new exercise program; initial supervision is recommended for these individuals. 83 As with any lifestyle change, cancer survivors should be encouraged to develop small realistic goals that can be progressed over time. 84 

Cancer survivors should be counseled that social interactions are not just acceptable but also beneficial, (as long as local health strategies and measures taken to ensure safety are not violated). As with exercise activities described above, the use of virtual social platforms may be helpful in increasing social interactions in a safe manner. 85 Many gyms, places of worship, and social groups such as book clubs have transitioned to online platforms. Workplaces are conducting meetings and creating virtual workspaces for people to connect over video connections. Cancer centers and community cancer support programs have also developed online programs that should be encouraged to help support cancer survivors. Future efforts should be geared towards developing more engaging and intuitive platforms to encourage meaningful social interactions during pandemic waves and beyond.

Cancer survivors already face burdens associated with financial burdens and are particularly at risk for additional negative financial effects as a result of COVID-19, thus affecting quality of life as well as morbidity and mortality. [86] [87] [88] [89] Survivors whose employment is deemed "essential" and cannot be conducted from home may have to weigh the benefits of work with potential increased exposure depending on their occupational risks and may be forced into temporary unemployment. For other, their financial situation gives them no option but to continue going to work, potentially resulting in increased risk of COVID-19 transmission and associated distress. 41, 90 This must be considered in light of the research which shows that gaining new employment after job loss is more difficult for cancer survivors compared to the general healthy population. 91 Those individuals who are self-employed or work for small employers may also face unique short-and long-term uncertainties. Being able to work has been shown to affect the quality of life of cancer survivors as having a job contributes to feelings of normalcy, resilience, and meaning. 92 Being unemployed can also result in loss of health insurance benefit, particularly for those in the US. Such a financial situation can be detrimental for survivors who depend on insurance benefits for care and can result in psychological stress. Moving forward, it will be essential to assess and discuss access to care and risk of financial toxicity and to facilitate access to social work and resources about loss of health coverage (i.e. NCCS).

While engaging patients in goals of care discussions has long been emphasized, the pandemic has highlighted the importance of goal-concordant care in several ways. The additional risk of COVID-19 has underscored the significance of proactive advance care planning for all oncology patients. 93 As previously noted, cancer survivors most likely to develop severe COVID-19 will be older and have greater burden of chronic illness. These may (or not) be the same individuals who may wish to forgo prolonged life support and/or who may find their quality of life unacceptable after prolonged life support. 94 In the context of the pandemic, advance care planning prior to serious acute illness and revisited at the onset of serious acute illness should be a key objective. Clinicians should include clear documentation of these discussions, especially if they take place during a telemedicine visit. Several online resources can guide the providers to carry out these conversations. 39, [95] [96] [97] [98] 

As the COVID-19 pandemic continues to evolve, emerge in new areas, re-emerge or abate in others, active cancer treatment as well as other urgent and emergent conditions will likely take priority. The pandemic has uncovered and exacerbated many challenges and highlighted the limitations of traditional healthcare delivery systems. While focusing on the needs of all survivors, it is vital to address and re-address the needs of long-term cancer survivors who are already vulnerable to physical, psychological and financial effects of cancer and that are now amplified by the COVID-19 pandemic. Healthcare professionals, policymakers, and patient groups must take a systematic approach to evaluate, adopt, and refine measures needed to improve the health of cancer survivors during and beyond this pandemic.

Not applicable.

Role of Funder: Not applicable. 

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