Mitigating the Impact of the COVID-19 Pandemic on Adult Cancer Patients through Telehealth Adoption: A Systematic Review

During the first wave of the COVID-19 pandemic, the delivery of life-saving and life-prolonging health services for oncology care and supporting services was delayed and, in some cases, completely halted, as national health services globally shifted their attention and resources towards the pandemic response. Prior to March 2020, telehealth was starting to change access to health services. However, the onset of the global pandemic may mark a tipping point for telehealth adoption in healthcare delivery. We conducted a systematic review of literature published between January 2020 and March 2021 examining the impact of the COVID-19 pandemic on adult cancer patients. The review’s inclusion criteria focused on the economic, social, health, and psychological implications of COVID-19 on cancer patients and the availability of telehealth services emerged as a key theme. The studies reviewed revealed that the introduction of new telehealth services or the expansion of existing telehealth occurred to support and enable the continuity of oncology and related services during this extraordinary period. Our analysis points to several strengths and weaknesses associated with telehealth adoption and use amongst this cohort. Evidence indicates that while telehealth is not a panacea, it can offer a “bolstering” solution during a time of disruption to patients’ access to essential cancer diagnostic, treatment, and aftercare services. The innovative use of telehealth has created opportunities to reimagine the delivery of healthcare services beyond COVID-19.


Introduction
Health systems worldwide pivoted towards telehealth when the COVID-19 pandemic started [1]. This means that a range of consultations and services was delivered via telephone, video conferencing, and other messaging services [2], extending from consultations with general practitioners in primary care to specialist consultants in hospitals across medical areas, including cancer care [3]. This was particularly pertinent for cancer patients and survivors who are at greater risk of infection and developing more severe health complications compared to the general population, due to their weakened immune systems [3]. Globally, telehealth combined with other public health guidelines and initiatives, such as dedicated pathways and hubs, helped protect cancer patients and survivors from exposure to  In the current literature, a range of terms is used to describe the use of information and communication technology (ICT) to either deliver health services, transfer information, and/or provide education to patients and healthcare professionals at a distance [4]. For this study, we use the term "Telehealth" to characterise two-way communications among stakeholders [5] and their use of ICT [6,7] to enable the delivery of healthcare, exchange of [4]. For this study, we use the term "Telehealth" to characterise two-way communications among stakeholders [5] and their use of ICT [6,7] to enable the delivery of healthcare, exchange of health data, and dissemination of health-related education across geographically dispersed locations [8][9][10][11][12][13]. Research indicates that telehealth primarily focuses on the delivery of healthcare services [7,13,14], including the diagnosis, treatment, and prevention of disease and injuries [8]. The terms telehealth, telemedicine, and telecare are often used interchangeably. Telehealth is an overarching term involving clinical and nonclinical applications and encompasses both telecare and telemedicine [9]. Telecare occurs when a health-related request for assistance is made; a disease is not necessary to prompt such a request, and the other actor is not necessarily a healthcare professional [9]. Whereas telemedicine is typically more clinical, focusing on patient assessment, diagnosis, and treatment [9]. Colucci et al. [9] classify both telehealth and telemedicine as communication strategies whereby an action is taken remotely for the purpose of providing care or a cure. Telehealth also encompasses tele-radiology, tele-stroke, tele-ICU, tele-psychiatry, teleburn, tele-prescription, and virtual care [15]. The role of healthcare professionals is core to the delivery of telehealth services [8].
Data from Google Trends (an online tool for comparison of the popularity of terms searched by users of Google Search and their trends over time) (Figure 1) illustrate the relative number of searches (based on the total volume of searches over time by geographic region) for the terms "Telehealth" and "Telemedicine" since 2017. As evidenced, these terms were widely searched for during March 2020, when the World Health Organization (WHO) declared COVID-19 a global pandemic, with Google Trends highlighting telehealth as the more popular search term. The pattern illustrated in Figure 1 supports Edwards et al.'s [6] assertion that healthcare professionals are more familiar with the term telehealth compared with telemedicine. Indeed, March 2020 marks a time when frontline healthcare professionals scrambled to identify new ways to communicate with and deliver healthcare services to the most vulnerable patients [16].
There are many benefits associated with telehealth adoption; these include reported high levels of patient satisfaction with the telehealth experience [17], efficiency, privacy, comfort [18], and improved convenience, particularly for patients with physical limitations [19] as they can access important services from their own home. Other studies identify reduced fuel and parking costs and the cost of work absence [20] as financial benefits for patients. While, in their study of telehealth neonatal services, Ballantyne et al., [21] highlight avoiding traffic, not being late for appointments, and not having to arrange childcare as motivators for telehealth adoption. Advantages for healthcare providers include being able to access patients from their home offices [22] and reducing patient noshows [23]. However, some studies identify challenges such as equipment costs, patient privacy, insufficient training, and limited communication between clinicians and information technology specialists [24].
We conducted a systematic literature review examining the social, psychological, health, and economic impacts of COVID-19 on cancer patients. This review captured the The pattern illustrated in Figure 1 supports Edwards et al.'s [6] assertion that healthcare professionals are more familiar with the term telehealth compared with telemedicine. Indeed, March 2020 marks a time when frontline healthcare professionals scrambled to identify new ways to communicate with and deliver healthcare services to the most vulnerable patients [16].
There are many benefits associated with telehealth adoption; these include reported high levels of patient satisfaction with the telehealth experience [17], efficiency, privacy, comfort [18], and improved convenience, particularly for patients with physical limitations [19] as they can access important services from their own home. Other studies identify reduced fuel and parking costs and the cost of work absence [20] as financial benefits for patients. While, in their study of telehealth neonatal services, Ballantyne et al. [21] highlight avoiding traffic, not being late for appointments, and not having to arrange childcare as motivators for telehealth adoption. Advantages for healthcare providers include being able to access patients from their home offices [22] and reducing patient no-shows [23]. However, some studies identify challenges such as equipment costs, patient privacy, insufficient training, and limited communication between clinicians and information technology specialists [24].
We conducted a systematic literature review examining the social, psychological, health, and economic impacts of COVID-19 on cancer patients. This review captured the first wave of the pandemic, exploring the immediate responses of stakeholders to the crisis, thus revealing how healthcare services were taking steps to mitigate the effects of the pandemic for the most vulnerable patients. Telehealth emerged as a key theme; findings are presented here. This article is structured as follows; the next section describes the research materials and methods used and the systematic literature review execution. The following section reports the results and discussion. Finally, the conclusion considers limitations, implications arising from this study, and opportunities for future research.

Materials and Methods
The methodology for this systematic review was guided by Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [25] and the population, intervention, comparators, outcomes, context, studies (PICOCS) framework was employed [26] ( Table 1). The review's inclusion criteria were limited to studies that focus on the economic, social, health, and psychological implications of COVID-19 on cancer patients/survivors; studies written in English and published between January 2020 and March 2021. The following types of studies were excluded: letters to the editor, editorials, case studies, reports, protocols, commentaries, short communications, reviews, opinions, perspectives, and discussions (PROSPERO registration number: CRD42021246651). The search strategy was developed using a combination of free text words and subject headings relevant to CINAHL, MEDLINE, PsycINFO, PsycArticles, and EMBASE platforms and was refined using Boolean operators. The search was conducted on 31 March 2021. Caregivers, nursing and medical staff, and paediatric cancer patients "cancer" OR "oncology" OR "malignant" OR "tumour" OR "metastasis" OR "neoplasm" Intervention COVID-19 pandemic -"COVID-19" OR "coronavirus" OR "2019-ncov" OR "SARS-CoV-2" OR "cov-19" OR "severe acute respiratory syndrome coronavirus-2" OR "pandemic" Outcome economic, social, health, and psychological implications of COVID-19 on cancer patients/survivors -"financial toxicity" OR "out-of-pocket" OR "productivity" OR "absenteeism" OR "unemployment" OR "cost" OR "waiting time" OR "expenses" OR "financial stress" OR "inconvenience" OR "opportunity cost" OR "income" OR "wellbeing" OR "social isolation" OR "exclusion" OR "loneliness" OR "happiness" OR "life satisfaction" OR "fatigue" OR "insomnia" OR "psychological distress" OR "emotional distress" OR "anxiety" OR "depression" OR "post-traumatic stress disorder" OR "psychological" OR "quality of life" OR "health-related quality of life" OR "survival" OR "mortality" OR "disease progression" OR "diagnosis" OR "screening" OR "recurrence" OR "disease stage" OR "delay" OR "support" OR "surgery" OR "treatment" OR "target therapy" OR "radiotherapy" OR "chemotherapy" OR "immunotherapy" OR "hormone therapy" OR "survivorship programme" OR "follow-up-care" year of publication, country; study characteristics: aim/objective, perspective, study design, reason for inclusion; population characteristics: sample size, type of cancer, age, gender, patient, or survivor group; methods: context/setting, data source, study timeframe, data collection methods, data analysis methods; and outcome variables: economic impact, social impact, health-related impact, psychosocial impact. The JBI critical appraisal tools for cross-section, prevalence, qualitative, and cohort [27] as appropriate and CHEC list [28] for cost analyses were used to assess quality. The evidence was pooled and summarised to create an inventory of results with a narrative synthesis. Two authors (AL and AK) independently performed quality assessment. If there was conflict or uncertainty, a third author (AM) was consulted. Risk of bias in a study was considered high if the "yes" score was ≤4; moderate if 5-6; and low risk if the score was ≥7 on the JBI tools. Quality review results are presented in Appendix A.

Overview of Search Results
The search initially yielded 5383 studies, of which 167 were considered for full text review (see Murphy et al. [29] for further information). The review's inclusion criteria focused on the economic, social, health, and psychological implications of COVID-19 on cancer patients and the availability of telehealth services emerged as a key theme (See Appendix B). Overall, 37 of the 167 articles reported on the use of telehealth in delivering oncology care during the COVID-19 pandemic ( Figure 2). In this collection, many papers detailed experiences of telehealth in the USA (35%) and referred to services available for multiple/all cancer types (67%). Most of which were in a hospital setting (92%), two were in the community (5%), and one was web-based (3%).
Telehealth was employed as part of oncology services redesigned to ensure continuity of care and reduce risk of COVID-19 transmission [33,34,36,37,41,47,56]. Included in this were efforts to evaluate patients' side effects/symptoms, avoid unnecessary hospital visits post-surgery [39], and reduce outpatient department workloads during the pandemic [38]. Where available, telehealth facilitated consultations for a variety of activities including, for patients seeking information regarding their oncological treatments, symptom management and replenishing opioid medications [51] or post-surgery to evaluate patients' side effects [39]. In one instance, telehealth was employed to deliver tobacco treatment for tobacco-dependent cancer patients during the pandemic in New York City, which resulted in higher attendance and increased completion odds compared to in-person visits [42].

Satisfaction with Telehealth
The review demonstrates the rapid uptake of telehealth overall, and many studies found a high satisfaction rate amongst patients, caregivers, and clinicians [32,43,48,[50][51][52][53]55,59]. Some patients expressed the desire to continue telehealth visits in the future [37,50,54,55]. Several studies outlined the advantages of using telehealth, which included increased access for patients and their families with regards to attendance at appointments [42,49,52,54] and decreased waiting lists [49]. Several authors suggested telemedicine was feasible given the circumstances of the pandemic, as it minimises disruptions to care and reduces patient risk of COVID-19 exposure [42,44,46,49,51,58], including avoiding visits to emergency departments [54] and saved time and costs from the hospital's perspective [37,61]. Moreover, from a patient's perspective, telehealth reduced travel time and expenses and increased convenience [45,54,55,58,61].
However, some patients preferred in-person visits and had no desire to continue telemedicine in the future, especially for staging results or treatment decisions [55,57]. Some studies highlight concerns about the accuracy and adequacy of virtual examinations (Canada [49] and Italy [60]) and their inconsistent use [31]. Others highlight that telehealth was not a substitute for treatment; for example, the use of telehealth did not mitigate the reductions in diagnosis and surgery (USA [65]). From the patients' perspective, concerns about access barriers were also discussed. These included technical difficulties with internet access [42,46,53,54,64], costs of technologies/hardware [63], and communication barriers [49]. Several studies reported that telemedicine was less feasible for older patients as they tended to encounter more difficulties with technology [31,42,[53][54][55]. Moreover, for specific activities such as genetic testing, requiring at-home sampling non-adherence was high [45]. Patient access barriers associated with telehealth were reported in developing economies such as network issues in India [64] and Brazil [46], and costs of technologies in Brazil [63]. Nevertheless, some institutions in developed countries also had access and adoption issues (USA, [65]) and concerns regarding the financial sustainability of providing telehealth (USA, [31]).
The review suggests some cancer patients and caregivers were very satisfied with telehealth and were comfortable using it as it offered them "support and connectedness" (India, [50], helped cope with worries [49], and reduced distress [53]. However, these favourable experiences were not universal and for some, the switch to telehealth was associated with higher levels of cancer worry and feelings of isolation (USA, [62]; Canada [49]). While some patients indicated a desire to continue with telehealth [37,55] and even expressed their willingness to pay for telehealth service in the future (India [50]), others indicated they were not inclined to continue using it. This was the case especially for staging results and treatment decisions [57], or it was only seen as a temporary measure until post-lockdown when the clinics reopened [35]. However, even those who were interested in continuing telehealth indicated a blend of telehealth and in-person visits is most desirable and suggested avoiding telehealth when providing results or prognoses [55]. As well as clinical appropriateness, adherence could become an issue for online course/programme delivery when COVID-19 restrictions are removed and people are no longer working from home [42]. To facilitate successful future virtual care, several factors should be considered. For example, appointments need to be scheduled in a pragmatic and logical way; with suitable detailed instructions, to manage expectations; with sufficient time for questions and with a cautious approach to self-care [49].

Discussion
This systematic review focused on the economic, social, health, and psychological implications of COVID-19 on cancer patients and the rapid expansion of telehealth services emerged as a key theme in response to the pandemic. Use of telehealth during the pandemic was particularly important for cancer patients and survivors who, due to their weakened immune system, were at greater risk of contracting infections and of developing more severe infections compared to the general population [3]. So, employing telehealth along with other public health guidelines and initiatives provided protection for this cohort. Despite the adoption of telehealth and other efforts, most healthcare systems paused essential inpatient and outpatient services during phase one of the pandemic. The result was missed or delayed cancer diagnosis and disrupted treatment leading to worsening health outcomes, quality of life, and in some cases mortality [29].
In the study, we briefly outlined the benefits and implications of telehealth with the purpose of mitigating the impact of the pandemic through reducing the risk of COVID-19 exposure for cancer patients and their families. The results showed that telehealth adoption seemed to "bolster" the delivery of healthcare services, providing a level of continuity of care during this highly uncertain time. However, it is evidenced that a "one size fits all" approach to telehealth is not appropriate to support the delivery of essential healthcare services for cancer patients. Albeit for its continued use, consideration of constraints is warranted to determine which patients and services may be successfully enabled by telehealth.
From an economic perspective, there were costs and benefits associated with the adoption of telehealth. Healthcare professionals' emergency response to maintaining a line of communication with cancer patients and their families meant pragmatic decisions were made to ensure some level of service was provided at a time when patient protection against COVID-19 infection was a priority. Telehealth emerged as one key valuable tool available to healthcare providers, in an extremely limited toolkit of possible responses to the pandemic. During the early phase of the pandemic, for some service providers, telehealth adoption consisted of using existing available technologies such as telephone consultations and video calls [38]. This was the case for approximately 61% of the studies presented here. For the remainder, there are costs associated with setup and maintenance of telehealth technology [53], including data protection. Following the early phase, strategic investments were made in hardware and software solutions to support the delivery of telehealth beyond the initial emergency response [66].
The cost of telehealth to national health systems, healthcare professionals, patients, and their families differs across jurisdictions, owing to variations in financial reimbursement models for health services. While some articles included in this review briefly consider cost in terms of reducing the cost of travel, access, and quality of care for cancer patients, future research could establish the time and cost savings for cancer patients accessing telehealth services. While studies indicated that patients were prepared to pay for telehealth services in the future [51], to ensure sustainability going forward, as telehealth shifts to becoming more embedded as part of routine services, appropriate reimbursement mechanisms will be necessary. This will require research to move beyond traditional approaches to support this emerging model of care delivery to answer questions such as: who will pay, where, and for what services? The latter could also consider potential savings arising from fewer appointment "no-show" incidents.
Patients' access to essential services via telehealth reduced the need for face-to-face interactions, when were stretched to capacity with COVID-19 patients or in anticipation of a surge of COVID-19 patients needing specialist care. The availability of telehealth services minimised the need for emergency admissions to acute services [65]. Reductions in non-attendance [42,49,52,54] also enabled the latter. Telehealth enabled the continuity of multidisciplinary decision-making for cancer patients with "virtual tumour boards" bringing together a range of medical disciplines for discussions on how to best care for a patient with cancer [33,35,56].
Telehealth provides beneficial spillovers for patients and their families. These include reduced travel time and efficiency gains with reduced waiting times from performing consultations from home with a loved one present. However, there are also costs and access barriers, including network issues and technology costs [46,63,64], which disproportionately impact vulnerable groups. The latter can include older adults [31,42,[53][54][55], those with poorer literacy skills, and those from lower economic backgrounds. Additionally, for those with cancers at sites which could impact cognition and other functions, for example, brain tumours, telehealth may not be as beneficial.
From a social perspective, while some cancer patients and their families extolled the benefits of telehealth, the pandemic exacerbated existing challenges around equitable digital access and utilisation of healthcare services. This "digital divide" has disproportionately affected vulnerable patient populations, for example older groups [53]. In addition, the attitude of staff, patients, and their families to the adoption and diffusion of telehealth technology differs, owing to several factors. Perceived skill gaps and lack of available hardware, software, internet access, and technical support can impact successful telehealth adoption. If telehealth is retained in the delivery of routine oncology services, understanding the adoption barriers and facilitators is necessary to ensure that the lessons learned are not left behind. Researchers, healthcare decision makers, and policy makers should explore new opportunities to tackle these challenges. One option is to assess the potential of telehealth hubs as an approach to centralising telehealth services, thus overcoming issues relating to access and support.
Finally, from a psychological perspective, the switch to telehealth for some was associated with higher levels of cancer worry and feelings of isolation [49,62], whereby the lack of in-person access created mental health strain for patients and survivors who were forced to solely rely on telehealth communication. For some patients, this outweighs the comfort and support benefits of being at home. While this review only captured the first wave of COVID-19, if oncology telehealth were to continue, efforts to minimise these adverse psychological impacts are warranted. A user-centred approach is necessary to design and develop telehealth that supports quality patient-healthcare professional communication and relationship development in a virtual environment. New opportunities to co-create telehealth services should be identified to ensure the design of usable and accessible services for cancer patients. This is particularly important when a patient is newly referred to a service. Additional research should explore clinical workflows and opportunities to incorporate telehealth to complement existing services, so patients experience the benefits that were accrued during COVID-19 and healthcare professionals are formally and explicitly allocated the time necessary to deliver quality personalised telehealth services. This research should include key efficiency and effectiveness indicators of cancer services.
New telehealth solutions should be designed to adapt to the changing needs and preferences of patients and their families. For example, appointments need to be scheduled appropriately and with sufficient time to allow for questions and consideration of information with appropriate health care practitioners and sufficient support information [49]. Likewise, patients' preferences for format matter must be considered as well, for example, telephone versus video calls. Moreover, the types of consultations for which telehealth is used need further exploration and consideration. For example, telehealth is suitable for some settings and services, such as counselling [42,47], replenishing medications, and for patients seeking information regarding their oncological treatments [51]. However, it is unsuitable for others, such as staging results and treatment decisions [55,57], which carry a significant psychological burden which could be exacerbated by telehealth. Emerging technologies such as artificial intelligence and machine learning techniques could be used to predict a patient's changing healthcare needs, incorporating factors such as their living arrangement and ability to communicate in a private space, their mental and spiritual wellbeing, etc.
A more intelligent blended approach to designing services that incorporate both telehealth and traditional face-to-face consultations may be needed to ensure quality of care and positive patient outcomes. These findings correspond with existing research assertions that telehealth is not a panacea. While telehealth is not a universal solution to delivering cancer services during a pandemic or beyond, it facilitated continuity of care during a highly uncertain time for some.

Conclusions
This paper provides a systematic literature review to identify the economic, social, health, and psychological implications of COVID-19 on cancer patients during wave one, with the availability of telehealth services for cancer patients emerging as a key theme. This review is not without limitations. Most of the studies included in the review are single institutional studies, where telehealth was employed for a variety of reasons in various settings, with small sample sizes, so wide-scale adoption and satisfaction of telehealth cannot be determined. Furthermore, the methodologies employed yield potential biases. These include selection biases arising from convenience sampling [44] and observation bias owing to data collection methods [52]. However, some studies lacked outcome data [15], where collected self-reported data were relied upon [44] and validated instruments were lacking [43].
The time and scope of this review means only the first wave of the pandemic was assessed. While some initiatives have persisted and, in many cases, helped to mitigate the impact of the pandemic on adult cancer patients, it is likely other temporary measures have waned. This study reveals that there have been telehealth successes and failures; the lessons learned present a significant opportunity to reimagine the delivery of healthcare, leveraging telehealth as a complement rather than a substitute. This approach will enable healthcare systems globally to future-proof their operations by better preparing for unique unexpected disruptive events such as pandemics and natural disasters.

Data Availability Statement:
The data presented in this study are available in Table 2 and [29].

Conflicts of Interest:
The authors declare no conflict of interest.

Appendix A Quality Review I PREVALENCE STUDIES [27]
1.
Was the sample frame appropriate to address the target population? 2.
Were study participants sampled in an appropriate way? 3.
Was the sample size adequate? 4.
Were the study subjects and the setting described in detail? 5.
Was the data analysis conducted with sufficient coverage of the identified sample? 6.
Were valid methods used for the identification of the condition? 7.
Was the condition measured in a standard, reliable way for all participants? 8.
Was there appropriate statistical analysis? 9.
Was the response rate adequate, and if not, was the low response rate managed appropriately?
Were the criteria for inclusion in the sample clearly defined? 2.
Were the study subjects and the setting described in detail? 3.
Was the exposure measured in a valid and reliable way? 4.
Were objective, standard criteria used for measurement of the condition? 5.
Were strategies to deal with confounding factors stated? 7.
Were the outcomes measured in a valid and reliable way? 8.
Was appropriate statistical analysis used?

III QUALITATIVE STUDIES [27]
1. Is there congruity between the stated philosophical perspective and the research methodology? 2.
Is there congruity between the research methodology and the research question or objectives? 3.
Is there congruity between the research methodology and the methods used to collect data? 4.
Is there congruity between the research methodology and the representation and analysis of data? 5.
Is there congruity between the research methodology and the interpretation of results? 6.
Is there a statement locating the researcher culturally or theoretically? 7.
Is the influence of the researcher on the research, and vice-versa, addressed? 8.
Are participants, and their voices, adequately represented? 9.
Is the research ethical according to current criteria or, for recent studies, is there evidence of ethical approval by an appropriate body? 10.
Do the conclusions drawn in the research report flow from the analysis, or interpretation, of the data?
Were the two groups similar and recruited from the same population? 2.
Were the exposures measured similarly to assign people to both exposed and unexposed groups? 3.
Was the exposure measured in a valid and reliable way? 4.
Were strategies to deal with confounding factors stated? 6.
Were the groups/participants free of the outcome at the start of the study (or at the moment of exposure)? 7.
Were the outcomes measured in a valid and reliable way? 8.
Was the follow-up time reported and sufficient to be long enough for outcomes to occur? 9.
Was follow-up complete, and if not, were the reasons for loss of follow-up described and explored? 10.
Were strategies to address incomplete follow-up utilised? 11.
Was appropriate statistical analysis used? • 90% of follow-up consultations and 40% of specialist visits were conducted by telephone service • Acceptance of phone-based follow-ups and restaging visits perceived as "not very adequate" (17%) or "not adequate at all" (18%).