key: cord-1051563-953cf1yj authors: Edge, Rhiannon; Meyers, Josh; Tiernan, Gabriella; Li, Zhicheng; Schiavuzzi, Alexandra; Chan, Priscilla; Vassallo, Amy; Morrow, April; Mazariego, Carolyn; Wakefield, Claire E.; Canfell, Karen; Taylor, Natalie title: Cancer care disruption and reorganisation during the COVID-19 pandemic in Australia: A patient, carer and healthcare worker perspective date: 2021-09-17 journal: PLoS One DOI: 10.1371/journal.pone.0257420 sha: 80f304e37f44723443338a566da188d13af6bbad doc_id: 1051563 cord_uid: 953cf1yj The COVID-19 pandemic has dramatically impacted cancer care worldwide. Disruptions have been seen across all facets of care. While the long-term impact of COVID-19 remains unclear, the immediate impacts on patients, their carers and the healthcare workforce are increasingly evident. This study describes disruptions and reorganisation of cancer services in Australia since the onset of COVID-19, from the perspectives of people affected by cancer and healthcare workers. Two separate online cross-sectional surveys were completed by: a) cancer patients, survivors, carers, family members or friends (n = 852) and b) healthcare workers (n = 150). Descriptive analyses of quantitative survey data were conducted, followed by inductive thematic content analyses of qualitative survey responses relating to cancer care disruption and perceptions of telehealth. Overall, 42% of cancer patients and survivors reported experiencing some level of care disruption. A further 43% of healthcare workers reported atypical delays in delivering cancer care, and 50% agreed that patient access to research and clinical trials had been reduced. Almost three quarters (73%) of patients and carers reported using telehealth following the onset of COVID-19, with high overall satisfaction. However, gaps were identified in provision of psychological support and 20% of participants reported that they were unlikely to use telehealth again. The reorganisation of cancer care increased the psychological and practical burden on carers, with hospital visitation restrictions and appointment changes reducing their ability to provide essential support. COVID-19 has exacerbated a stressful and uncertain time for people affected by cancer and healthcare workers. Service reconfiguration and the adoption of telehealth have been essential adaptations for the pandemic response, offering long-term value. However, our findings highlight the need to better integrate psychosocial support and the important role of carers into evolving pandemic response measures. Learnings from this study could inform service improvements that would benefit patients and carers longer-term. The COVID-19 pandemic has dramatically impacted cancer care worldwide. Disruptions have been seen across all facets of care. While the long-term impact of COVID-19 remains unclear, the immediate impacts on patients, their carers and the healthcare workforce are increasingly evident. This study describes disruptions and reorganisation of cancer services in Australia since the onset of COVID-19, from the perspectives of people affected by cancer and healthcare workers. Two separate online cross-sectional surveys were completed by: a) cancer patients, survivors, carers, family members or friends (n = 852) and b) healthcare workers (n = 150). Descriptive analyses of quantitative survey data were conducted, followed by inductive thematic content analyses of qualitative survey responses relating to cancer care disruption and perceptions of telehealth. Overall, 42% of cancer patients and survivors reported experiencing some level of care disruption. A further 43% of healthcare workers reported atypical delays in delivering cancer care, and 50% agreed that patient access to research and clinical trials had been reduced. Almost three quarters (73%) of patients and carers reported using telehealth following the onset of COVID-19, with high overall satisfaction. However, gaps were identified in provision of psychological support and 20% of participants reported that they were unlikely to use telehealth again. The reorganisation of cancer care increased the psychological and practical burden on carers, with hospital visitation restrictions and appointment changes reducing their ability to provide essential support. COVID-19 has exacerbated a stressful and uncertain time for people affected by cancer and healthcare workers. Service reconfiguration and the adoption of telehealth have been essential adaptations for the pandemic response, offering long-term value. However, our findings highlight the need to better integrate psychosocial support and the important The aims of this study are to describe the ways in which cancer care in Australia has been disrupted and reorganised during the COVID-19 pandemic, and to understand the impact this has had from the perspectives of both people affected by cancer and healthcare workers. Two concurrent cross-sectional surveys were conducted online to assess the impact of COVID-19 on cancer care delivery in Australia with: a) people affected by cancer, including cancer patients, cancer survivors, carers, family members or friends and b) healthcare workers. People affected by cancer were eligible to participate if they resided in Australia, were aged 18 or above, and had a current or previous diagnosis of cancer, or were a caregiver, family member or friend of someone diagnosed with cancer. Respondents were asked tailored survey questions depending on their relationship with the person affected by cancer (e.g., caregiving frequency, attendance at appointments). Healthcare workers were eligible to participate if they were employed or involved in the delivery of cancer services in Australia. The surveys were advertised on the Cancer Council NSW and Cancer Council Australia websites and were promoted via social media (Facebook and Twitter). Invitations were also distributed through existing cancer community and healthcare professional networks across Australia (e.g., Cancer Voices and Clinical Oncology Society of Australia). All survey responses were collected between 22 June and 30 September 2020. During this time, Australia was under nation-wide COVID-19 restrictions and both international and inter-state travel bans were in place. The study period also corresponded with the COVID-19 cluster which emerged in Melbourne, Victoria in late June 2020, resulting in more than 110 days of lockdown restrictions. Under these restrictions, Melbournians and other Victorian residents were ordered to stay at home unless they needed to leave for medical reasons, essential shopping, essential work, or outdoor exercise (within geographical limits). Upon closure of the survey on 30 September 2020, Australia had recorded 27,000 COVID-19 infections and 886 deaths [18] . Ethical approval was granted for this research by Cancer Council NSW's Human Research and Ethics Committee (HREC) (Ref: #322). For both the surveys, participants were directed to an online version of the Participant Information Statement and specifically asked for their consent before beginning the survey. Demographic data and other descriptive information were collected for all participants. For those affected by cancer, data were collected on year of diagnosis, cancer stage, cancer type and current treatment. For healthcare workers, data were collected on the type of profession, length in role, primary work setting, and whether their role involved direct clinical interactions with patients. Both surveys comprised of sections regarding changes to cancer care delivery and experiences of telehealth. The measures used in the surveys were based on available pre-existing evidence around the impact of COVID-19, adapted versions of relevant validated tools, and stakeholder (i.e., clinician, consumer) consultation. For the measures used in the survey for those affected by cancer, questions were informed by an in-depth qualitative analysis of a National Cancer Information and Support Line and Online Cancer Community Forum in Australia (https://www.cancer.org.au/online-resources/cancer-council-online-community) [19] . Additionally, some measures regarding cancer care quality and telehealth described in this paper were adapted from The Cancer Care Coordination Questionnaire for Patients [20] and The Telehealth Satisfaction Scale [21] . The healthcare worker survey included a specific section focused on cancer care delivery and reorganisation which is the focus of this analysis. The development of measures in this section of the survey were informed by emerging evidence regarding the impact of COVID-19, the literature on previous crisis events (e.g., the Severe Acute Respiratory Syndrome (SARS) epidemic), and healthcare performance. Four key categories focussed on exploring quality of care [22] , organisational support [e.g., 23], resources [24] , time and priorities [25] , in consideration of the crisis. In both surveys, our definition of telehealth included both telephone and online consults. The study surveys were tested by our consumer representative and by reviewers experienced in cancer care to assure quality while piloting was not done due to the time critical nature of the survey. Data quality was checked at regular intervals post survey release. Demographic data and quantitative survey responses were examined using frequency and percentages for categorical variables, and mean and standard deviation for continuous variables. Qualitative survey responses were imported into NVivo 12 Plus software (QSR International Pty Ltd 2018) to separately undergo an inductive thematic qualitative content analysis. Using this approach, a preliminary review of the content was performed by GT to develop the initial coding structure which was then shared with the research team (RE, JM and NT) for secondary review and comment. This informed the refinement of the coding framework which was then applied to the complete dataset. Similar codes were grouped together into higher order categories and subthemes, identified by salience and frequency [26] . In the results, alignments between quantitative survey findings and the emergent themes from the qualitative analysis were identified and reported. A total of 852 people affected by cancer (683 cancer patients and survivors; and 169 carers, family members and/or friends) and 150 healthcare workers participated in the two surveys. Participants' demographics are shown in Table 1 . In both surveys, more than 50% of the sample provided at least one response to an open-ended question relating to cancer care disruption and telehealth. Results focus on four common areas surveyed with healthcare workers and those affected by cancer to understand the impact of cancer service disruption and reorganisation from different perspectives: 1) experiences of cancer service and care disruption, 2) the perceived quality of clinical care during the pandemic, 3) experiences of telehealth, and 4) the impacts of COVID-19 on the supporting role of carers and family members in cancer care. Descriptive quantitative data from the survey is accompanied by qualitative findings and representative quotes to illustrate key themes. During the pandemic, a range of disruptions to routine cancer care services were reported by both those affected by cancer and healthcare workers. Overall, 42% of cancer patients and survivors reported experiencing some level of disruption to their cancer care or treatment. Of this cohort, 44% (n = 118) were receiving active treatment (including chemotherapy, radiation therapy, immunotherapy or surgery). 49% of carers suggested there had been care disruptions for the person whom they cared for. More specifically, almost a third of cancer patients and survivors (28%) indicated that their medical appointments had needed to be rescheduled, 10% reported that their cancer treatment had been postponed, 7% reported elective surgeries had been delayed, and 12% suggested their planned cancer screening tests had been rescheduled (Fig 1) . Cancer patients and survivors described feelings of stress and anxiety associated with these rapidly unfolding changes, and highlighted communication issues with their healthcare provider in some instances: Although reported cancellations were relatively low (suggested by 10% of respondents overall), there were still instances where appointments, surgeries, clinical trials and hospital "Cancellation of all support groups face to face. Cancellation of hospital wellness programs." Patients and carers also articulated frustrations about the perceived prioritisation of COVID-19 over their cancer-related symptoms and reported that this caused distress. Some patients also described their hesitancy to attend future appointments at healthcare centres due to their fears of potential COVID-19 exposure. Disruptions to cancer services were also reported by healthcare workers, with 43% agreeing that there had been atypical delays in delivering cancer care, and half (50%) agreeing that patient access to research and clinical trials had been reduced since the onset of the pandemic. In associated comments, they provided details about delays to essential cancer diagnostic procedures and treatments: "Non-essential surgery was cancelled/delayed. I did not directly deal with the consequences of that with most patients but nursing and psychology staff did." (Healthcare worker) "Transplants were made more difficult due to trouble precuring donors and getting cells, more organisation time, more delays and sometimes no available donor." (Healthcare worker) Further, consistent with the hesitancy reported by some cancer patients and survivors in attending healthcare centres, 45% of healthcare workers agreed that the number of consultations cancelled by patients had increased from prior to the pandemic. They expressed concern about the potential long-term impacts of reduced appointment attendance and delays to treatment and diagnostics on long-term cancer prognosis: "Very concerned about the reduction in diagnosed cases and what that will do to our patients and us over the next 5 years." (Healthcare worker) "[It is] concerning for staff that cancer referrals are well down on usual and so we worry about more advanced presentations and our workload over next few months." (Healthcare worker) Despite the disruptions observed across cancer services during the study period, 61% of cancer patients, survivors and carers agreed that they felt fully informed about changes to cancer treatment plans. Further, the majority reported that they did not encounter difficulties obtaining appointments with their regular healthcare provider, nor experience longer wait times for appointments (Fig 2) . This sentiment was also echoed in some of the comments they provided in the survey: However, whilst the majority responded positively, there were also some concerns flagged by patients and carers about care quality. In some instances, they described a lack of information provided by the health system about service disruptions, particularly in the earlier weeks of the pandemic. Further, some explained how their cancer treatment plans had essentially "disappeared" and that they were experiencing challenges in accessing usual care. "The hospital just carried on as if nothing had changed for the first 6 weeks of the pandemic. There was no additional information given." (Carer) "Would like some information about the resumption of non-emergency surgery." (Patient) For healthcare workers, similar ambiguities to patients and carers were identified in their perceptions of care quality during COVID-19. As demonstrated in Fig 3, 72% reported being happy with the quality of care they had been able to provide to cancer patients during this crisis, however, almost a third (31%) suggested that changes to cancer diagnostic procedures and/ or pathways had made them suboptimal. Healthcare workers highlighted the additional challenges of maintaining quality of care and meeting patients' needs during the pandemic, with 73% agreeing that the complexity of care had increased and 85% agreeing (50% strongly agreeing) that COVID-19 had increased pressure on their patients' mental health and wellbeing. "Definitely noticed patients undergoing cancer treatment feel vulnerable to severe COVID infection and are more likely to go to extreme measures to isolate with subsequent increase in anxiety/depression/loneliness/job loss/financial and relationship strain." (Healthcare worker) "COVID-19, and the associated impact of this has been an overlay that has affected every aspect of work-more complex patient interactions, more complex workplace interactions (and my own personal capacity to deal with challenges has been reduced)." (Healthcare worker) Cancer patients and survivors indicated that most of these telehealth consults during the pandemic had been with their GP (65%) or a specialist consultant (64%) (e.g., medical oncologist). A smaller proportion had received psychological support or had an appointment with an allied health professional over telehealth. For healthcare workers, 60% reported that more than half of their regular appointments had been moved to telehealth consultations since the onset of the pandemic, with the majority (68%) agreeing they had received adequate support to adopt these alternative modes of service delivery. Overall, general patient satisfaction with telehealth consults for their cancer care was high, with 80% rating the accessibility and convenience of the appointment and quality of care they received as either 'good' or 'excellent'. Respect of privacy and the process of logging/dialling into the appointment were also highly rated. However, when asked about the psychological and emotional support they had received over telehealth, 18% reported their experience had been 'poor' or 'fair' (Fig 4) . The main perceived benefits of telehealth for cancer patients and survivors included the reduced exposure risk to COVID-19, reduced costs of attending treatment (i.e., travel, parking, childcare) and more timely access to services. In contrast, the most frequently cited difficulties were concerns about whether telehealth would deliver the same quality of care as a physical examination, with 18% of respondents suggesting this was of concern for them. Cancer patients, survivors and carers described a lack of personalised care (e.g., reduced rapport and interpersonal connection) and difficulties interpreting information they had been provided through online or telephone consults. They also highlighted how telehealth was not always optimal for certain types of appointments, particularly when physical examinations were required, or psychological support was being delivered. When cancer patients and survivors were asked about their likelihood of using telehealth services in future, more than half (55%) indicated that they would use this again, however, 1 in 5 (20%) answered that they were unlikely to. Healthcare workers also articulated benefits of telehealth such as decreased wait times, streamlined processes and increased privacy. However, they too raised concerns about the appropriateness of telehealth consultations where physical assessments were required, or interpersonal connection was important for the delivery of optimal care. Healthcare workers also described the challenges they had experienced with making accurate diagnoses over telehealth and highlighted how non-verbal communication and body language cues that may signify psychological distress were easier to miss. The positive and negative perceptions of both healthcare workers and patients or carers in relation to telehealth are shown in Table 2 . Over three quarters (79%) of healthcare workers reported that involving carers in consults had become more challenging since the onset of the COVID-19 pandemic. They explained how the restrictions on hospital visitation had been difficult to communicate to patients and their families, and that the reduction in essential support was likely having a negative impact on their mental health and wellbeing. "Families do find it challenging, understandably, due to restrictions on how many people can visit. . ." (Healthcare worker) Patients and their carers similarly described the challenges they faced attending in-person consults together as a result of restricted hospital visitation and social distancing measures. Further, almost half (48%) of carers reported that they had been unable to attend telehealth consults with the person diagnosed by cancer. They described how not being able to attend appointmentswhether in-person or via telehealth-had placed an additional burden on them to provide the same levels of practical and emotional support as before the pandemic. Some carers suggested that they were no longer able to listen to and clarify important information for their loved ones, nor understand how they were best able to provide support during intensive treatments. Patients also highlighted the lonely experience of attending appointments with a reduced social support network. They felt overwhelmed attending cancer treatments alone, and described challenges with digesting and interpreting health information from clinicians without this additional support. "It was also lonely attending appointments alone and not being able to take a support person to radiotherapy on occasions." (Patient) Although Australia's response to the pandemic has largely been effective in terms of limiting case numbers and fatality rate [7] , disruptions to cancer services, as outlined in this research and elsewhere [2, 6, 11, 12] , demonstrate an immediate psychosocial impact on people affected by cancer and may have longer term implications. Our findings highlight that patients, survivors, carers, and healthcare workers have adapted relatively well to unprecedented overhauls in standard protocols and offer important insights for future policy and practice in relation to crisis preparedness, as well as ongoing cancer care. During our study period, disruptions were observed across a wide range of cancer services, including screening, diagnostics and treatments, and consultation formats, aligning with other recent research [11, 12] . Whilst the true cost of these disruptions will take time to understand, there are concerns that such rapid health service reconfiguration will result in delayed diagnosis and poorer prognosis [10, 27] . Using breast cancer as an example, modelling commissioned by the Australian Government suggests temporary pauses to BreastScreen services could adversely impact clinical outcomes including time to diagnosis and survival (a potential reduction in population-level survival rates of up to 1.9% by end 2023) [28] . Additionally, modelling of the 6.5-month period of COVID-19-related restrictions in Victoria-Australia's most affected state-found a 10% reduction in cancer pathology notifications and an estimated 2,530 missed or delayed cancer diagnoses [27] . Furthermore, international evidence suggests that for many cancers, even modest delays to treatment can result in a substantial proportion of patients with early-stage cancers progressing from having curable to incurable disease [29] . Ongoing work by the COVID-19 and Cancer Global Modelling Consortium (CCGMC) is quantifying the impact of delays on outcomes, in addition to disruptions to treatment of cancer [30] . Post-pandemic service planning must consider these concerns to minimise the unintended consequences of the COVID-19 response. Given the key role of primary care in cancer screening and diagnosis, strategies to address potential diagnostic and treatment queues will require collaboration across all sectors of the health system. Considering the immediate and widespread disruptions experienced by people with cancer, it is a positive reflection on the Australian pandemic response effort that patients and carers perceived changes to their cancer treatment plans were communicated effectively and wait times were not adversely affected for the majority. Indeed, only a small proportion of healthcare workers perceived changes to cancer care to be sub-optimal. However, the psychological impact of COVID-19 should not be underestimated. Given the high levels of uncertainty about future restrictions, the increasing clinical complexity of caring for people affected by cancer, and reduced social support networks, it is not surprising that healthcare workers in this study were concerned about the mental health burden of COVID-19. Recently developed guidelines highlight practical strategies for clinicians to employ with patients, caregivers, and family to address the uncertainty associated with their care and the adoption of these should be strongly encouraged [5, 10, 31] . Moreover, at a time when demand for supportive care services has surged, many community support organisations that play an important role in addressing the unmet supportive care needs of people affected by cancer have been forced to reduce their program and service offerings due to funding deficits [32] . This "perfect storm" may compound the adverse psychological outcomes of the pandemic for this vulnerable group and warrants further attention. Not all indirect consequences of the pandemic have been undesirable. The rapid implementation of telehealth within cancer services-the adoption of which has previously been slow and fragmented across jurisdictions-has largely been successful and may offer permanent value in enhancing cancer care quality and access, as well as provide innovative and highly acceptable solutions to crisis preparedness and response strategies [33] . Telehealth has enabled healthcare workers to work remotely while patients and carers can remain at home, thereby minimising risk of virus transmission. It is important to note that despite the shift to telehealth being met with high overall levels of satisfaction among these participants, important gaps remain, particularly in relation to perceptions of care quality, personalised care, the role of carers and the delivery of psychosocial support-echoing themes previously identified in existing telehealth literature [33, 34] . Furthermore, MBS analysis reveals that most consultations are being done by telephone rather than video telehealth [11] -despite Department of Health recommendations that videoconference services are the preferred substitute for face-to-face consultations [35] . Encouragingly, steps have already been taken to prompt proactive discussion and action on issues of trust, isolation and disconnectedness between clinicians and consumers using telehealth [5, 10] . Our findings also highlight that greater attempts to consider carers in virtual models of care should be made. Clear governance, policies and procedures to guide safety and quality in cancer telehealth consultations are clearly needed. Considering the potential value of telehealth, further research and investment from State and Federal governments is needed to address the concerns of cancer patients and carers-up to 20% of whom in our study report they are unlikely to use again-to ensure the continued viability of telehealth to augment faceto-face care. Finally, whilst our study highlights the rapid reconfiguration of cancer care in Australia during COVID-19, further research is required to understand the extent to which such changes are clinically appropriate, offer high-value care for patients, survivors and their carers, and impact cancer outcomes. Consideration of shared decision making and patient-centred care, and evaluation of the risks and benefits of clinical decision-making-particularly as COVID-19 vaccines are rolled out for cancer patients [36] -should underpin cancer care policy and practice [5, 10, 31] , both during the pandemic and beyond. We acknowledge that our study has limitations. Our sample of participants recruited using national websites, existing cancer community networks and social media channels may have resulted in a convenience sample that was not representative of the wider population of those affected by cancer. We also acknowledge that certain demographic groups were overrepresented in our sample (e.g., NSW respondents, women, and people with early stage and localized cancers, and in recovery and remission). Additionally, given that only a small proportion of respondents affected by cancer were from Victoria (<10%), the state most affected by COVID-19 restrictions during the study period, our findings may underrepresent the true impacts of the pandemic on cancer care nationally. Our study found reports of notable disruptions to cancer care, yet we could not determine the clinical appropriateness of such changes, nor the extent to which these reports corroborate objectively measured service disruption, or whether these were likely to affect morbidity and mortality. Despite these limitations, we believe that this research provides a timely and valuable contribution to the emerging evidence of the impact of COVID-19 pandemic on cancer care, with a unique approach of exploring the experiences and perceptions of both the care recipients and care providers concurrently. The relevant timing of our two surveys and the large sample size of people affected by cancer also increases the relevance and applicability of our study. As the pandemic evolves over time, further research is required to understand the changing experiences of people affected by cancer and healthcare workers in response to the pandemic-related policy and practice changes and as COVID-19 vaccine uptake increases. The exceptional circumstances of the COVID-19 pandemic have altered cancer care. Although Australia has been largely successful in curbing the spread of the virus to date, the pandemic has exacerbated what is already an immensely stressful and uncertain time for people affected by cancer. The long-term effects remain to be seen [6] . The reorganisation of cancer care and the adoption of telehealth has been essential, and the value of these adaptations for the pandemic response, preparedness, and beyond, is clear. However, our findings highlight the need for efforts to better integrate psychosocial support and the important role of carers into evolving pandemic response measures to guide health systems towards an equitable and personcentred digital future. Although the COVID-19 response is ongoing and contexts are constantly evolving, how we respond is ultimately dependent on how well we efficiently translate lessons learned into effective policy and practice. How has COVID-19 impacted cancer screening? 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Current treatment options in oncology Organisations for patients with cancer feel the brunt of COVID-19 pandemic Cancer Survivors' Experience With Telehealth: A Systematic Review and Thematic Synthesis Grappling with the "human" problem hiding behind the technology: Telehealth during and beyond COVID-19 COVID-19 Telehealth Items Guide Canberra2020 COVID-19 vaccines and cancer: Australian Government The research team would like to thank our research consumer, Kathryn Leaney, and staff at Cancer Council NSW for their contributions to the survey question development, support with participant recruitment, and for the in-kind dedication of their time and resource to assist the research team with this project. They would also like to thank the many people affected by cancer and healthcare workers who participated in this study to provide timely insights about cancer care during the COVID-19 pandemic.