Counting the social, psychological, and economic costs of COVID-19 for cancer patients

Purpose Cancer patients were particularly vulnerable to the adverse impacts of the COVID-19 pandemic given their reliance on the healthcare system, and their weakened immune systems. This systematic review examines the social, psychological, and economic impacts of COVID-19 on cancer patients. Methods The systematic search, conducted in March 2021, captures the experience of COVID-19 Wave I, when the most severe restrictions were in place globally, from a patient perspective. Results The search yielded 56 studies reporting on the economic, social, and psychological impacts of COVID-19. The economic burden associated with cancer for patients during the pandemic included direct and indirect costs with both objective (i.e. financial burden) and subjective elements (financial distress). The pandemic exasperated existing psychological strain and associated adverse outcomes including worry and fear (of COVID-19 and cancer prognosis); distress, anxiety, and depression; social isolation and loneliness. National and institutional public health guidelines to reduce COVID-19 transmission resulted in suspended cancer screening programmes, delayed diagnoses, postponed or deferred treatments, and altered treatment. These altered patients’ decision making and health-seeking behaviours. Conclusion COVID-19 compounded the economic, social, and psychological impacts of cancer on patients owing to health system adjustments and reduction in economic activity. Identification of the impact of COVID-19 on cancer patients from a psychological, social, and economic perspective following the pandemic can inform the design of timely and appropriate interventions and supports, to deal with the backlog in cancer care and enhance recovery. Supplementary Information The online version contains supplementary material available at 10.1007/s00520-022-07178-0.


Introduction
Cancer is a leading cause of death globally, with almost 10 million deaths and 19.3 million incidences worldwide in 2020 [1]. This has a significant economic burden globally, estimated at $1.16 trillion in 2010 [2]. Such cost estimates capture expenditure on several types of cancer care, depending on prevalence, treatment patterns, and pharmaceutical spend. However, the economic burden of cancer extends beyond the costs of healthcare delivery. Patients and survivors also face objective costs (i.e. financial burden), arising from out-of-pocket payments. These vary depending on the public healthcare system in which they are treated, and insurance coverage. Additionally, there are subjective costs (financial distress) [3], which incorporates the psychological consequences and coping behaviours associated with the financial burden of cancer. Financial distress has adverse effects on health outcomes, collectively affecting quality of life (QoL) and well-being [3]. Recently, the COVID-19 pandemic disrupted health services globally. Cancer patients were particularly vulnerable to its adverse impacts given their reliance on the healthcare system, and their weakened immune systems.
Here, we investigate the social, psychological, and economic costs of the pandemic on cancer patients. National and institutional public health guidelines issued to protect against COVID-19 both influenced cancer care. Stay-athome orders, social distancing, reconfigured healthcare delivery, reduced healthcare capacity, and re-distributed resources were needed to meet the demands of COVID-19. This in turn negatively impacted cancer care.
This systematic review examines the social, psychological, and economic impacts of COVID-19 on cancer patients. The systematic search, conducted in March 2021, captures the experience of COVID-19 Wave I, when the most severe restrictions were in place globally. Taking a patient perspective, the findings provide reflections on how cancer care for patients undergoing treatment was affected by the pandemic. Consideration is given to innovations arising during the pandemic and lessons learned for designing future developments and supports, which are to mitigate the social, psychological, and economic impacts associated with cancer.

Study selection criteria
This systematic review was conducted in accordance with the principles of conducting systematic reviews [4]. The PICOCS framework (i.e. population, intervention, comparators, outcomes, context, studies) was used to support inclusion criteria [5] (see Table 1). (There was a minor adaptation including "context" and excluding "comparator" as it was not applicable.) Studies published between January 2020 and March 2021 examining the impact of the COVID-19 pandemic on adult cancer patients undergoing treatment and survivors (2 years post-diagnosis) were examined. Inclusion and exclusion criteria are outlined in Table 1. Studies included were limited to those written in English and focused on the economic, social, and psychological implications of COVID-19 on cancer patients/ survivors. Table 2 Literature search strategy A comprehensive search strategy was employed using a combination of free-text words and subject headings relevant to CINAHL, MEDLINE, PsycINFO, PsycArticles, and EMBASE databases and refined using Boolean operators. Searches were performed on the 31st of March 2021. Full search terms and combinations are provided in Appendices 1 and 2. The search protocol was registered (CRD42021246651).

Data extraction and quality assessment
Data extraction is presented in tabular format to assist reporting uniformity, reproducibility, and minimising bias (provided on Table 3). The evidence was combined and summarised using a narrative synthesis. Methodological quality of studies was evaluated using the Joanna Briggs Institute critical appraisal tools (for cross-sectional, prevalence, cohort, and qualitative studies) and the Consensus on Health Economic Criteria (CHEC) list for cost analyses. Two authors performed quality assessment independently (AL and AK). If there was conflict or uncertainty, a third author 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 3.

Worry and fear
The most common mental health domain(s) identified were worry and/or fear around their cancer and getting COVID-19. Firstly, there was a heightened sense of fear of cancer recurrence or disease progression due to COVID-19-related disruptions or delays in cancer care [7][8][9][10][11][12][13][14]. Instruments used to measure fear and the level of fear experienced varied. For example, in a survey of 16 European countries, 71% of patients were concerned about cancer progression if their treatment/follow-up was cancelled/postponed [8]. In contrast, a survey in India reported fear of treatment delays and cancer progression as mostly moderate or minimal [10].
Secondly, there was fear and worry around getting COVID-19 amongst cancer patients [7-9, 11-13, 15-35]. A Singaporean study reported that 66% of patients had an elevated level fear of COVID-19 [36]. Gheorghe et al. [37] found that 68.5% of Romanian cancer patients were "very" or "somewhat worried" about COVID-19 compared to the influenza virus. Biagioli et al. [38] found that 37.3% of Italian cancer patients were "very or extremely" afraid of going to hospital because of an increased risk of contracting COVID-19 there, and 24.5% were "very or completely" afraid that their cancer care would become less important than being protected against COVID-19 infection, which would then have a negative impact on their prognosis. They also found that 53.8% believed they were at a higher risk of COVID-19 infection than the general population. Similarly, Erdem and Karaman [39] report that one-third of Turkish cancer patients were afraid to leave their house. These were more likely to be > 65 years, female, with stage 1 cancer, and with low education attainment. Those that did attend hospital appointments (~ 33%) were more likely to have stage 4 cancer; wore a mask (67%); and preferred not to use public transport owing to COVID-19 risk (95%). The majority (97%) did not accept visitors to their houses and washed their hands more often than usual (97.3%). Those finished treatment (radiotherapy or surgery) with co-morbidities (40%) were also afraid of COVID-19, in particular, females [7]. Higher levels of worry were found among females and older patients in Italy [16,30], patients with comorbidities, Health impact "cancer" OR "oncology" OR "malignant" OR "tumour" OR "metastasis" OR "neoplasm" "covid-19" OR "coronavirus" OR "2019-ncov" OR "sars-cov-2" OR "cov-19" OR "severe acute respiratory syndrome coronavirus-2" OR "pandemic" "financial toxicity" OR "outof-pocket" OR "productiv-    • Females had a significantly higher score for "Total concerns" category (p-0.004) and anxiety levels (p < 0.001) • Age and travel for treatment were concerns for COVID-19 risk       • The greatest concern of patients was the wide community spread of COVID-19 • 19.1% of patients had anxiety (score ≥ 10) • Fear was the most common emotion, followed by anxiety • Anxiety was significantly higher in patients married, education lower than tertiary level • Patients that were non-Chinese and married had a higher level of COVID-19 fears      • Jan-March 2020: reduced by 8% • Average weekly admissions showed a 40% reduction in March 2020 Chemotherapy admissions: • Jan-March 2020: reduced by 6% • 14% reduction in daily average Specialist visits: • Jan-March 2020: reduced by 3%. 35% reduction daily average visits, 7 patients were COVID positive • Almost all patients felt that the organisational measures adopted to minimise the risk of SARS-CoV-2 infection were clearly expressed (98%, 95%) • Acceptance of phone-based follow-ups and restaging visits, which were perceived as "not very adequate" (17%) or "not adequate at all" (18%) • Fear of accessing hospital facilities 34% • Fear that chemotherapy treatment could increase the risk of contracting SARS-CoV-2 infection 27% immunocompromised and on active treatment in Denmark, the USA, and China [24,28,33], and amongst those with higher stress levels in Iran [40].
Patients tended to prioritise their cancer care over fear of contracting COVID-19, suggesting they were more afraid of delayed treatment and cancer progression than COVID-19 [10]. However, some sub-groups were willing to postpone/ delay appointments and treatments [16,21,32].
Worryingly, as much as 61.8% were found to fear both COVID-19 infection and cancer progression equally [37]. In practice, the two fears/worries are intertwined, with patients reporting fear of getting COVID-19 infection when in hospital for treatment [11] and fearing that chemotherapy treatment could increase risk of COVID-19 infection (27% of Italian cancer patients sampled [41]). Disparity also existed amongst those who worried more about COVID-19 infection than their cancer, low socioeconomic groups [37], those undergoing palliative care [42], older [8,16], frailer patients with co-morbidities [16], or those with a good understanding of immunosuppression [10].

Distress, anxiety, and depression
Košir et al. [9] conducted an international survey and found those currently or undergoing treatment within the last 6 months reporting higher levels of psychological distress on average; the most common concern being contracting COVID-19. Some American cancer patients found attending in-person appointments or treatment alone, and the cancellation or movement to virtual social support groups was emotionally challenging and distressing [26]. In France, being unemployed aggravated psychological distress further [43].
Several studies reported anxiety amongst samples of all cancer patients during the pandemic [29,36,42,44]. Additionally, higher levels of anxiety were found amongst female patients in the UK, USA, Poland, and China [19,26,33,35,43,45]; patients from lower income households [11]; older and more vulnerable patients in the Netherlands and Northern Italy [18,30]; married patients in Singapore [36]; and patients with lower educational attainment in Italy, Singapore, and China [35,36,46]. In contrast, younger Chinese cancer patients demonstrated elevated levels of anxiety, suicide ideation, and low sleep quality, during the pandemic [47]. While in China, Wang et al. [33] found those employed had a lower risk of anxiety and depression.
Higher levels of depression were reported amongst female patients in China [43], older patients in Turkey [14], those from lower income households in South Korea and India [11,44], patients who were unemployed in China [43], and unmarried non-parents in South Korea [11].

Social isolation and loneliness
Several studies reported social isolation and loneliness amongst cancer patients [9,20,38,48,49] which was mediated by detachment from loved ones, lack of social interaction, loneliness, fear of infection, worries about the future, and economic difficulties [38]. Several at-risk groups identified as feeling isolated and anxious. These included American women with ovarian cancer (10%) [20]  and young cancer patients (aged 18-39) undergoing cancer care who felt more isolated (52%) than pre-pandemic, specifically missing social interactions [9]. Elran-Barak and Mozeikov [48] reported that lower levels of education and living without minor children in Israel were associated with feelings of loneliness and isolation. Leach et al. [26] in the USA found cancer patients experiencing social distancing and living alone had feelings of loneliness, while disruptions to cancer care were associated with increased loneliness and social isolation [26,49]. Some patients' perceived risk of COVID-19 infection caused them to engage in extreme levels of social isolation where they had no visitors and lived alone [26]. For others, the pandemic exasperated underlying situations. For example, Miaskowski et al. [49] upon comparing a more stressed group to a less stressed group found the former reported significantly higher levels of loneliness and social isolation and less resilience than the less stressed group.

Implications of social and psychological impacts
The review revealed that depression and anxiety progression might be associated with deliberate appointment delays [14]. When delays were at post-treatment follow-up or palliative care, this was exasperated further [42]. Also, Shinan-Altman et al. [31] found that while incidences were low, patients with higher anxiety had more contact with healthcare professionals during the pandemic. Nevertheless, amongst the sample, anxiety did not directly influence healthcare decision-making.
Changes to the way healthcare organisations altered cancer care, to reduced COVID-19 transmission and increased uncertainty, for which tolerance and resilience varied. Hill et al. [23] found COVID-19 fear and intolerance of uncertainty were strongly correlated. Studies reported that health management changes to treatment plans increased patients' psychological burden [9,14,20,40,43,[50][51][52][53]. These changes also increased uncertainty with an association between intolerance of uncertainty and anxiety, depressive symptoms, and stress [23]. While uncertainties can be reduced with additional information, health literacy is influenced by socio-economic factors. Erdem and Karaman [39] found that higher educational status was associated with better knowledge of COVID-19 transmission. Better knowledge of COVID-19 was associated with patients aged 40-54 years, in higher education, being female, living in urban areas, with a profession, and a higher income amongst a sample of Romanian cancer patients [37].
Collectively, adverse effects on specific mental health domains had a broad impact. For example, loneliness and isolation amongst cancer patients contributed to declines in general mental health [48] and translated into declines in QoL [15,20]. Several studies found deterioration in QoL due to COVID-19 compounded by the effects of treatment and financial implications in terms of affordability of care [20,26]. Despite some respondents being aware of and worried about their QoL [20], those with higher stress levels concerning COVID-19 had worse QoL [40]. Lower QoL and emotional functioning scores were correlated with concerns about contracting COVID-19 [24], with negative spill-over effects found on general health status and physical health in Italy [53] and Israel [48], respectively. Aggravating this further was postponement of care, which negatively impacted QoL [53]. Socio-economic differences were found here too. A higher QoL was correlated with patients who were older [54], employed, with fewer co-morbidities, and not receiving treatment within the last two months [24]. Patients with brain tumours, endometrial/cervical/vulva, and thoracic cancers had lower QoL scores [24]. Being female, having lower educational attainment, crowded housing conditions, and longer illness duration also negatively affected self-reported health status among patients in Israel [48].

Out-of-pocket expenses
From an individual perspective where treatments are not covered under government schemes or insurance, patients experience a large financial burden, in-terms of out-ofpocket expenses, expensive health insurance premiums, or deductibles [26]. This was the case for a considerable proportion of cancer patients in India [44] and Jordan [50]. While this is not a new phenomenon, it has been exasperated by COVID-19. Modified workflows and redistributed cancer care resources saw widespread use of telemedicine, with mixed effects. Transition to telemedicine saved US patients' time and money ($170) [55]. In contrast, Bakkar et al. [50] found that treatment changes incurred additional patient costs in Jordan. Globally, testing for COVID-19 (negative results were required to attend appointments) introduced varying fee structures with additional costs experienced amongst cancer patients in India [56] and South Korea [11]. These costs affected patients' decision to undergo cancer treatment particularly in poorer countries [56].

Household finances
Widespread lockdowns during COVID-19 Wave I caused an economic downturn, with negative implications on labour markets. Cancer patients in India (22.2%) expressed fears around losing their jobs and the implications of the expected economic crisis for their family [13]. Similarly, in the USA, cancer patients reported concerns with maintaining employment. These economic conditions exasperated pre-existing cancer financial burdens, including paying for prescriptions and high insurance deductibles in private healthcare markets in the USA [26]. US patients were also concerned with affordability of treatments and transportation to medical facilities [34]. Reduced earnings caused some patients to choose not to attend medical appointments. For example, 46% of cancer patients in India reported financial difficulties as the primary reason for missed consultations [57].
Several studies identified socio-economic factors associated with the economic impacts of COVID-19. Patients that were unemployed, with low educational attainment, or with lower incomes, or were under financial pressure had greater difficulties accessing care in India [44]. In the USA, non-Hispanic white, married, more educated, and older cancer patients were less likely to cite financial worries [26]. These socio-economic inequalities coupled with increased financial burden create barriers to accessing care [44].

Payers and providers
The consequences of COVID-19-related healthcare changes are potentially worsening patients' clinical condition, which also has economic consequences at the provider level with implications for patients. For example, there is an increased likelihood of post-operative ICU following delayed surgery [58]. During the pandemic, demands for services like respiratory assistance increased. This dual increase in demand had resource implications for healthcare providers; reduced resources limit choices to delivering post-operative cancer care or care for COVID-19 patients [59].
The introduction and expansion of telemedicine during the pandemic had mixed effects for healthcare providers and payers. Parikh et al. [55] reported the transition to telemedicine saved hospitals time and money in the USA. However, Goenka et al. [60] report that while it did ensure continuation of care, its cost and financial impacts must be considered. It may not be financially suitable for all care due to implementation and maintenance costs compared with reimbursement received, cost savings to patients (direct and indirect), and care coordination. Mahl et al. [42] found similar results for tele-consultation technologies for palliative and follow-up services in Brazil. Furthermore, the high prevalence of anxieties and fears discussed above culminated in increased demand for support services and information, as demonstrated by the increased volume of calls, emails, and messages found in one North American study [34]. One Italian study found such communications tended to have more negative than positive messages (57% vs 43%) [21].

Innovations to mitigate impacts
Social and psychological impacts, along with modified workflows that redistributed healthcare resources, had an economic impact on patients and healthcare systems. US patients experiencing higher stress had more financial concerns [49], and COVID-19 exasperated existing financial burden associated with cancer on families, with some not being able to afford to attend consultations [57]. Studies revealed coping strategies adopted by cancer survivors and patients to deal with the impact of the pandemic [20,61]. Mechanisms used to cope included connection to family and friends, spirituality/prayer, music therapy, emotional supports, positive reframing, and daily routine, including self-care, hobbies, and planning [30,61,62]. These strategies were an important predictor of QoL [20] and positive health behaviours. Positive lifestyle choices were likely to alleviate mental health burden and improve HRQoL [30,35,54], while others employed avoidance coping strategies, including self-distraction and substance use [62].
Using positive coping strategies was important as delivery of support services was adversely impacted by COVID-19 [13,51,61]. Such supports included psychological and peer group support services, counseling for patients [13,51,61], and caregiver supports [35]. Maintaining or quickly resuming these supports during the pandemic was associated with less anxiety [35] and distress [51]. Additionally, patients with higher social support had more contact with healthcare professionals during the COVID-19 pandemic [31].

Discussion
Economic burden associated with cancer for patients is measured through direct and indirect costs with both objective (i.e. financial burden) and subjective approaches (financial distress) [3]. This adjustment to economic burden measurement coincides with the growing knowledge of cancer as a chronic disease, which widens perspective and shifts understanding of possible side effects beyond clinical outcomes.
Pre-pandemic psychological strain was caused by possible cancer treatment side effects which have adverse health outcomes [63]. The pandemic exasperated these health outcomes further. National and institutional public health guidelines to reduce COVID-19 transmission resulted in suspended cancer screening programmes, delayed diagnoses, postponed or deferred treatments, and altered treatment regimes in many countries. These health system shocks also altered patients' decision making and health-seeking behaviours. For example, to shield from COVID-19, patients delayed seeking medical appointments, avoided clinical settings, etc. In the immediate and long term, this has direct impacts on health outcomes, increasing cancer morbidity and mortality. Longer-term strategic outcomes are also hampered with deferred cancer strategies that have direct consequences for achieving high-level targets such as the United Nations' (UN) Sustainable Development Goal 3 of good health and well-being for all and the European Commission Cancer Mission of improving the lives of those affected by cancer through prevention and cure.
Collectively, these types of costs can affect patients' QoL that represents an additional cost to their well-being [3,64,65]. This review predominately captures the experience during the first wave of the pandemic, when national lockdowns and public health guidelines were at the highest level internationally. So while many of the impacts and costs from previous frameworks [3] were identified in the review, the studies adopted a short-term perspective. We suspect that as the pandemic persists, and more longitudinal data becomes available, further costs and impacts will be documented capturing a broader range of costs, for example, re-distribution of resources in healthcare delivery and subsequent opportunity costs of telemedicine from a patient and provider perspective, the associated treatment costs of COVID-19, or the feelings of isolation that affected QoL.
Despite gaps in range and severity of costs, evidence from this review demonstrates the demand for psychological support and information to alleviate fears and provide reassurance to patients. COVID-19 increased information asymmetries in the delivery of all healthcare services, including cancer care. Imperfect and inadequate information create uncertainties which influence patients' behaviour and decision-making. With poor information and high levels of uncertainty, patients were risk adverse, reducing their health-seeking behaviours, avoiding public transport, clinical settings, etc. Such behaviours have long-term impacts; later diagnosis and delayed treatment adversely impact cancer patients' health outcomes, QoL, and mortality.
While economies and healthcare systems are recovering, COVID-19 remains a threat for cancer patients. Accurate and effective information and support for cancer patients are still needed to mitigate further impacts and to support patients in its aftermath. In some settings, tele-health could be used to provide this; however, a one-size-fits-all approach is not suitable. Supports and information need to be tailored to the target audience, depending on the healthcare system characteristics, resources available, and the socio-economic profile of the patient population. This is imperative as we emerge from the pandemic, to mitigate its affects, promote recovery in health systems and in patients, and implement learnings for future possible pandemics.
The review revealed several approaches to minimise the economic, social, and psychological impacts of COVID-19 for cancer patients, centring around provision of information and support services and coping strategies. Regarding information, three recommendations emerged. Firstly, more information is required, specifically with regard to how to cope with the pandemic [9]. Secondly, effective communication between physicians and patients is required [14]. Effectively delivered communications provide valuable information that can reduce information asymmetries. Thirdly, information could be provided via online education programmes, which may alleviate anxiety and improve HRQoL [35], as appropriately designed interventions can reduce cancer-related psychosocial outcomes and quality of life [66,67].

Limitations
This review mainly captured the first wave of the COVID-19 pandemic in March 2020. Many studies were reliant on single institutions (e.g. [44,55]) and lack long-term followup [55]. In some cases, data were only available for short periods (e.g. [44,59]) which had negative implications on sample size. Data collection methods varied, with many using online methods that can exclude those experiencing technology barriers.

Conclusion
COVID-19 compounded the economic, social, and psychological impacts of cancer on patients owing to health system adjustments and reduction in economic activity. Identification of the impact of COVID-19 on cancer patients from a psychological, social, and economic perspective following the pandemic can inform the design of timely and appropriate interventions and supports, to deal with the backlog in cancer care and enhance recovery. While the long-term effects and economic fallout for cancer patients are not easily quantified, they are real and further support is required to alleviate the issues cancer patients face.