Financial toxicity among cancer patients, survivors and their families in the United Kingdom: a scoping review

Abstract Background The aim of this scoping review was to identify key research gaps and priorities in order to advance policy and practice for people living with cancer in the UK. Methods The review adhered to PRISMA guidelines for scoping review. We searched MEDLINE, EMBASE, Scopus, Web of Science and Google Scholar on 16 July 2022. There were no restrictions in terms of study design and publication time; gray literature was included. The key words, ‘financial’ or ‘economic’, were combined with each of the following words ‘hardship/stress/burden/distress/strain/toxicity/catastrophe/consequence/impact.’ Results 29/629 studies/reports published during 1982–2022 were eligible to be included in the review. No study conducted a comprehensive inquiry and reported all aspects of financial toxicity (FT) or used a validated measure of FT. The most three commonly reported outcomes related to financial hardship were financial well-being (24/29), benefit/welfare (17/29) and mental health status (16/29). Conclusions It is evident that FT is experienced by UK cancer patients/survivors and that the issue is under-researched. There is an urgent need for further research including rigorous studies which contribute to a comprehensive understanding about the nature and extent of FT, disparities in experience, the impacts of FT on outcomes and potential solutions to alleviate FT and related problems.


BACKGROUND
The term 'financial toxicity', while lacking an agreed definition, is commonly used to refer to both the objective financial burden and the subjective financial distress experienced by cancer patients, survivors, and their families as a result of cancer diagnosis and treatment [1,2].
Objective financial burden stems from out-of-pocket payment (OOP) related to direct medical costs, direct non-medical costs (e.g., fuels for transportation, heating, special foods), and indirect non-medical costs (e.g., loss of income) [3].Subjective financial distress, which is much more complex to assess, results from (i) the accumulation of OOP spending (direct from income or indirect through using savings or selling property); (ii) the concerns about the costs and how to deal with them; and (iii) the challenge of changing behaviours and carrying out cost coping strategies (e.g., seeking financial assistance, reduce leisure activities) [3,4].
Financial toxicity (FT) leads to a range of adverse financial, medical, and social outcomes.
Firstly and most obviously, the financial well-being of patients, survivors, and their families may be negatively impacted by FT as they may lose savings and/or assets; have lower income and slower career development due to employment disruption during the cancer treatment; accumulate debts on credit cards; and fall behind on mortgage payments [3,5].Regarding health outcomes, lower health-related quality of life (HRQoL) has been mentioned by several studies on the topic [4][5][6][7].Financial toxicity may also result in additional mental health distress and conditions such as depression and anxiety -the risk of developing these kinds of mental health problems is 3 times higher among cancer survivors who experience FT compared to cancer survivors without financial hardship [8].
The risk of FT and the level of severity varies between countries.In part this can be explained by variations in access to publicly funded care and welfare supports.It might be reasonable to expect that FT is more relevant in low-and middle-income countries (LMICs) where patients are more financially vulnerable and OOP accounts for 30-50% of health care financing [9].In fact, even in high income countries (HICs) with publicly funded health system and universal coverage, FT exists and has now become a serious issue [8,10,11].Studies from Canada, Italy, Germany, and Japan have reported significant prevalence of FT among cancer patients/survivors as well as its impact on health outcomes [7,[11][12][13].For example, in Italy where services are provided free at point of use by the state, a study with pooled data from 16 prospective multicentre trials reported 22.5% patients experienced FT that was significantly associated with an increased risk of death (HR 1.20, 95% CI 1.05-1.37,P = 0.007) [7].
Media reports and voluntary sector bodies report the existence of FT among cancer patients in the UK and growing concerns regarding its effects in light of rapid increases in energy prices, rising inflation and interest rates.While the overwhelming and increasing cost of treatment, patient visits, and prescriptions are covered by the government, all other direct non-medical and indirect costs still fall on the patients.Research has shown that individuals from the most socioeconomically disadvantaged groups such as lower income families, rural dwellers, minority groups, immigrants, and young people are at greater risk of financial hardship [5,8].
Despite the importance of the problem and growing interest, there is uncertainty about the nature and extent of FT studies in the UK.This scoping review was conducted to review available published and grey literature about FT among cancer patients, survivors, and their families in UK.The aims were to chart available empirical data about the topic of FT, identify the research gaps and key research priorities to advance policy & practice for people living with cancer in the UK.

METHODS
The conduct of this scoping review followed the methodological framework proposed by Arksey & O'Malley (2005) [14] and Levac et al (2010) [15] as well as the PRISMA guidance for the conduct and reporting of scoping reviews [16] (See Appendix 1, Supplementary information for PRISMA-ScR checklist).There are five key stages to conducting a scoping review (plus optional stage 6).

Stage 1: Identifying the research question
Our research question was, 'What is known from existing literature about financial toxicity among cancer patients, survivors, and their families in the UK?'.We used the framework of FT proposed by Witte et al (2019) [4] wherein subjective financial distress was classified into three domains: (i) material conditions (e.g., the use of active and passive financial resources), (ii) psychological response (e.g., worries and concerns about their financial situation), and (iii) coping behaviours (to manage increased expenses).We decided to search for studies that reported data related to any aspect of these domains in order to ensure the breadth of coverage.

Stage 2: Identifying relevant studies
We performed the search in four bibliographic databases including MEDLINE (via Ovid, 1946present), EMBASE (via Ovid, 1947-present), Scopus (2004-present), and Web of Science (1900-present) on July 16, 2022.Search inquiries did not apply a time limit or restrict any study type, but an English language-only restriction was applied.The results from initial searching indicated that the term 'financial toxicity' was not used commonly in the UK; therefore, we applied a wide range of alternative terms and a broad encompassing search strategy.The terms, 'financial' and 'economic' respectively were combined with hardship or stress or burden or distress or strain or toxicity or catastrophic or consequence or impact.Detailed database search strategies are presented in Table S1, Supplementary information.In order to capture a wider range of study designs as well as grey literature, we searched Google Scholar and websites of relevant charity organisations including Macmillan Cancer Support, Cancer Now, Cancer Action, and Young Lives vs Cancer (formerly CLIC Sargent).Additional potential papers were retrieved from the reference lists of included studies.Literature for which full text was not available (e.g., conference abstract) were excluded as information provided in an abstract is not enough to capture the full scope of an article and hinder the accuracy and quality of interpretation.

Stage 3: Study selection
Selection criteria for studies were based on the PEO framework (PEO -Population, Exposure, and Outcome) as follows: (1) Population: cancer patients (those who are under treatment, including patients with initial treatment after diagnosis and people with on-going treatment for metastatic cancer), cancer survivors (those who finished initial treatment), and family members of cancer patients/survivors (whether or not they were providing informal care); (2) Exposure: financial toxicity (including objective financial burden and subjective financial distress) experienced by the population of interest; (3) Outcome including financial well-being, HRQoL, mental health status and conditions such as depression and anxiety, benefits/welfare, counselling service, and any other support with a purpose that was to ease FT.Details of inclusion/exclusion criteria are presented in Table S2, Supplementary information.
All citations resulting from the searches were imported into Covidence (web-based software platform that streamlines parts of the systematic review process).After removing duplicated citations, a selection process was conducted in two steps including 1) Title and abstract screening, and 2) Full-text review.Two reviewers (TTN and THT) independently conducted these two steps.
In step 1, studies were moved to full-text review if at least one reviewer voted 'included'.In step 2, when disagreement on study inclusion occurred, final inclusion was reached by consensus.

Stage 4: Charting the data
A data charting form was developed and piloted by the research team using three randomly selected included studies and refined accordingly (See Appendix 3, Supplementary information).Two reviewers (TTN and THT) independently extracted data.Recorded information revolved around the PEO framework and the Witte et al (2019) conceptualisation of FT [4] and included (i) General information (author(s) and their affiliation, year and type of publication, geographic coverage); (ii) Methods and participants (Objectives/research questions, study design, studied population); (iii) Exposure (FT) and outcomes (terms were used to describe the problem of FT, exposure definition or description, tools were used to measure it, outcomes of FT were studied); and (iv) Key findings.

Stage 5: Collating, summarising, and reporting the results
We provide a descriptive numerical summary analysis of the extent, nature, and distribution of the included studies to show the dominant areas of research.We then provide a qualitative thematic analysis in which findings from included reviews were organised and presented by different outcomes of FT.Finally, the implication of findings, the broader context and recommendations regarding future research are presented.

RESULTS
We identified 740 citations from systematic searches on four databases and included the first 200 search results on Google Scholar.After removing duplicates, 623 citations were screened by title and abstract.53 citations were moved to full-text review, of which, 23 were included  (See Appendix 2, Supplementary information for full list of excluded reviews and justification for the exclusions).There were 6 additional studies (2 peer-reviewed articles [40,41] and 4 grey literature reports [42][43][44][45] identified through manual searches of the reference lists of included citations and websites of relevant organizations.As a result, a total of 29 studies were included in analysis  (Figure 1).
In the only study that specifically investigated financial toxicity, patients were surveyed and classified as facing FT when they experienced greater financial burden at follow-up compared to their assessment at baseline [31].Financial burden was identified based on only one question (Q28) in the European Organisation for Research and Treatment of Cancer (EORTC) core Quality of Life questionnaire (EORTC QLQ-C30) which asked patients to score financial difficulty relating to disease or treatment from 1 (not at all) to 4 (very much) [31].
No study used a validated instrument to assess FT such as 'COST -The COmprehensive Score for financial Toxicity' [46].Most studies used bespoke questionnaire while some used generic instruments which cover a wide range of aspects related to cancer care such as Supportive Care Needs Survey-Short Form 34 (SCNS-SF34) [38], EORTC QLQ-C30 [22,27,31], and Social Difficulties Inventory (SDI) [22,27].
Only 2/24 studies quantified the loss of income and extra expenditure.Studies from Macmillan reported that households, on average, were £570 worse off per month following a diagnosis of cancer [43].Young Lives vs Cancer studies reported that parents spent £600 extra per month during active treatment of their children while young cancer patients spent £360 extra per month [45].Likewise, few studies (5/24) reported the disparities among sociodemographic groups.These studies reported that financial impact was more severe for those of working age, especially self-employed or part-time employed [19,22,43]; lone parents [20]; and among those who belonged to minority ethnic groups [33].
Impact of benefit/welfare system 17/29 studies detailed the experiences that were reported by patients, survivors, and/or carers regarding the benefit/welfare system [17-19, 21-24, 26-28, 30, 32, 33, 35, 36, 41, 45].Financial burden resulted in cancer patients applying for benefits such as attendance allowance, disability attendance allowance (DLA), and/or personal independence payment (PIP) [22,33,45] even though there was stigma associated with applying [18,24].Studies also reported patients' dissatisfaction towards the benefit system -they complained that the application process was complicated and lengthy [26,41,45], the benefits that they received were inadequate [35], and there was an overall lack of information about benefit entitlements [18,19].All these issues added to the stress felt by patients (more details in next sub-section).2/17 studies reported that patients who did not qualify for state benefits (their applications were denied) had to rely on grants from charitable organisations or support from family/friends [17,22] though these two studies were published in 1982 and 2012.
The most common aspect reported was 'worry about money' which led to additional stress [19,24,35,42,45] and, as quoted, 'if you've got money worries it brings you down a little bit further' [19].Lone parents were more likely to report money worries [20,41].Occurrence of negative emotions such as regret, disappointment, and self-reproach about their financial situation was viewed as leading to coexisting health problems and other difficulties [40].
Family stress/strife, breakdown of relationships/families were other significant psychosocial challenges facing patients and carers [40].

Impact on employment during and after treatment
5/29 studies reported the impact of financial burden on employment of patients, survivors, and/or carers during and after treatment [26,30,34,39,40].All these studies reported that patients had to return to work prematurely due to financial pressure as a result of being off work.

Impact on health-related quality of life
Only 2/29 studies reported the impact of financial burden on the HRQoL of patients, survivors, and/or carers [23,42].Macmillan's study reported that the HRQoL of 61% of patients was negatively affected though the validity of the method of measuring HRQoL was unclear [42].
Rogers et al (2012) reported that 53% of patients who suffered financially had decreased HRQoL as measured by the University of Washington Quality of Life questionnaire (UWQoL) [23].

Nature, extent and distribution of studies
No study in the UK has investigated FT as this term is commonly understood.Flaum et al (2020) was the only study with the explicit objective of investigating financial burden and FT.According to the authors, it was the first study of FT among UK cancer patients and it reported a prevalence of 20% of cancer patients who experienced FT [31].However, the definition of FT in this study did not follow international practice.Financial burden was identified based on only one question (Q28) from the EORTC QLQ-C30 while FT was defined as greater financial burden at followup survey [31].Objective financial burden and subjective financial distress were not clearly delineated in any study.As a result, we needed to adjust and broaden the inclusion criteria of the scoping review in order to include studies that reported any aspect of FT.
The significant increase in the number of publications on the subject in recent years reflects a growth of interest in the issue of FT within the field of cancer research.These publications came mostly from authors in academia though there were contributions from charity organisations and/or hospital Trusts.Indeed, charity organisations have published their own reports about the financial impact of cancer.These reports appeared to indicate a stronger presence of a wide variety of aspects related to financial impact than the peer-reviewed articles which tended to focus on only one aspect.While the voluntary sector has spearheaded research in this area, collaboration between the voluntary sector and academics may in the future help bring additional rigor to such studies and give a greater degree of credibility to their results.
Regarding geographical coverage, only one third of included studies provided UK-wide data.
However, potential differences between England, Scotland, Wales, and Northern Ireland were not studied, despite the fact that these countries face distinct economic environments and organize health and social care differently [47].This should be a consideration for further research.

Methods of studies: Design, participants, exposure, and outcomes
Most common study designs were applied in included studies, including mixed-methods, a cross-sectional study, secondary data analysis, qualitative research, and a systematic review/review.However, a key limitation is that all quantitative studies used retrospective data.
There has not been a study in the UK that has used prospective data to investigate the issue of FT among cancer patients.A prospective cohort study following patients from the point of diagnosis to finish initial treatment would provide invaluable insights to the causes and effects of FT on cancer patients.Such studies may be less likely to be subject to recall bias as well as providing the opportunity to study the relationship between FT and cancer as treatment progresses and/or economic conditions change.
The most studied population was cancer patients.Studies have paid some attention to survivors and carers/family members though they tended to be studied separately.Future research should assess the FT situation from the perspective of all key parties (i.e., patients, survivors, carers/family members) as well as the views of other stakeholders such as the community and voluntary sector.The involvement of one or more charity organisations in the recruitment process and the associated larger sample sizes in these studies points to the importance of adopting a collaborative approach in future research.
The validated questionnaire to investigate FT, COST, has not been used in any UK studies.
Authors often used bespoke questionnaire or generic instrument which was not specialised for the issue of FT.It is recommended that future research should use COST to improve research rigour and facilitate the comparison of results with similar research around the world.

Key findings of studies -dominant areas of research amongst studies
The majority of studies focused on describing objective financial burden and its material impact on the financial well-being of cancer patients, survivors, and/or carers/family members.
Subjective financial distress, especially its psychosocial effects, is under-researched.There is a need too to give research attention to investigating disparities between different sociodemographic groups.The review found that studies are sparse regarding the causes of financial stresses and strain.Whilst some FT-related outcomes were investigated (e.g., impact on financial well-being, mental health, employment, HRQoL), there is a need to assess FT using psychometrically validated instruments.These critical gaps for future research need to be addressed in order to plan person-centred service responses for patients who encounter FT.

Strengths and limitations
This scoping review provides a comprehensive and thorough review of available literature about financial toxicity among cancer patients, survivors, and their families in the UK.As a first step, the scoping review identified key research gaps and suggested priorities for future research.Our comprehensive and systematic approach to identification, selection, data charting and analysis followed the rigorous methodological framework set out by Arksey & O'Malley (2007) and Levac et al (2010) [14,15] and PRISMA guidance for the conduct and reporting of scoping reviews [16].We plan to carry out (optional) stage 6 of the methodological framework (i.e., consultation exercise) in the months ahead.

CONCLUSIONS
There exists a paucity of research on financial toxicity among cancer patients, survivors and their families in the UK.Current evidence is ad hoc and at times anecdotal with studies using different definitions, methods and studying often only small parts of the overall issues.
Nevertheless, that FT exists in the UK is evident.A comprehensive study designed to provide a better understanding about the nature and extent of the problem, disparities in experience (among different sociodemographic groups and types of cancer), the impacts of FT on outcomes, and potential solutions to alleviate FT and related problems is urgently needed.[28] Benefits and allowances that families may be entitled to claim Com menta ry x x a. Increased financial burden due to loss of income and increased costs for special diet, new clothing, heating, travel, and car parking b.Financial support from state welfare benefit system were needed the most by people with limited or no income Moffatt 2012 [21] Impact of welfare rights advice services on the quality of life and wellbeing of people with cancer Mixed P + C

Tables and Figures
x x b.Welfare benefits helped offset additional costs associated with cancer c.Receiving welfare benefits reduced levels of stress and anxiety related to financial difficulties.Rogers 2012 [22] Financial burden of having head and neck cancer, and its relation with health-related quality of life (HRQoL) Quan P x x a. 54% patients experienced at least one moderate or large financial burden.Greater financial difficulty due to loss of income.Younger people were more likely to experience financial difficulty b. 39% patients applied for benefits.Of those applied, 71% had received it.Patients in working age and men were more likely to apply for benefits

Figure 1 Figure 2
Figure 1 PRISMA flow diagram of literature search and selection

Table 1 :
Overview of general information, methods, and participants of 29 included studies

Table 2 :
Summaries of included studies' key findings (studies published before 2011)

Table 3 :
Summaries of included studies' key findings (studies published after 2010) .

Table 1 . Overview of general information, methods, and participants of 29 included studies
* Not mutually exclusive

Table 2 : Summaries of included studies' key findings (studies published before 2011)
Study design -Mixed: Mixed methods, Qual: Qualitative research, Quan: Quantitative data, Rev: Narrative review, Sys rev: Systematic review Pop: Studies population -C: Carers/family members, P: Patients, S: Survivors

Table 3 : Summaries of included studies' key findings (studies published after 2010)
The number of parents who said that money was 'often' or 'frequently' a worry increased eight-fold after diagnosis, from 8% to 65%.76% families said that childhood cancer had been a 'big problem' for their finances.Loss of income, especially for patients were in paid employment or self-employed at the time of diagnosis.Less or no impact on income of retired participants.Spend of savings, selling of possessions, altering usual activities and enjoyment of life to cope with loss of income c.Occurrence of negative emotions such as regret, disappointment, and self-reproach could lead to coexisting health problems and other difficulties.Family stress/strife, breakdown of relationships/families were other psychosocial facing patients and carers d.Return to work prematurely due to financial commitments.Concerns about job loss, employability, and lack of promotion.Callanan 2012