The unmet supportive care needs of people affected by cancer during the COVID-19 pandemic: an integrative review

Purpose To critically synthesise evidence regarding the supportive care needs of those living with cancer during the COVID-19 pandemic. Methods An integrative systematic review followed a pre-registered protocol, reported according to the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) Guidelines. We searched three databases (CINAHL, MEDLINE, and APA PsycINFO) using keywords and included all qualitative, quantitative, and mixed methods studies irrespective of research design published between December 2019 and February 2022. All articles were double screened according to a pre-determined eligibility criterion with reference lists of the final included studies checked for further studies. The review process was managed using Covidence systematic review software. Data from the studies were extracted, methodological quality appraisal conducted, and a narrative synthesis conducted. Results Eighteen publications were included. The findings identified that individuals affected by cancer reported a range of physical, psychological, social, and health system unmet needs during the global pandemic. Unique to the pandemic itself, there was fear of the unknown of the longer-term impact that the pandemic would have on treatment outcomes, cancer care follow-up, and clinical service delays. Conclusion Many individuals living with cancer experienced unmet needs and distress throughout the different waves of the COVID-19 pandemic, irrespective of cancer type, stage, and demographic factors. Implications for Cancer Survivors We recommend clinicians use these findings to identify the individual person-centred needs to optimise recovery as we transition to the post-pandemic cancer care. Supplementary Information The online version contains supplementary material available at 10.1007/s11764-022-01275-z.


Introduction
Globally, cancer is a significant cause of mortality. In 2020, cancer caused ten million deaths, equating to nearly 1 in 6 people [1]. Many individuals affected by cancer require timely supportive care and rehabilitation in routine clinical service delivery [1]. In March 2020, the World Health Organization (WHO) declared COVID-19 as a global pandemic [2]. This pandemic has consumed peoples' existing way of life in every aspect, from lockdowns, mandated mask wearing, to transitioning new models of cancer care delivery [3], and adhering to ever changing social distancing requirements [4]. Cancer services had to manage burgeoning clinical service demand due to COVID-19 and adapt to adhere to constant changes in legislation, restrictions, and transition cancer service models of care to models of telehealth [5].
Supportive care is defined as a person-centred holistic approach to the provision of cancer services for those living with or affected by cancer [3,6]. This holistic lens to care encompasses the informational, social, psychological, spiritual, and physical needs during diagnosis, treatment, or follow-up phases, including issues of health promotion and prevention, survivorship, palliation, and bereavement [7]. An existing suite of systematic reviews have already identified the unmet supportive care needs in a variety of cancer groups [7][8][9][10][11][12] prior to the COVID-19 pandemic underscoring a range of unmet supportive care needs for people affected by cancer. Noteworthy, one recent systematic review [12] excluded patients reporting unmet supportive care needs during the COVID-19 pandemic because this was beyond the scope of their review. Therefore, evidence is yet to be pooled and critically synthesised to enable health care professionals and researchers to comprehensively understand the impacts of COVID-19 on supportive care experiences among people affected by cancer [3]. Gaining new insights about the supportive care needs experienced during the COVID-19 pandemic will not only inform transitions of care moving into the endemic but may highlight helpful knowledge insights which could be applied to learnings in the preparation for future pandemics within cancer health care systems and care needs.
An interruption or change to the accessibility of cancer screening, diagnostic, and treatment services has a significantly negative impact on the outcomes of cancer treatment for patients [13]. It has been suggested that addressing supportive care needs is the foundation of a successful intervention because of its positive influence on quality of life and psychosocial outcomes [6,7,10]. Therefore, the purpose of this systematic review was to critically synthesise evidence related to supportive care needs of those affected by cancer during the COVID-19 pandemic and address the research question: "What are the unmet supportive care needs among people diagnosed with cancer during the COVID-19 pandemic?".

Methods
This integrative systematic review [14] is reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRIMSA) guidelines [15]. We pre-registered the integrative review protocol on the National Institute for Health Research PROSPERO -International Prospective Register of systematic reviews with the review available from: https:// www. crd. york. ac. uk/ prosp ero/ displ ay_ record. php? Recor dID= 313525.

Types of studies
All qualitative, quantitative, and mixed methods studies irrespective of research design which identified supportive care needs among people affected by cancer during the COVID-19 pandemic. The WHO declared the first case of the Novel Coronavirus on the 31 st December 2019 [16] and later declared COVID-19 as pandemic on the 11 th March 2020 [2]. Therefore, the database search was limited to December 2019 to February 2022 to capture all studies related to the research question. All commentaries, editorials, and studies where supportive care needs were not reported and published in non-English language were excluded.

Types of participants
All participants affected by cancer irrespective of age, gender, cancer type, stage, or treatment and their family members and caregivers were included.

Types of outcome measures
The primary outcome of this review was related to unmet supportive care needs (e.g. the Supportive Care Needs Survey [17]) and qualitative experiences, informed by the definition of supportive care [7] explicitly reported in relation to the COVID-19 pandemic (see Table 1).

Literature search
We searched MEDLINE, CINAHL, and PsychINFO using a wide range of keywords and free text items to increase the sensitivity and inclusiveness (see Supplementary  Table 1). The electronic searches began on 24 th February 2022 and concluded on 25 th February 2022. All records were managed using the software package Endnote X20 and uploaded to Covidence systematic review software with duplicate records were removed and pre-selection eligibility criterion applied to all records.

Study selection
Two authors (HL, CP) independently reviewed the publications (titles and abstracts) applying the eligibility criteria. One author (HL) retrieved all full-text articles that met inclusion criteria and all authors independently screening the full-text articles with disagreements resolved through consensus discussion.

Data extraction and management
Data extraction was performed on the retained full-text studies meeting the inclusion criteria. The data were extracted by one reviewer (HL) and independently quality checked by a second reviewer (CP and PK). The data extraction tables were developed and tested on a small sample of studies and then further refined through discussion among the reviewers. The first table of data extraction included information on the purpose, setting, country, sample size, participant characteristics, sampling used, response rate, attrition, design, time points, and data collection tools. The second data extraction table related to the supportive care needs outcome data according to the classification of supportive care needs.

Quality appraisal
The quality appraisal of all included studies was conducted by utilising the Mixed Methods Appraisal Tool (MMAT) [18]. The MMAT enabled quality appraisal of qualitative research, randomised controlled trials, quantitative descriptive studies, and mixed methods studies. There are seven questions for each category of study design, ranked as "Yes" (green), "Unclear" (yellow), or "No" (red). The quality appraisal enabled the research team to identify limitations and potential bias within each of the individual studies. No study was excluded based upon individual methodological quality appraisal scores to enable an understanding of the current state of the evidence base.

Data synthesis
This review completed tabulation of primary research studies and use of narrative synthesis to generate findings. The data synthesis process followed the integrated review methodology proposed by Whittemore and Knafl [14]. Data synthesis involved data reduction (subgroup classification by study design and domain of unmet need, with results tabulated), data comparison (identifying patterns and themes through clustering and counting and making contrasts and comparisons), and conclusion drawing and verification (synthesis of subgroup analysis to inform a comprehensive understanding of the topic, verified with the primary source data for accuracy).

Results
Of the 122 publications retrieved from the search, we removed 19 duplicates (see Fig. 1). In total, 33 papers were reviewed in full-text and 18 papers included. There were a range of study designs underscoring that this is a developing evidence base; studies included five qualitative, 12 quantitative, and one mixed methods study. Across the included studies, there was a range of methodological quality (see Table 2), with the methodological quality overall considered good across the included studies. Studies were conducted in a range of countries, including USA (n = 7), Germany (n = 1), UK (n = 3), Ireland (n = 1), Italy (n = 1), Canada (n = 1), Iran (n = 1), Brazil (n = 1), Turkey (n = 1), and Australia (n = 1). Sample size varied from 16 to 1529 participants, with a total sample size of 3924 represented in the systematic review. Cancer type varied throughout the studies (neurological: n = 2; haematological: n = 3; head and neck cancers: n = 4; breast cancer: n = 2; varied cancer types: n = 4; and unreported cancer types: n = 3). Population across the studies varied from children and families (n = 3), adults (n = 8), older adults (n = 5), and unreported (n = 2) (see Table 3).

Experiences of unmet supportive care needs
There were a range of unmet supportive care needs related to physical, psychological/emotional, cognitive, patient-clinician communication, health system/information, spiritual,

Identification of studies via databases and registers
Identification Screening Included daily living, interpersonal/intimacy, practical, family, and social needs (see Tables 4 and 5 for an overview). Detailed information in relation to the unmet supportive care needs of the included studies is in Supplementary Tables 2 and 3.

Physical needs
The physical needs were commonly reported across the included studies as a well-being concern. Physical needs were well described in the palliative care cancer participants [19]. Common needs reported included fatigue, weakness, and mobility issues affecting physical functioning and activities of daily living because of restrictions during the COVID-19 pandemic [19][20][21][22][23]. People affected by cancer were socially isolated due to the implications of the COVID-19 pandemic. Many experienced exacerbations of additional onset of pain [19,21,24] because of a reduction to mobility which made accessing an already restricted health care service significantly more difficult. Furthermore, the negative effect of gastro-intestinal symptomatology of nausea, vomiting, poor appetite, a dry mouth, or constipation were also expressed [19] compounding the nutritional deficits experienced by those affected by cancer as a daily unmet need during the pandemic [21]. Lastly, participants noted that the COVID-19 pandemic negatively affected their physical well-being through disturbances to sleep, eating, and exercise [22].

Psychological needs
Many of the participants irrespective of age, cancer type, or treatment regimen expressed unmet needs related to psychological or emotional domains of well-being [19][20][21][24][25][26][27][28]. The fear of contracting COVID-19 in people affected by cancer was further compounded due to their own recognition that they were at an increased risk of infection which led to anxiety and distress.
It contributes to a little bit of anxiety because, you hear over and over and over, people that are in a higher risk category. And, you know, by you being diagnosed       (2) tend to bounce back after illness or hardship All interviews were conducted by a single researcher. Interviews were conducted by telephone (n = 15) and Microsoft teams (n = 1) and were recorded and transcribed verbatim to assist with analysis. Field notes were recorded immediately after each interview to support analysis and research reflexivity After T1 interviews, all participants received a copy of their interview transcript and were provided with an opportunity to amend or clarify their responses prior to data analysis. To enhance the depth of analysis and validation of the study findings, participants will receive a summary of the thematic analysis of interviews conducted at the previous timepoint  were audio recorded and transcribed verbatim by a professional transcription agency During the third interview, an infographic of the preliminary study findings created with the assistance of plain language editors. The infographic was used to discuss the interpretation of results from the first two data collection time points and elicit further perspectives Interview questions touched on a range of topics, including cancer-related concerns, coping, health challenges, and changes to health care appointment delivery. In this article, they focus on the cancer and health service delivery-related data and findings      Children and their families also expressed fear of the unknown in relation to COVID-19. Many participants described that they had come to terms with living with cancer, but were afraid, experienced anxiety and a sense of a lack of control due to the ongoing pandemic as illustrated by this quote: corona is strange and unknown to me [30] page 3.
Many participants commented they were always wearing a mask and went to extreme levels in cleaning and sanitising; and for some individuals even showering after leaving and returning to their house [29]. People affected by cancer acknowledged that COVID-19 was frightening for everyone, not just for those affected by cancer [29]. Noteworthy, some individuals reported that an additional diagnosis of cancer during the pandemic further compounded a sense of an additional "phobia" [30]. Many participants expressed to only feeling safe and secure when at home [30] but when they left the house this caused significant heightened levels of anxiety. People living with cancer voiced [23] issues due to the public perception that they were not visibly ill, and therefore lacked insight into the additional infection control measures needed to protect people with cancer, including those who had immunocompromised status. Strategies driven by fear of contracting COVID-19 [31,32] included taking extra precautionary measures to avoid people, places, hospitals, and for some even family members all of which had an emotional impact. Participants also expressed fear that staff in their local hospitals would not be wearing adequate personal protective equipment (PPE) to keep them safe and protected from the virus while receiving care and treatment [25]. There was also fear of the unknown of the long-term impact that the pandemic would have on treatment outcomes, care follow-up, clinical service delays, and the overall impact that this would have on them in the future [23,24,26]. However, in contrast, some participants [24,33] had significantly higher levels of fear of cancer reoccurrence compared to the fear of COVID-19. Other psychological disturbances reported included how the pandemic negatively affected their sleep [22,23], which compounded a lack of energy and tiredness [24] with temper outbursts [22]. There was also a positive association between fear of COVID-19 and increased symptoms of psychological distress and unmet psychological needs [32,34].

Patient-clinician communication needs
Across the included studies, many expressed concerns with the transition to virtual appointments with their health care team, noting that the previous model of in-person appointments provided reassurance and feelings of comfort [35]. In contrast, telehealth appointments meant it was easier to just agree with their clinician and many patients forget to ask important questions that they wanted to ask: I think because on the phone it's very easy to just go, oh yeah everything, grand, and then the phone call is over in literally a minute or two and then you are like, oh I forgot to ask them that [31] page 8.
Many individuals affected by cancer during the COVID-19 pandemic expressed that the quality-of-care carried out over telehealth was suboptimal compared to in-person consultations. In contrast, only one participant positively noted that telehealth saved a lot of travel time in their day [35]. The transition to telehealth similarly restricted opportunities to engage with health care professionals, with some participants noting a change to empathy, and an attitude to blame COVID-19 for everything that goes wrong [31], while others displayed compounding uncertainty around the next steps in their treatment plans due to lack of interaction with their multidisciplinary care team [23]. Patients reported struggling with opting for support from health care professionals in what might be viewed as them being bothersome, but all they needed and wanted was just their normal follow-up for cancer care [35]. Lastly, some participants reported being most concerned with the reduction in hospital care and access to their care team because of the consequences of reduced face-to-face hospital appointments resulting from COVID-19 infection control policies [27].

Health system and information needs
Many participants represented in the included studies reported additional anxiety and fear during the COVID-19 pandemic when required to attend hospital. Some highlighted concerns regarding the infection control measures and how they varied between patients and staff: None of the patients were wearing masks and you know there was a lady in the bed, you know in the next bed to me who had a cough you know, not COVID but just, you know, things like that [31]  Some participants commented on the lack of available personal protective equipment (PPE) available to hospitals during different stages of the pandemic. Some participants noted that at the beginning of the pandemic accessing masks, gloves, and disinfectants came at high cost to them [30]. Participants often presented common concerns regarding interruptions to the quality and accessibility of care, flow and re-direction of service, and disturbances to the participation in clinical trials [19,20,25,28]. Furthermore, scheduling issues, treatment delays, and miscommunication with health care teams were particularly concerning among the young adolescent cancer survivors [23]. Lastly, participants demonstrated confusion regarding government regulations and testing requirements when attending hospitals and noted that these did not align in every situation. Additionally, participants reported distress that the public were not respecting recommendations in the community to keep others safe given they were living with cancer [30].

Spiritual needs
The spiritual needs of people with cancer were rarely discussed throughout the included studies. These findings represent a potential lack of holistic assessment given the restrictions enforced for funerals, restricted visitors during in-patient, and out-patient hospital visits for people with cancer; however, some participants indicated feelings of peace over distress when describing end of life experiences in relation to COVID-19 in palliative patients [19]. People affected by brain cancer [25] expressed concerns with "end of life" care.

Daily living and practical needs
People affected by head and neck cancers noted periods of social isolation, which were exacerbated at holiday times, when they could not have family or friends over to visit due to the increasing infection risk. Many individuals did not have a support system available to them, resulting in poor diets and reduced oral intake [29]. Findings from several studies observed that participants commented on problems with accessibility of food delivery services and food during shortages causing similar nutritional deficits [21]. Patients sacrificed their self-care due to work demands [36]. Few participated in exercise or health self-management behaviours. Practically, participants expressed varying issues with transport [20,25], resulting in deficits in the accessibility of care [20,32] or medications [21], and causing an overall disruption to their daily lives [22]. Many experienced financial toxicities due to reduced household income. Many participants expressed concerns about reduced household income from not being able to attend work [36] due to enforced lockdowns. Others alluded to issues with medical insurance or reimbursement [25,26], loss of employment, financial difficulties, reduction to working hours, or being forced to take sick or take annual leave [23,28]. Many participants reported distressed about not being able to engage in usual activities of living with a loss of work as an additional practical concern for them [24,26]. Financial concerns were a significant predictor of psychological distress [34] with a positive association between loss of income and unmet needs.

Interpersonal/intimacy needs
Only one study explored interpersonal/intimacy-related needs. Women with breast cancer were the only sample group that reported needs in relation to intimate relationships during the COVID-19 pandemic, noting statistically significant reductions in changes to sexual feelings, sexual relationships, and a lack of information regarding intimate relationships from their health care team during the pandemic [27].

Family-related needs
Children and family represented a small portion of the participants included in this review. Survivors of childhood brain cancer and their caregivers [22] noted that the closure of schools and day-care facilities plus the family's inability to care was disruptive to the family dynamic [25]. A positive association was reported between unmet needs and reduced support within the family to mobilise their own support [27]. Participants expressed feelings of isolation because they were not allowed to attend or support the patient during treatment or be present during discussions with the medical team due to COVID-19 restrictions [19,23,27]. The lack of family support during consultations leads to a significant change in opportunities that contributed to decisional regret in cancer treatment and care decision-making [27]. People affected by cancer also shared worries in relation to job security and the disruption that this causes to daily functioning and broader family-related needs [22,23].

Social needs
Socially, participants of the included studies collectively presented a common theme due to recurrent restrictions and lockdowns leading to feelings of isolation. Across the included studies, many sub-themes of isolation were expressed by participants. One participant noted that not allowing anyone into their home held a substantial impact on their family life as their usual support systems were not readily available to them. Illustrated by the following quote: So you're very much on your own all of the time, you suffer in silence because you know it will end [31] page 7.
Feelings of social isolation extend further beyond support within their home, to simple daily living needs [29] or support when attending hospitals for cancer treatment. People diagnosed with cancer needed to have their family or support network at their side as an important psychosocial aspect of care; however, during the pandemic, this was not allowed. Participants demonstrated they felt mostly isolated by visitor restrictions in hospitals during their treatment journey [25]. Additionally, people affected by cancer were forced to attend review appointments alone: Let's say you're having a PET scan done to see if your if your cancer is gone and you don't have anybody there to celebrate with when you get a good report and you don't have anybody to cry with when you get a bad report. I just I can't imagine doing that all myself. [29]  When people affected by cancer attended appointments alone, they were distressed and conveyed that they needed to have a support person: I'd nobody with me, so nobody heard [the diagnosis], you know my husband wasn't there, so I phoned him when I was outside and I was bawling on the phone, sure he thought I was going to die [31] page 8.
Participants with endocrine-based cancers reported isolation negatively affected their quality of life [26] and others shared feelings of loneliness due to lack of social interaction during treatment [31]. Patients alluded to a positive association between feelings of restriction due to the isolation and psychological distress which significantly impacted their mental well-being [20,23,32]. Some expressed that they felt less connected with family and friends due to restrictions and the stay-at-home orders imposed on all during the pandemic [22]. However, some individuals reported positive feelings toward the pandemic, with participants noting they had increased family time and a new perspective on life [31], positively commenting on the infection control measures in hospital making them feel safe. Some participants [23] reported that they felt a sense of resilience because of the pandemic and they could apply the coping strategies which they developed when they were diagnosed with cancer. Females with breast cancer positively commented on the additional support when coping with house based caring pressures due to the lockdowns and regulations [27].

Discussion
This systematic review sets out to understand the supportive care needs of people affected by cancer during the COVID-19 pandemic. The COVID-19 pandemic has had a significant negative impact on humanity, but more ominously for those living with or affected by cancer. Due to their immunocompromised state, they are required to be hypervigilant toward social endeavours and increased infection control measures when accessing health care facilities whether in-or out-patient. This review critically examined evidence published between December 2019 and February 2022 to identify the experiences of supportive care needs among those living with cancer. It was evident that people living with cancer reported physical, psychological/emotional, cognitive, patient-clinician communication, health system/information, spiritual, daily living, interpersonal/intimacy, practical, family, and social needs specific to the impact of COVID-19. It was evident that patients reported reduced assess and availability for symptom management support during the pandemic, further compounded by the rapid implementation of telehealth services in cancer. These findings have important implications because many individuals experienced poor symptom management because of reduced access to health care services (particularly with problems with pain, nutrition, fatigue, and psychological well-being).
Service reconfiguration, accompanied by social distancing, lockdowns, and curfews, was evident to have a negative impact on people affected by cancer. While it was a necessity that patients needed to be managed, for the most part, without visits to hospitals to minimise infection risk, this was identified as a health care system concern. A significant global push and rapid adoption to transition to cancer care to telehealth services remains [3] but for many participants represented in this review they expressed that they had concerns with this model of care. Patients valued the face-to-face in-person consultations with their care team and found that often the telehealth model lacked empathy and compassion at times, with missed opportunities to ask questions and gain the information that they needed. While momentum continues for the sustained use of cancer telehealth services post-pandemic [37], researchers and health care professionals cannot disregard the important concerns expressed by patients during COVID-19. Further research is needed to identify appropriate risk stratified telehealth models of cancer care [3], to ensure that the challenges of connectivity, communication, and access for remote areas, including safeguarding the elderly and vulnerable patients, are fully addressed.

Limitations
This systematic review has many strengths including the clear and specific methodology which followed a registered priori protocol. In addition, to the independent reviewer's contributions throughout the entirety of the systematic review process, the study provided insights across heterogenous study populations in terms experiences of unmet supportive care needs experienced during COVID-19. There are several limitations worthy of comment. This integrative review only included peer-reviewed studies published in the English language and as such it may have limited our understanding of the wider global impact of the COVID-19 pandemic on those living with cancer with cultural differences. The studies included for review were also conducted in mostly developed and western nations potentially biasing the management and impact the COVID-19 pandemic had on its participants. Despite these limitations, the review team followed a transparent prior review methodology to improve the rigour and validity of the findings.

Conclusion and implications for cancer survivors
The global negative consequences of the COVID-19 pandemic on experiences of supportive care for people living with cancer are evident. This review has identified important areas of unmet supportive care needs, which require careful consideration in the future development of cancer care services. The results of this review may also be applied to and used to inform the management of any future pandemics within cancer supportive care. Although the current emphasis is on managing COVID-19, the focus soon must centre on the recovery plan and restoration of the balance of cancer care in the era of COVID-19 and beyond.
Funding Open Access funding enabled and organized by CAUL and its Member Institutions This systematic review was funded by the University of Canberra PACES Research Scholarship.

Conflict of interest The authors declare no competing interests.
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