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Research Paper| Volume 14, ISSUE 3, 101449, April 2023

The experience of patients with lung cancer during the COVID-19 pandemic and its importance for post-pandemic outpatient cancer care planning: A cross sectional study exploring the roles of age and frailty

Published:February 15, 2023DOI:https://doi.org/10.1016/j.jgo.2023.101449

      Abstract

      Introduction

      The COVID-19 pandemic impacted the care and experiences of people with cancer, but it presented an opportunity to improve the delivery of outpatient care post-pandemic.

      Materials and methods

      We performed an observational cross-sectional study with people with lung cancer throughout the COVID-19 pandemic. A survey investigated patients' experiences and preferences regarding the delivery of cancer care to plan for post-pandemic care, as well as the pandemic's impact on their functional status (physical and psycho-social), exploring the role of age and frailty.

      Results

      Amongst 282 eligible participants, 88%, 86%, and 59% of patients reported feeling appropriately supported during the pandemic by their cancer centre, friends/family, and primary care services, respectively. Remote oncology consultations were delivered to 90% of patients during the pandemic, of which 3% did not meet patients' expectations. Regarding post-pandemic outpatient care preferences, face-to-face appointments were preferred by 93% for the first appointment, by 64% when discussing imaging results, and by 60% for reviews during anti-cancer treatments. Older patients aged 70 years and above were more likely to favour face-to-face appointments (p = 0.007), regardless of their frailty status. Patient preferences changed over time, with the more recent participants preferring remote appointments during anti-cancer treatments (p = 0.0278). Regarding the pandemic's impact, abnormal levels of anxiety and depression were found in 16% and 17% of patients, respectively. Younger patients experienced higher abnormal levels of anxiety and depression (p = 0.036, p = 0.021). Amongst the older sub-group, those with frailty had higher levels of anxiety and depression (p < 0.001). Amongst all participants, 54% reported a considerable negative impact from the pandemic on different aspects of their daily life, particularly emotional and psychological health and sleep patterns, which were more marked in younger patients and the older sub-group with frailty. Older patients without frailty reported the least impact on their functional status.

      Discussion

      There is a need for more personalised outpatient consultation options during cancer care. Whilst there is a preference for face-to-face consultations for older patients, following the pandemic there is a growing acceptance of remote consultations particularly during anti-cancer treatment. Older patients with lung cancer without frailty were less affected by the pandemic than those with frailty and younger patients, requiring less support from healthcare services.

      Keywords

      1. Introduction

      There is evidence to suggest that people diagnosed with cancer, a respiratory disease, or those aged over 65 are at increased risk of severe illness from COVID-19 [
      Underlying Medical Conditions Associated with Higher Risk for Severe COVID-19: Information for Healthcare Professionals | CDC [Internet].
      ,
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      • Pennington A.F.
      • Goodman A.B.
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      • Belay B.
      • Ko J.Y.
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      Underlying medical conditions and severe illness among 540,667 adults hospitalized with COVID-19, march 2020–march 2021.
      ]. People with lung cancer may be particularly vulnerable as many people diagnosed with lung cancer are aged over 75 years [] and are likely to also have other respiratory conditions such as chronic obstructive pulmonary disease [
      • Durham A.L.
      • Adcock I.M.
      The relationship between COPD and lung cancer.
      ]. Patients with lung cancer are usually treated with a combination of surgery, radiotherapy, chemotherapy, or immunotherapy which also puts them at greater risk [
      • Verma R.
      • Kilgour H.M.
      • Haase K.R.
      The psychosocial impact of COVID-19 on older adults with cancer: a rapid review.
      ]. In March 2020, COVID-19 was declared a pandemic by the World Health Organisation [
      • Cucinotta D.
      Vanelli M. WHO Declares COVID-19 a Pandemic.
      ]. Many countries including the United Kingdom (UK) went into ‘lockdown’ where people were only allowed to leave their homes for very limited reasons and vulnerable patients were advised to ‘shield’ which meant their daily lives were even more restricted []. These restrictions had a huge impact on the lives of individuals. Recent research has suggested that COVID-19 caused psycho-social issues for many individuals, particularly older adults who often had underlying health conditions [
      • Verma R.
      • Kilgour H.M.
      • Haase K.R.
      The psychosocial impact of COVID-19 on older adults with cancer: a rapid review.
      ] [
      • Dubey S.
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      • Ghosh R.
      • Chatterjee S.
      • Dubey M.J.
      • Chatterjee S.
      • et al.
      Psychosocial impact of COVID-19.
      ]. A study of older people with cancer reported that the majority of participants had been affected by the pandemic in terms of increased physical isolation and a change in routine. Twenty-seven percent also reported some level of loneliness [
      • Clifton K.
      • Gao F.
      • Jabbari J.
      • Van Aman M.
      • Dulle P.
      • Hanson J.
      • et al.
      Loneliness, social isolation, and social support in older adults with active cancer during the COVID-19 pandemic.
      ].
      In addition to the impact on individuals, healthcare systems, and in particular cancer services, were severely disrupted during the pandemic [
      • Richards M.
      • Anderson M.
      • Carter P.
      • Ebert B.L.
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      The impact of the COVID-19 pandemic on cancer care.
      ,
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      • Hall G.
      • Denaxas S.
      • Chang W.H.
      • et al.
      Estimated impact of the COVID-19 pandemic on cancer services and excess 1-year mortality in people with cancer and multimorbidity: near real-time data on cancer care, cancer deaths and a population-based cohort study.
      ]. There is evidence to suggest that the pandemic caused delays in cancer diagnosis and treatment, changes to treatment [
      • Moraliyage H.
      • De Silva D.
      • Ranasinghe W.
      • Adikari A.
      • Alahakoon D.
      • Prasad R.
      • et al.
      Cancer in Lockdown: Impact of the COVID-19 Pandemic on Patients with Cancer.
      ,
      • Frey M.K.
      • Ellis A.E.
      • Zeligs K.
      • Chapman-Davis E.
      • Thomas C.
      • Christos P.J.
      • et al.
      Impact of the coronavirus disease 2019 pandemic on the quality of life for women with ovarian cancer.
      ], and more limited access to support services [
      • Zomerdijk N.
      • Jongenelis M.
      • Yuen E.
      • Turner J.
      • Huntley K.
      • Smith A.
      • et al.
      Experiences and needs of people with haematological cancers during the COVID-19 pandemic: A qualitative study.
      ]. There was also a rapid shift to remote appointments in order to limit attendance at cancer centres [
      RCR Advice on Non-urgent and Cancer Imaging During the Coronavirus Pandemic | The Royal College of Radiologists [Internet].
      ,]. These sudden changes to clinical practice and service delivery may have further exacerbated the negative effects that patients with cancer may have experienced. Chen et al. [
      • Chen M.
      • Mohd Said N.
      • Mohd Rais N.C.
      • Ho F.
      • Ling N.
      • Chun M.
      • et al.
      Remaining agile in the COVID-19 pandemic healthcare landscape – how we adopted a hybrid telemedicine geriatric oncology care model in an academic tertiary cancer center.
      ] described how they had adapted their geriatric cancer care model to overcome barriers during the pandemic. The team adopted a hybrid telemedicine model to minimise site visits and face-to-face contact; earlier telephone engagement and assessment showed an improvement in the quality of life for patients [
      • Chen M.
      • Mohd Said N.
      • Mohd Rais N.C.
      • Ho F.
      • Ling N.
      • Chun M.
      • et al.
      Remaining agile in the COVID-19 pandemic healthcare landscape – how we adopted a hybrid telemedicine geriatric oncology care model in an academic tertiary cancer center.
      ]. Other studies have also recognised the importance of the comprehensive geriatric assessment in cancer care during the pandemic and beyond [
      • Tantirige N.N.
      • Yoganayagam N.
      • Ilyas G.
      • Wang Y.
      • Harari D.
      • Kalsi T.
      Impact of COVID-19 on geriatric oncology services in a single Centre in the UK: effect on service delivery and clinical characteristics of older patients with cancer seen via pre- and post- retrospective service evaluation.
      ]. A study of older survivors of cancer reported that changes to clinical practice were problematic for this patient population and suggested four key recommendations for future care: enhancing baseline information, facilitating caregiver support and engagement, greater technology integration, sustained use, and public appreciation of PPE [
      • Haase K.R.
      • Kain D.
      • Merchant S.
      • Booth C.
      • Koven R.
      • Brundage M.
      • et al.
      Older survivors of cancer in the COVID-19 pandemic: reflections and recommendations for future care.
      ]. Other studies of older adults have also made recommendations for the future such as peer-to-peer contact, online mental health interventions, [
      • Bartels M.M.T.J.
      • Gal R.
      • van der Velden J.M.
      • Verhoeff J.J.C.
      • Verlaan J.J.
      • Verkooijen H.M.
      Impact of the COVID-19 pandemic on quality of life and emotional wellbeing in patients with bone metastases treated with radiotherapy: a prospective cohort study.
      ] and the importance of developing the non-geriatric workforce in delivering better geriatric oncology care [
      • Tantirige N.N.
      • Yoganayagam N.
      • Ilyas G.
      • Wang Y.
      • Harari D.
      • Kalsi T.
      Impact of COVID-19 on geriatric oncology services in a single Centre in the UK: effect on service delivery and clinical characteristics of older patients with cancer seen via pre- and post- retrospective service evaluation.
      ].
      The aims of this research study were to understand how the COVID-19 pandemic impacted the experiences of people with lung cancer regarding the delivery of cancer care to plan for post-pandemic, and how these changes and the restrictions faced during the pandemic impacted patients' functional status (physical and psycho-social), exploring, in particular, the role of age and frailty status.

      2. Materials & Methods

      2.1 Study Design

      This is an observational cross-sectional study that recruited a random sample of people with lung cancer under the care of a specialist cancer centre in the North West of England throughout the COVID-19 pandemic. The purpose of the study was to investigate the experience of participants with the delivery of care to plan for post-pandemic. The study also sought to understand how pandemic changes and restrictions impacted participants' functional status, exploring, in particular, the role of age and frailty status. This included people diagnosed with any lung cancer histological sub-type, any cancer stage, and at any point in their cancer management pathway between diagnosis and discharge or end of life.
      This study was performed in line with the principles of the Declaration of Helsinki and approval was granted by London Surrey Borders Research Ethics Committee (20/LO/1014). Written informed consent was obtained from all individual participants included in the study. Moreover, the development of the study questionnaire included patient involvement to ensure the questions were appropriate and easy to understand.

      2.2 Study Procedures

      The randomly selected patients were recruited at two different time points throughout the COVID-19 pandemic. The first wave was recruited between October and December 2020 and the second wave in February 2021.
      For the random selection of people with lung cancer in the first wave, a list was initially generated (using the electronic health records) with all the patients seen at the cancer centre between January and March 2020. IBM SPSS® Statistics v.21 was then used to make a simple random selection of patients. For the random selection in the second wave, a list was generated including only new patients under the care of the cancer centre since March 2020. No patient characteristics were used to stratify the random selection process. To ensure that only appropriate patients actively under the care of the cancer centre were selected, those who were transferred, on end-of-life care, on best supportive care, or deceased, were excluded.
      The randomly selected patients from each wave were contacted by letter with an invitation to participate in the study, along with a copy of the paper questionnaire, a consent form for signature, and a paid return envelope. Patients who returned the completed questionnaire to the research team without the signed consent form or an invalid consent form (not legible or signed) were deemed ineligible for the study and were excluded. The research team transcribed all the answers to a spreadsheet and complemented the information provided in the questionnaires with clinical data extracted from the electronic health record for subsequent analysis.

      2.3 Data Analysis

      For the sample size calculation, a sample of at least 250 completed questionnaires was deemed appropriate by the research team. Therefore, anticipating a participation/completion rate in the region of 30%, the researchers concluded that a random selection of about 900 patients with lung cancer should be invited to participate.
      The questionnaire consisted of 62 individual questions with one section focusing on the patient's experience with the changes in the delivery of care during the pandemic. Another section focused on how the pandemic impacted their functional status (physical, social, and psychological). Finally, the questionnaire also included several validated tools for self-assessment in order to better characterise the participants. Most questions were developed by the research team and were reviewed by a volunteer patient group to ensure these were clear and appropriate before undergoing ethical review. The researchers also added a sub-questionnaire with seven questions commonly used in the National Health Service for patients to self-assess the quality of the communication with clinical teams regarding their care. The answers to these seven questions (from “very poor” to “very good”) were converted into a score from 0 to 100%. To infer their quality of life, patients were asked to rate their health from 0 to 100 (which was based on the EQ-5D instrument). Several validated tools were added for patients to self-assess their anxiety, depression, and frailty. The validated Hospital Anxiety and Depression Scale (HADS) consists of seven screening questions for each component (anxiety and depression), with a normal result if the final score (for each component) is 0–7, a borderline abnormal score if 8–10, and an abnormal score if 11–21. The self-assessment version of the Geriatric-8 (G8) tool was used for those patients aged 70 years and above; it consists of eight questions with an abnormal result if a score is 14 or lower (0–17).
      All the eligible patients' questionnaires (with consent form signed and legible) were included for analysis and any missing data were recorded as missing and no data imputation was performed. These data were complemented by clinical data from the electronic patient records which allowed the team to contextualise the participants in terms of their patient and cancer characteristics at the time of study participation.
      Apart from descriptive data analysis, the researchers also planned inferential statistical analysis to explore the role of age and frailty status within the main study aims. Age was assessed as both a categorical variable (cut-off at 70 years) and as a continuous variable. Assessment of the differences between groups for categorical variables was assessed using Chi-squared or Fisher Exact tests for analysis containing groups with low values, or MannWhitney-U or Kruskal-Wallis tests were used for difference between two or more groups of continuous variables. Spearman's correlation coefficient was used to assess the correlation of continuous variables. Analysis was performed using the package SciPy in Python. Lastly, a p-value below 0.05 was deemed statistically significant.

      3. Results

      3.1 Study Sample Characterisation

      The study questionnaires were posted out to 883 patients, with 682 (77%) sent in the first wave and 201 (23%) in the second wave. Three hundred five questionnaires were completed and returned (78% from the first wave and 22% from the second wave), resulting in a 35% study participation rate. A total of 282 participants (Table 1) were eligible for analysis, with 23 excluded for not completing the consent form or this not being legible.
      Table 1Baseline patient and cancer characteristics (n = 282).
      Age
       Median, years (min-max)71 (31–89)
       Older sub-group (70+), n (%)151 (54)
      Sex
       Male, n (%)143 (51)
       Female, n (%)139 (49)
      Cancer type
       NSCLC, n (%)241 (86)
       SCLC, n (%)39 (14)
       Thymoma, n (%)2 (<1)
      Cancer stage
       Stage I-IIIa, n (%)145 (51)
       Stage IIIb-IV, n (%)137 (49)
      Cancer management status
       On surveillance/follow-up, n (%)176 (62)
       On active treatment, n (%)106 (38)
      Cancer diagnostic investigations timing
       Pre-pandemic, n (%)208 (74)
       During pandemic period, n (%)74 (26)
      NSCLC, non-small cell lung cancer; SCLC, small cell lung cancer.
      A total of 220/282 patients (78%) reported being able to fully comply with the pandemic-related shielding recommendations, whilst 56/282 (20%) were only able to comply partially. Neither age nor frailty impacted the ability to comply with shielding. In this context, 37/282 of all surveyed patients (13%) reported having had a COVID-19 infection before completing the questionnaire (confirmed by a test or deemed very likely by the participant).
      A total of 280/282 patients (99%) completed the 14 self-assessment questions to identify signs suggestive of anxiety or depression (the HADS questionnaire), with abnormal or borderline levels found in 104/282 (37%) and 94/282 (33%) of them, respectively. Twenty-six patients (9%) had abnormal levels of both anxiety and depression. There was a significant correlation between anxiety and depression, hence patients with abnormal levels of depression had a relative risk 6.5 times higher of also having abnormal levels of anxiety vs normal to borderline levels (95% confidence interval [CI] 3.9–10.5; p < 0.001). Significantly higher levels of anxiety were found in the sub-group of younger patients aged 31 to 69 years (p = 0.036) with abnormal levels in 22% of these vs 12% in the older counterparts aged 70 years and above. Regarding depression, higher levels were also identified in the younger sub-group (p = 0.058), with abnormal levels in 21% of these vs 13% in the older sub-group. This difference was clearer when analysing age as a continuous variable (p = 0.021), suggesting a difference in age outside the two sub-groups. There were no differences in the levels of anxiety and depression per sex, cancer type, stage, cancer management status (active treatment vs follow-up), or the time point within the pandemic period (wave 1 vs 2).
      A total of 148/151 patients in the older sub-group (70 years and above) completed the frailty self-assessment tool (G8 screening tool), with 109/151 (74%) self-assessed as having frailty. The incidence of anxiety in older patients was significantly higher in those with frailty (17% vs 0%; p < 0.001), with similar results for depression (19% vs 0%; p < 0.001).
      Regarding overall health, a total of 273 patients (97%) rated this for the day they completed the questionnaire on a scale from 0 to 100. The average was 67 points and whilst there were no differences according to age, those with frailty reported significantly lower levels (p < 0.001).

      3.2 Impact of the Pandemic on the Delivery of Cancer Care

      Reflecting on their cancer pathway, 48 of all 282 surveyed patients (17%) believed that the pandemic had a negative impact on their cancer treatment. In a similar proportion, 13 patients amongst those who were diagnosed during the pandemic period (18%) believed the pandemic delayed their cancer diagnosis.
      Regarding the quality of communication with the cancer centre during the pandemic, a total of 260/282 patients (92%) completed all seven questions assessment (Fig. 1) and were considered for analysis. Of these, 247 (95%) reported good communication with the oncology team during this period (answers “very good” and “good” in the overall score). There were no differences with the experienced communication according to age or frailty.
      Fig. 1
      Fig. 1Quality of the communication with the cancer centre during the pandemic (the overall score was calculated using the average answers across all seven questions).
      Patients were then asked if they felt supported by their different support systems during the pandemic. Patients reported feeling appropriately supported (answers “strongly agree” and “agree”) by their cancer centre, their friends and family, and their primary health care services in 88%, 86%, and 59% of cases, respectively. Both older and younger patients felt similarly well-supported and there was no difference for those with frailty. Those on active anti-cancer treatment felt significantly more well-supported by the cancer centre than those on follow-up (p = 0.0037).
      Patients were asked about their experiences with outpatient care during the pandemic at the cancer centre. A total of 253/282 patients (90%) reported having had at least one of their standard face-to-face hospital appointments replaced by a phone consultation. Nine patients (3%) felt the phone consultations did not meet their expectations, of which eight had abnormal levels of anxiety and/or depression and five were also older with frailty. When asked if not being able to have a friend or relative with them during their appointments had been a problem for them, this was significantly more problematic during face-to-face compared to telephone appointments (24% vs 10%, p < 0.001). Younger patients were more likely to report this being a problem for them compared to older patients during both face-to-face (p = 0.024) and telephone appointments (p = 0.038) when treating age as continuous. Older patients with frailty were also more likely to report this as a problem, yet this was more clear during telephone appointments (p = 0.032) than during face-to-face appointments (p = 0.087).
      The final section of the questionnaire asked patients about their preferences regarding post-pandemic outpatient care at the cancer centre in terms of face-to-face or remote (telephone and/or video) consultations. Whilst 93% of patients preferred to have a face-to-face first appointment, this preference for face-to-face dropped to 64% when discussing imaging results and to 60% for the reviews during anti-cancer treatments. Whilst patients of any age similarly preferred the first appointment to be face-to-face, older patients were more significantly in favour of face-to-face, compared to younger patients, for the majority of their consultations (p = 0.007), during on-treatment reviews (p = 0.008), and to discuss imaging results (p = 0.013) when treating age as continuous. Amongst the older group of patients, there were no differences in terms of preferences between those who were fit and those with frailty. Lastly, when considering changes in preferences over time, the majority of participants in the second wave of the study no longer preferred face-to-face consultations during anti-cancer treatment review (p = 0.0278), compared to those on the first study wave earlier in the pandemic (Fig. 2).
      Fig. 2
      Fig. 2Patient's preference for face-to-face outpatient appointments in the cancer centre for the post-pandemic period according to their timing of study participation.

      3.3 Impact of the Pandemic on the Physical, Social, and Psychological Needs

      Respondents were asked if, as a person with lung cancer, they believed the COVID-19 pandemic had a substantial impact on the different aspects of their daily lives (Fig. 3). All patients answered at least some questions in this section, with a rate of missing data of 1.2%. Overall, 54% of patients reported a considerable negative impact from the pandemic (answers “strongly agree” and “agree” in the overall score). The most impacted aspects, reported by over 60% of patients, were their social lives, relationships with family and friends, and independence in their daily life activities.
      Fig. 3
      Fig. 3Negative impact of COVID-19 pandemic in different aspects of patients' daily life (the overall score was calculated using the average answers across all seven questions).
      A greater proportion of younger patients reported that the pandemic impacted their financial situation (p < 0.001), compared to older patients. There was a trend for the negative impact on emotional and psychological health in the younger sub-group (p = 0.071), which was clearer when analysing the role of age as a continuous variable (p = 0.01). The negative impact on the sleep pattern also identified a potential trend in younger patients when analysing the patients' age as a continuous variable (p = 0.059). Similarly, those older patients with frailty reported a more negative impact on their emotional and psychological health (p = 0.001) and on their sleep pattern (p = 0.002) than those who self-assessed as fit. There were no significant differences according to cancer type, stage, cancer management status (active treatment vs on follow-up), or the time point within the pandemic period.

      4. Discussion

      This survey study had a participation rate of 35%, which was slightly lower than other studies using postal questionnaires during the COVID-19 pandemic [
      • Jones M.T.
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      ]. This was potentially due to people with lung cancer being overall more vulnerable, thus finding it potentially harder to participate using this methodology. Regarding the study sample, this seems representative of the population in terms of age, tumour stage, and cancer management status. The average score for overall health was 67 (out of 100) which indicates that both patients who were feeling well and less well were included. However, the incidence of frailty amongst older adults aged 70 years and above was higher than expected with a rate of 74%, whilst the median incidence of frailty in patients with cancer is estimated in the region of 42% [
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      ]. This study included only people with lung cancer and used patient self-assessment instead of clinician-reported, which may partially explain the higher rate. Additionally, there may have been a selection bias in which patients with more problems may have felt more compelled to respond to the survey.
      Regarding the overall experience with the delivery of care, patients reported very good communication and felt appropriately supported at the cancer centre. Although communication was rated highly by participants, the lowest scores were around shared decision-making. Other research has suggested that decision-making for people with cancer was particularly difficult during the pandemic as participants needed to consider the added risk of contracting COVID-19 when thinking about their treatment options [
      • Haier J.
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      ]. Haier et al. [
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      ] reported that decisional conflicts were more profound in patients with higher levels of anxiety and depression, highlighting the need for a different approach for this patient group.
      Whilst the majority of patients felt telephone consultations for their outpatient cancer care met their expectations, it seemed (despite the small numbers) that those who were more disappointed were, in general, patients with potentially more complex needs and a combination of abnormal levels of anxiety, depression, and frailty. Younger patients reported not having someone with them at appointments as more problematic. This may be because of their higher levels of anxiety and depression. Other studies have reported mixed views from patients and health professionals on the ease of including caregivers in telephone consultations [
      • White V.
      • Bastable A.
      • Solo I.
      • Sherwell S.
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      ,
      • Turner K.
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      • Gonzalez B.D.
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      ]. Older patients generally reported a preference for face-to-face consultations, but frailty was not an influencing factor. A study of rheumatology patients also found that with increasing age, patients were less satisfied with remote consultations [
      • Jones M.T.
      • Arif R.
      • Rai A.
      Patient experiences with telemedicine in a National Health Service Rheumatology Outpatient Department during Coronavirus Disease-19.
      ]. There is some evidence to suggest that the level of care for older people has been reduced with the increased use of remote consultations [
      • Benzeval M.
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      • Burton J.
      • Crossley T.F.
      • Fumagalli L.
      • Jäckle A.
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      ,
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      ]. Participants expressed a preference for first appointments to be delivered face-to-face, which was echoed in another study of gynaecological cancer patients where the first appointment was important to build trust [
      • Christiansen M.G.
      • Pappot H.
      • Pedersen C.
      • Jarden M.
      • Mirza M.R.
      • Piil K.
      Patient perspectives and experiences of the rapid implementation of digital consultations during COVID-19 - a qualitative study among women with gynecological cancer.
      ]. There was a noticeable change in preferences in this study over time, with a higher number of patients on the second wave preferring telephone consultations. This finding suggests that the care and support delivered remotely may have improved as clinical and admin teams became more proficient in this method of communication and assessment. But it may also be that the patients became more used to and confident in virtual visits. All these findings suggest that moving to a post-COVID era, a more personalised and patient-centred outpatient clinical pathway is needed. In fact, the results from this study are being used at this cancer centre to improve clinical pathways in the post-COVID era.
      Participants reported feeling much less supported by their primary care providers, a finding echoed in other studies [
      • Kamposioras K.
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      ]. A focus on COVID-19 issues meant patients with existing health conditions were often neglected as workload pressures on primary care caused increased waiting times and delays [
      • Lim J.
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      ]. Qualitative studies report varying experiences and suggest there may be differences in interaction with primary care based on key demographic criteria, such as socioeconomic status, where patients from a higher socioeconomic status were more likely to seek help [
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      • et al.
      Socioeconomic differences in help seeking for colorectal cancer symptoms during COVID-19: a UK-wide qualitative interview study.
      ], and age, where patients aged 30–64 age were more likely to engage with virtual care than older groups [
      • Ramona DeJesus P.
      • Chavez A.
      • Erickson R.
      Patients’ experience with virtual care during COVID-19 pandemic in primary care practice.
      ].
      Regarding these patients' experiences during the pandemic, most patients reported a negative impact from the pandemic, in particular regarding their social lives, relationships with family and friends, and independence with their daily life activities. Anxiety and depression were prevalent, with 37% and 33% of participants having borderline or abnormal levels, respectively. Other studies in the context of COVID-19 reported high levels of anxiety and depression in 10–42% and 24–59% of participants, respectively [
      • Bafunno D.
      • Romito F.
      • Lagattolla F.
      • Delvino V.A.
      • Minoia C.
      • Loseto G.
      • et al.
      Psychological well-being in cancer outpatients during COVID-19.
      ,
      • Turgeman I.
      • Goshen-Lago T.
      • Waldhorn I.
      • Karov K.
      • Groisman L.
      • Reiner Benaim A.
      • et al.
      Psychosocial perspectives among cancer patients during the coronavirus disease 2019 (COVID-19) crisis: An observational longitudinal study.
      ,
      • Toquero P.
      • Blanco Fernández C.
      • López Martí M.P.
      • Hernández Marín B.
      • Vera Cea E.B.
      • Garrido García A.
      • et al.
      Emotional distress in cancer patients during the first wave of the COVID-19 pandemic.
      ]. Importantly, as we do not have pre-pandemic data for comparison, it is unclear to what extent these levels of anxiety and depression reflected primarily the impact of the pandemic or the impact of a cancer diagnosis. Vicinanza et al. [
      • Vicinanza F.
      • Ippolito E.
      • Sisto A.
      • Santo B.
      • Fiore M.
      • Trodella L.E.
      • et al.
      The psychological impact of the covid-19 pandemic on radiotherapy cancer patients.
      ] reported that people with lung cancer were more concerned regarding COVID-19 compared to patients with other cancer diagnoses, and Bafunno et al. [
      • Bafunno D.
      • Romito F.
      • Lagattolla F.
      • Delvino V.A.
      • Minoia C.
      • Loseto G.
      • et al.
      Psychological well-being in cancer outpatients during COVID-19.
      ] reported people with lung cancer as more likely to experience psychological issues compared to breast and lymphoma patients. These differences may be due to the poorer prognosis of lung cancer, its treatment regimens, and the concern that they may be more severely impacted by COVID-19 due to it being a respiratory disease [
      • Bafunno D.
      • Romito F.
      • Lagattolla F.
      • Delvino V.A.
      • Minoia C.
      • Loseto G.
      • et al.
      Psychological well-being in cancer outpatients during COVID-19.
      ].
      Lastly, this study found that anxiety and depression rates were higher in younger people aged 31–69 years than older people aged 70 years and above; younger people also reported a greater impact on their emotional and psychological health. This is different from the findings of other research during COVID-19, which have suggested older patients were likely to experience higher rates of anxiety and depression [
      • Bafunno D.
      • Romito F.
      • Lagattolla F.
      • Delvino V.A.
      • Minoia C.
      • Loseto G.
      • et al.
      Psychological well-being in cancer outpatients during COVID-19.
      ], whilst others found that age did not play a role [
      • Turgeman I.
      • Goshen-Lago T.
      • Waldhorn I.
      • Karov K.
      • Groisman L.
      • Reiner Benaim A.
      • et al.
      Psychosocial perspectives among cancer patients during the coronavirus disease 2019 (COVID-19) crisis: An observational longitudinal study.
      ,
      • Lavdaniti M.
      • Patrikou K.
      • Prapa P.-M.
      • Vastardi M.
      • Fradelos E.C.
      • Papathanasiou I.V.
      • et al.
      A cross-sectional study for assessing perceived symptoms, depression and quality of life in advanced lung cancer patients.
      ]. One may argue that perhaps younger patients who were struggling the most were more compelled to participate in the study. Additionally, younger patients could have had a more active and sociable lifestyle before the pandemic and, therefore, struggled the most to cope with the management of lung cancer during the pandemic. But since this study did not request any pre-pandemic data, this is unclear. Interestingly, when looking at the possible role of frailty amongst the older cohort, those self-assessed as frail reported higher levels of anxiety and depression. Therefore, older patients with lung cancer who were fit seem to have coped better during the pandemic, compared to those with frailty or younger patients. In line with this finding, those with more psychological problems also reported more sleep disturbances. Other research has found that older patients with higher levels of social support experience lower levels of anxiety and depression [
      • Chambers A.
      • Damone E.
      • Chen Y.T.
      • Nyrop K.
      • Deal A.
      • Muss H.
      • et al.
      Social support and outcomes in older adults with lung cancer.
      ]. Another relevant finding was that younger patients were more severely impacted financially during the pandemic, as they are more likely to be working and have dependants, which is in line with the published literature [
      • Sharp L.
      • Timmons A.
      The Financial Impact of a Cancer Diagnosis Item Type Report.
      ].

      4.1 Limitations

      Participants in this study were selected from a single cancer centre therefore their experiences may not be generalisable to other geographical areas. Participants were self-selected which may have caused bias in the types of people who have chosen to respond. For example, if people had not experienced any problems, they may not have felt they had anything to report and therefore decided not to participate. There may also be bias in the way participants reported on their experiences of communication at the cancer centre. Participants may have been more positive as the study was run by the cancer centre. We do not have any data on the functional status of participants pre-COVID-19, therefore we are unable to determine if the functional impacts have increased during the pandemic.

      5. Conclusion

      There is a need for more personalised outpatient consultation options during cancer care. Whilst there is a preference towards face-to-face oncology consultations for older patients, following the pandemic there is a growing acceptance of remote consultations, particularly during anti-cancer treatment. Older patients with lung cancer without frailty were less affected in terms of their functional status by the pandemic than those with frailty and younger patients, requiring less support from healthcare services. The results of this study are being used to guide how clinical pathways can be improved post-pandemic.

      Ethics approval and consent to participate

      This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by London Surrey Borders Research Ethics Committee (20/LO/1014). Written informed consent was obtained from all individual participants included in the study.

      Consent for publication

      All patients provided written consent for publication as part of their consent to participate in the study.

      Availability of data and materials

      The study questionnaire is available on. The study raw data is not publicly available.

      Funding

      This work was funded by The Christie Charitable funds in the United Kingdom.

      Author contributions

      Fabio Gomes, Sally Taylor and Janelle Yorke contributed to the study design. Material preparation and data collection were performed by Jake Coombermoore, Charlotte Eastwood, Melissa Stanworth and Claire Barnes. Data analysis was performed by Fabio Gomes, Lauren Scanlon and Andrew Williamson. The first draft of the manuscript was written by Fabio Gomes and Sally Taylor. All authors reviewed and approved the final manuscript.

      Declaration of Competing Interest

      The authors have no relevant financial or non-financial interests to disclose.

      Acknowledgements

      The co-authors would like to acknowledge The Christie Charity which funded this study.

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