key: cord-0692691-6xtl3y10
authors: McKay, Siobhan C; Lembach, Hanns; Hann, Angus; Okoth, Kelvin; Anderton, Joy; Nirantharakumar, Krishnarajah; Magill, Laura; Torlinska, Barbara; Armstrong, Matthew; Mascaro, Jorge; Inston, Nicholas; Pinkney, Thomas; Ranasinghe, Aaron; Borrows, Richard; Ferguson, James; Isaac, John; Calvert, Melanie; Perera, Thamara; Hartog, Hermien
title: Health‐related quality of life, uncertainty and coping strategies in solid organ transplant recipients during shielding for the COVID‐19 pandemic.
date: 2021-08-11
journal: Transpl Int
DOI: 10.1111/tri.14010
sha: 41160cdaa07ccc37783cc97c6d876ffa5f8938e5
doc_id: 692691
cord_uid: 6xtl3y10

Strict isolation of vulnerable individuals has been a strategy implemented by authorities to protect people from COVID‐19. Our objective was to investigate health‐related quality of life (HRQoL), uncertainty and coping behaviours in solid organ transplant (SOT) recipients during the COVID‐19 pandemic. A cross‐sectional survey of adult SOT recipients undergoing follow‐up at our institution was performed. Perceived health status, uncertainty and coping strategies were assessed using the EQ‐5D‐5L, Short‐Form Mishel Uncertainty‐in‐Illness scale (SF‐MUIS) and Brief Cope, respectively. Interactions with COVID‐19 risk perception, access to healthcare, demographic and clinical variables were assessed. The survey was completed by 826 of 3,839 (21.5%) invited participants. Overall, low levels of uncertainty‐in‐illness were reported, and acceptance was the major coping strategy (92%). Coping by acceptance, feeling protected, self‐perceived susceptibility to COVID‐19 were associated with lower levels of uncertainty. Health status index scores were significantly lower for those with mental health illness, compromised access to healthcare, a perceived high risk of severe COVID‐19 infection and higher levels of uncertainty. A history of mental health illness, risk perceptions, restricted healthcare access, uncertainty and coping strategies were associated with poorer HRQoL in SOT recipients during strict isolation. These findings may allow identification of strategies to improve HRQoL in SOT recipients during the pandemic.

Due to the highly contagious nature of COVID-19, governments have implemented various strategies promoting self-isolation and social distancing of the general population to mitigate viral spread [1] [2] [3] . The impact of strictly isolating vulnerable individuals during the pandemic to prevent infection with are unknown at present, however, the well-being of vulnerable individuals may be at risk during long periods of strict isolation [2, 4, 5] .

In March 2020, Public Health England introduced a 'shielding' policy, designed to protect individuals deemed clinically extremely vulnerable, such as oncology patients, individuals with respiratory disease, or patients taking immunosuppressive medications [6] . The 'shielding' guidance advised clinically extremely vulnerable individuals to stay at home at all times between 23rd March and 31 st July 2020 [7] . Additionally, shielded individuals were asked to stay 2 meters away from others as much as possible, even from household members. With the exception of emergencies, they could not physically attend appointments with healthcare providers. Due to the unprecedented nature of the pandemic, these expedient decisions were based on epidemiological principals rather than established evidence.

Evidence from the Middle East respiratory syndrome coronavirus (MERS-CoV) outbreak previously identified immunosuppression as a risk factor for severe infection and death [8] . The early accounts of COVID-19 risk in immunosuppressed solid organ transplant (SOT) patients were conflicting. While a protective effect of immunosuppression against the sequalae of the cytokine storm associated with severe COVID-19 was proposed, others suggested an increased risk of severe COVID-19 [9] [10] [11] [12] . In agreement with the latter, an increased mortality rate following symptomatic COVID-19 has been demonstrated in renal transplant recipients, in comparison to patients with renal disease awaiting transplant [13] . However, a multicentre study demonstrated that the severity of illness with COVID-19 in SOT recipients was related to age and other comorbidities [14] . In addition to the great deal of uncertainty concerning risk of infection and severity of illness, these individuals may also experience anxiety regarding their specific healthcare needs not being met due to restricted access to healthcare during shielding. Increased anxiety has been demonstrated in other patient populations that were also required to undergo shielding [15, 16] . In addition, Smith et al demonstrated worsening mental health in patients with asthma undergoing shielding during the pandemic, and individuals with a history of anxiety or depression were more vulnerable [17] . Our study was designed in response to rapidly defined Public Health research priorities for people experiencing severe distress during the COVID-19 pandemic [18, 19] .

This article is protected by copyright. All rights reserved We hypothesised that SOT recipients would have a higher level of self-perceived risk for severe COVID- 19 , leading to greater levels of uncertainty in illness and worse health-related quality of life (HRQoL). In addition, we hypothesised that social isolation from shielding would lead to higher levels of anxiety and depression, and consequently poorer HRQoL. Our aim was to investigate health-related quality of life (HRQoL), uncertainty and coping behaviours in solid organ transplant (SOT) recipients during the COVID- 19 pandemic, and identify deleterious and advantageous coping strategies used in this population. This will enable identification of at-risk groups for potential harm during shielding for this or future pandemics, allowing targeted interventions to support these individuals.

A cross-sectional survey of all SOT recipients being managed at a tertiary level transplant centre in the Midlands region of the UK, servicing a population of 10 235 000 people. Patient-reported outcomes (PROs) were the primary outcome of interest. To optimise the quality of reporting, the SPIRIT-PRO Extension guidelines were adhered to and reported where possible [20] . The study protocol was approved by the Human Research Ethics Committee (20/HRA/2613) and data acquisition approved by our institution (CARMS-16123).

All adult (≥18 years) liver, renal, heart, and lung transplant recipients identified through departmental electronic databases, that were alive and undergoing follow-up at our transplant centre in June 2020 were eligible for this study. A sample size calculation was not performed as the entire target population was approached.

All eligible transplant recipients were invited to participate via a postal invitation letter at the beginning of July 2020. The invitation included the participant information sheet (PIS), details of a uniform resource locator and participant-specific login details. This ensured only one online survey could be completed per recipient via the Research Electronic Data Capture (REDCap®) program [21] . A paper-based version of the consent and survey was provided upon request. Only English language versions of the study survey, including PRO tools, were provided and the use of a proxy to complete or translate the survey was permitted. The survey remained open for a 28-day period until the 31st July 2020, which coincided with the last day of the recommended shielding period by Public Health England.

Demographic, transplant and health characteristics, were self-reported by patients. COVID-19 infection was defined as reporting a positive COVID RT-PCR test, and suspected COVID-19 infection (in absence of a negative or positive test) as a self-reported illness with the presence of two or more of the following COVID-19 key symptoms; temperature, persistent cough, and anosmia. Self-reported illness consistent with COVID-19 was included in our case definition due to lack of routine testing of individuals with mild symptoms.

Both non-white ethnicity and a lower socioeconomic status have been extensively reported in the scientific literature and media as being associated with poorer COVID-19 outcomes, therefore this group may have

This article is protected by copyright. All rights reserved additional levels of concern or uncertainty [22, 23] . Data was collected on participants self-reported ethnicity and the Index of Multiple Deprivation (IMD) was used to assess socioeconomic status. The IMD quintile values, a measure of relative deprivation at small local area level, were calculated from each recipient's residential postcode using the English Indices of Deprivation 2019 [24] .

A single measurement with relevant PROs was performed with reference to the period of shielding (March-July 2020). The primary outcome measure was health-related quality of life (HRQoL) using the EQ-5D-5L questionnaire [25] . Secondary outcomes comprised levels of uncertainty and coping strategies, measured with the Short Form Mishel Uncertainty in Illness scale (SF-MUIS) and Brief COPE questionnaire [26] [27]. These tools were chosen to minimise the participant response burden.

EQ-5D-5L is a standardised, non-disease-specific measure of self-perceived health status widely used around the world in clinical research and population health studies, and real-world clinical settings, being recommended by several health technology assessment bodies internationally [28] . It incorporates 5 domains (mobility, self-care, usual activities, pain and discomfort, and anxiety and depression), further including an assessment of overall health using a visual analogue scale (VAS; best imaginable health is 100, and worst imaginable health is 0). The EQ-5D-5L version (using 5 levels of response; e.g. not, slightly, moderately, severely, or extremely) is more sensitive and suffers less ceiling effect than the original 3-level instrument (EQ-5D-3L) [29] . It has been validated in multiple populations across geographical and disease areas [30] . The EQ-5D-5L instrument was used according to the published instructions [31] . The five domain scores were used to calculate the health state index scores, ranging from less than 0 (where 0 is the value of a health state equivalent to dead; negative values representing values as worse than dead) to 1 (the value of full health), which were used in the analysis.

The SF-MUIS comprises 5 questions and assesses 4 components of uncertainty: ambiguity, complexity, inconsistency and unpredictability. This derives a score (range 5-25) with higher levels corresponding to increased levels of uncertainty-in-illness. In a validation study conducted in the Norwegian breast cancer population, the ordinal coefficient alpha for the SF-MUIS was 0.70, which is considered reasonably consistent. The correlation coefficient was 0.98, supporting excellent reliability of the scale.

The Brief COPE evaluates 14 coping strategies (Table 4 ) by answering 28 items on a 4-point Likert scale

(1 = "I haven't been doing this at all" to 4 = "I've been doing this a lot"). In the original validation study [27] , the Cronbach's alpha coefficient of each scale ranged from (0.50 to 0.90), showing acceptable to extremely good reliability [31] . The instrument was used according to the instructions available from the author [32] .

This article is protected by copyright. All rights reserved Participants self-reported COVID-19 infection status, shielding behaviour, risk perceptions and public trust were assessed using items from the World Health Organisations (WHO) standard protocol: COVID-19

Snapshot MOnitoring (COSMO Standard), using both Likert and VAS scales [33] . Items regarding the protective behaviour of shielding and public trust were modified to represent the UK-specific recommendations and healthcare system, as recommended. Access to and perceptions of primary, secondary, and tertiary healthcare services were assessed. Participants' concerns were investigated by allowing selection from a standard list of concerns derived from a general population survey on the mental health impact of the COVID-19 pandemic [18] .

EQ-5D-5L domains and index scores were compared with the general population in England using the Health Survey for England 2017 (HSE), which comprised a multi-stage, stratified, random probability sample of 7 997 adults respondents. Disease-specific comparison was achieved with four post-transplant cohorts, after crosswalk from EQ-5D-5L to EQ-5D-3L according to NICE guidelines [34] [35] [36] [37] . These four cohorts consisted of patients that were in the early or late post-operative period following either renal or liver transplantation and were compared to subgroups of the study population accordingly [34, 35, 38, 39] .

The rate of self-reported COVID-19 positive cases were compared to national registry data on SOT 

Analyses were performed using STATA/SE v16•1 (College Station, Tx: StataCorp LLC). Explanatory variables for primary and secondary outcomes, such as demographics, transplantation and immunosuppression details, shielding behaviours, perceptions of COVID-19 risk, self-reported COVID-19 infection status, and access to healthcare, were pre-specified.

The relationship between EQ-5D-5L index score (primary outcome) and explanatory variables was assessed using a backward stepwise selection process with an alpha-to-remove of ≥0.1 as criteria for inclusion in a multivariable linear regression model. Age, sex, ethnicity, IMD and BMI were forced into the model. A similar backward stepwise linear regression model was built for SF-MUIS uncertainty scale.

A two-sample t-test or Chi-square test was performed, as appropriate, to assess for statistically significant differences between comparison population datasets, and for differences in age, gender, type of organ transplanted, time since transplantation, ethnicity, first language, and IMD between survey responders and non-responders.

Patient and public involvement was first initiated during the design stage of the study, through consultation and pilot testing. Feedback and opinion on the questionnaire design, methods of administration, and time required to participate were obtained.

826 of the 3 839 (21•5%) SOT recipients invited to participate completed the entire survey and were included in the analysis (Figure 1 ). The median age of responders was 60 years, and 57% (470/826) were male (Table 1) . Time since transplant was more than five years in 61%, and 72% had undergone a liver transplant. 28% reported ≥2 co-morbidities (including renal dialysis, cardiac, respiratory, diabetes, hypertension), 20% had a history of a mental health illness, with depression being the most frequent (88/826). Most responders were on two or more immunosuppressive medications (67%). Responders were more likely to be older, had longer duration post-transplantation, be of a white ethnicity, and to have a higher IMD (Supplementary Table 1 ).

The adherence levels to different components of the shielding advice are shown in Table 2 declared adherence with shielding advice, which was significantly lower that the 99% adherence observed at a national level (p < 0•001). Adherence to the recommendation to stay home at all times was significantly better in our cohort.

Eight (1%) responders tested positive for COVID-19, and 16 (2%) declared a combination of 2 or more key symptoms for COVID-19. Twelve patients reported that their symptoms required hospital admission, but no recipients reported admission to the intensive treatment unit (ITU) or need for ventilatory support. A comparison with NHSBT registry data, showed no significant difference between our survey and either the national or regional level transplant registry infection rate in SOT recipients (Supplementary Table 3 ).

The probability of contracting COVID-19 was perceived as extremely likely or somewhat likely in a minority of responders (27%), and a perceived high level of knowledge regarding how to protect themselves from COVID-19 was reported (median Visual analogue scale (VAS) 94/100) (Table 3) .

However, a high perceived susceptibility to COVID-19 infection was reported (median VAS 78/100), and responders believed they would be severely unwell with COVID-19 (median VAS 91/100). 24% of responders reported their access to healthcare had been compromised during shielding, putting them at Accepted Article potential risk. Compared to local healthcare facilities and government, SOT recipients had the greatest confidence in their transplant centre to manage COVID-19 well (median 95/100) ( Table 3) .

Median uncertainty-in-illness during shielding for COVID-19, measured by the SF-MUIS score, was 11 (range 5 -24), and was considered low. The frequency of coping strategies used are shown in Table 4 .

Acceptance was the most frequently used coping strategy (92%, mean 3•25, SD 0.8, on a 4-point Likert scale), followed by active coping, self-distraction and planning. The least reported coping strategies were substance abuse, behavioral disengagement, denial and self-blame. The Cronbach-alpha value for the SF MUIS and Brief COPE responses was 0.66 and 0.77, respectively.

Comparing EQ-5D-5L domains and index scores for shielded SOT recipients to age-matched UK population controls, health was equivalent in the youngest and eldest cohorts (18-24 years, and >75 years), however significantly poorer for SOT recipients in the 35-74 age range for the majority of health domains (Table 5 ). Median EQ-5D-5L index score for age categories were consistently lower in SOT recipients but did not reach statistical significance ( Figure 2 ). The Cronbach-alpha value for the EQ-5D-5L was 0.88.

Comparing overall EQ-5D-3L index scores, perceived health status was worse for SOT recipients during shielding, than for pre-pandemic age-matched general population cohorts. Comparing perceived health status with disease-specific controls, did not reveal consistent results. EQ-5D-3L VAS in liver transplant recipients during shielding were equivalent to pre-pandemic controls in the early post-tranplant period (<2years), but with a trend to worse outcomes than the pre-pandemic group in the late period (>2years after liver transplantation). Conversely, perceived health status (EQ-5D index score) showed a trend towards better EQ-5D VAS scores in a smaller subgroup of renal transplant recipients during shielding compared to a pre-pandemic renal transplant cohort ≥2 years after transplantation ( Figure 3 ) [34] [35] [36] .

Multivariable linear regression model of EQ-5D-5L index scores revealed a significant relationship between several explanatory variables, as shown in Table 6 . A previous history of mental health illness, and being underweight or obese were significantly associated with lower EQ-5D-5L index scores.

Additionally, reporting not knowing whether they had been infected with COVID-19, perception of high likelihood of severe COVID-19 infection, compromised access to health-care, higher levels of uncertainty in illness, and a coping strategy of behavioural disengagement were also associated with lower EQ-5D-5L index scores. Conversely, increasing deprivation index, chronic respiratory comorbidity, a coping strategy of self-distraction and positive reframing, and perceived safe access to their hospital despite not needing to attend were associated with higher EQ-5D-5L index scores.

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Regression analysis revealed an association between increasing uncertainty and compromised access to healthcare, coping strategies of denial, substance abuse, behavioural disengagement and planning (Table 7) . Moderate deprivation, renal transplant recipients, higher EQ-5D-5L index scores, a low perceived risk of contracting COVID-19, public trust and an acceptance coping strategy were associated with lower levels of uncertainty.

This large cross-sectional study of unselected solid organ transplant recipients focused on identifying risk factors for poor health-related quality of life during shielding for the COVID-19 pandemic. A poorer selfperception of health status in shielded SOT recipients was most significantly associated with a previous history of mental health illness, being overweight, reporting compromised access to healthcare and a coping strategy of behavioural disengagement. Increased uncertainty was also associated with poorer health status index scores, compromised access to healthcare, and several coping strategies (denial, substance abuse, behavioural disengagement and planning).

Overall, our study population showed resilience with low levels of uncertainty, the ability to use acceptance, self-distraction and positive reframing as coping strategies and to adhere to protective behaviours.

The main concepts of illness uncertainty, coping strategies and quality of life, have previously been described to be interrelated and incorporated in a theoretical framework. This is the first study to report these in detail in a shielded transplant population during the COVID pandemic ( Figure 4) [43-47].

SOT recipients perceived themselves to be at high risk of contracting COVID-19 and experiencing a severe course of illness. Although, these perceptions may not be inappropriate, accurately quantifying risk, e.g. through methods such as cognitive re-appraisal and pro-active protective health behaviours, can reduce levels of fear and ensure it is proportional to the degree of threat [48] [49] [50] [51] . In accordance, adherence levels to shielding were high and responders generally felt they knew how to protect themselves from COVID very well. This was accompanied by low levels of uncertainty, comparable to previous pre-pandemic transplant cohorts [52] . Previous studies suggest that structure providers, such as credible authorities, can decrease Accepted Article uncertainty directly by promoting interpretation and congruency of events [53] . The overarching public health recommendation of shielding for clinically extremely vulnerable individuals in England may have decreased uncertainty in our study population by promoting a clear interpretation of events. This was evidenced in our study by high levels of public trust, high adherence to shielding and high confidence in the effectiveness of shielding. However, no international comparison cohort of SOT recipients was available to compare uncertainty levels and health status under different public health approaches [19] . Survey respondents expressed the highest level of confidence in the transplant service healthcare professionals to manage issues with COVID-19 well. These findings suggest that transplant units may be optimally positioned to promote interpretation of public health interventions aimed at improving the effectiveness and tolerability of shielding.

Acceptance was a frequent coping strategy in our patient cohort, and is suggested to be beneficial in times of uncertainty and improve psychological flexibility [19] 

This article is protected by copyright. All rights reserved shielded SOT recipients. However, comparisons of subgroups of shielded transplant recipients with pre-pandemic transplant cohorts at equivalent stages post-transplant were difficult to interpret.

Previous studies show poorer HRQoL specifically in the first 6 months post-transplant, while improving and stabilising significantly after this period [34] [35] [36] 66 ]. Our results may suggest these changes in HRQoL are equivocal and mild in a majority, but an ideal comparison group of non-shielded SOT recipients during the pandemic was lacking in our study population or nationally. International recruitment would have been hampered by major differences in policies and language barriers. The survey data was collected during the pandemic in a cross-sectional manner, and therefore a direct comparison to prepandemic levels was not achievable. It is possible that associations of HRQoL and uncertainty was preexisting and unrelated to the COVID pandemic. However, alternate methods such as providing the survey at outpatient visits, was not possible due to shielding requirements.

Conclusive evidence of which patients are most vulnerable to severe COVID-19 disease and would benefit most from shielding is currently lacking. We relied on self-reported COVID infection rates at a time that confirmatory testing was not implemented and our study obtained no responses from recipients with severe COVID infection. The national NHSBT registry data on showed similarly low COVID-19 infection rates in SOT, however, our study carries a significant risk of responder bias for this parameter.

In conclusion, our findings demonstrate a self perceived health status that is below average in shielded SOT recipients, a subgroup of clinically extremely vulnerable individuals. Our study shows a resilient population reliant on acceptance and adherence to protective behaviour. Strategies to improve outcomes during shielding for the pandemic may be targeted at identified risk groups, reducing uncertainty and prevention of maladaptive coping strategies. Provision of continuity of care, information and clear guidance during different stages of the pandemic may increase public trust and address the specific concerns of individuals deemed clinically extremely vulnerable to COVID-19.

This article is protected by copyright. All rights reserved Acknowledgements:

Surgeons of England, to undertake the study. The funding source had no role in the conduct of the study.

Data collected for this study, including individual participant data and the data data dictionary, will be made available to others at publication. The data will be in anonymised form to protect participants privacy.

The authorship agrees to provide access to all additional study documents. 

This article is protected by copyright. All rights reserved (7) Prefer not to answer 6 (1) [33] . † 0 = not susceptible, 100 = very susceptible ‡ 0 = not severely unwell, 100 = severely unwell § 0 = don't know at all, 100 = know very well † † 0 = extremely difficult, 100 = extremely easy ‡ ‡ 0 = no confidence, 100 = very confident 

This article is protected by copyright. All rights reserved Table 5 : Health-related quality of life in shielded solid organ transplant (SOT) recipients compared to UK population** (using EQ-5D-5L***) (7) 23 (14) 118 (10) 32 (14) 162 (13) 49 (20) 163 (15) 11 (22) 180 (21) 3 0 (0) 10 (2) 5 (10) 20 (2) (2) 5 0 (0) 6 (1) 0 (0) 2 (0) 4 (6) 9 (1) 2 (1) 22 (2) 3 (1) 17 (1) 1 (0) 6 (1) 0 (0) 3 (0) *P value<0.05 **UK population data derived from Health Survey England 2017 *** representing 5 levels of response for each domain; e.g. not=1, slightly, moderately, severely, or extremely=5. 

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