key: cord-0858026-q0563885
authors: Heightman, Melissa; Prashar, Jai; Hillman, Toby E; Marks, Michael; Livingston, Rebecca; Ridsdale, Heidi A; Bell, Robert; Zandi, Michael; McNamara, Patricia; Chauhan, Alisha; Denneny, Emma; Astin, Ronan; Purcell, Helen; Attree, Emily; Hishmeh, Lyth; Prescott, Gordon; Evans, Rebecca; Mehta, Puja; Brennan, Ewen; Brown, Jeremy S; Porter, Joanna; Logan, Sarah; Wall, Emma; Dehbi, Hakim-Moulay; Cone, Stephen; Banerjee, Amitava
title: Post-COVID-19 assessment in a specialist clinical service: a 12-month, single-centre, prospective study in 1325 individuals
date: 2021-11-11
journal: BMJ Open Respir Res
DOI: 10.1136/bmjresp-2021-001041
sha: 812da4ca3af5a5614ec271193ee96cf74a38f687
doc_id: 858026
cord_uid: q0563885

INTRODUCTION: Post-COVID-19 complications require simultaneous characterisation and management to plan policy and health system responses. We describe the 12-month experience of the first UK dedicated post-COVID-19 clinical service to include hospitalised and non-hospitalised patients. METHODS: In a single-centre, observational analysis, we report the demographics, symptoms, comorbidities, investigations, treatments, functional recovery, specialist referral and rehabilitation of 1325 individuals assessed at the University College London Hospitals post-COVID-19 service between April 2020 and April 2021, comparing by referral route: posthospitalised (PH), non-hospitalised (NH) and post emergency department (PED). Symptoms associated with poor recovery or inability to return to work full time were assessed using multivariable logistic regression. RESULTS: 1325 individuals were assessed (PH: 547, 41.3%; PED: 212, 16%; NH: 566, 42.7%). Compared with the PH and PED groups, the NH group were younger (median 44.6 (35.6–52.8) years vs 58.3 (47.0–67.7) years and 48.5 (39.4–55.7) years), more likely to be female (68.2%, 43.0% and 59.9%), less likely to be of ethnic minority (30.9%, 52.7% and 41.0%) or seen later after symptom onset (median (IQR): 194 (118–298) days, 69 (51–111) days and 76 (55–128) days; all p<0.0001). All groups had similar rates of onward specialist referral (NH 18.7%, PH 16.1% and PED 18.9%, p=0.452) and were more likely to require support for breathlessness (23.7%, 5.5% and 15.1%, p<0.001) and fatigue (17.8%, 4.8% and 8.0%, p<0.001). Hospitalised patients had higher rates of pulmonary emboli, persistent lung interstitial abnormalities and other organ impairment. 716 (54.0%) individuals reported <75% optimal health (median 70%, IQR 55%–85%). Less than half of employed individuals could return to work full time at first assessment. CONCLUSION: Post-COVID-19 symptoms were significant in PH and NH patients, with significant ongoing healthcare needs and utilisation. Trials of interventions and patient-centred pathways for diagnostic and treatment approaches are urgently required.

Chronic post-viral sequelae are well known, 1 but the SARS-CoV-2 pandemic's scale poses an unprecedented threat to long-term health. 2 3 Initially, funding, research, clinical practice and policy emphasised acute, hospitalised patients in areas with a high burden of COVID-19 cases and deaths. However, more recently, there has been an increasing focus on the longer-term effects of acute infection ('Long COVID' or 'post-COVID syndrome'), including non-hospitalised patients 4 5 (figure 1).

Clinically, long COVID remains a poorly defined disease. 5 6 To address the healthcare needs of an estimated 1.1 million individuals with long COVID in the UK 7 and the millions around the world, 8 there is a need to deliver clinical care while simultaneously reviewing clinical data in 'learning health system' approaches. 9 Research on clinical characterisation and management has been identified Key messages ► There is high symptom burden for non-hospitalised patients post-COVID-19, even compared with posthospitalised patients post-COVID-19. ► The significant, long-lasting health and social consequences of SARS-CoV-2 infection are not confined to those who required hospitalisation. ► This is the first study to report the baseline characteristics, investigations and outcomes of initial assessment of all eligible patients in a dedicated multiprofessional post-COVID-19 service, including 547 posthospitalisation, 566 non-hospitalised and 212 patients discharged from the emergency department.

Open access by both recent expert consensus groups and patients as a priority area. 10 COVID-19 hospitalisation is associated with a significant risk of end-organ impact, functional impairment, readmission and mortality. [11] [12] [13] Recent analysis of 6-month post-COVID-19 outcomes in China highlighted persistent physical, mental and functional impact during follow-up, but excluded non-hospitalised patients. 14 Recent electronic health record (EHR) analyses in the USA and Denmark, respectively, suggested major healthcare resource implications of long COVID in nonhospitalised individuals, 15 16 but no studies to date have reported on the models of care for long COVID.

More than 80 dedicated post-COVID-19 assessment clinics have been announced in England, 17 but many centres only started accepting referrals 1 year after the first wave of the pandemic. Various care models have been proposed through expert and patient consensus, 18 19 but Open access real-world data are lacking, particularly in community settings, where majority of patients with COVID-19 and long COVID are managed.

In April 2020, we established a dedicated service for assessment of post-COVID-19 complications at University College London Hospitals NHS Foundation Trust (UCLH) for both hospitalised and non-hospitalised individuals. We report the baseline characteristics, clinical presentation, management and outcomes of all individuals referred to this specialist clinic following suspected or confirmed SARS-CoV-2 infection over a 12-month period.

The UCLH post-COVID-19 service is a one-stop model of assessment (by physician and physiotherapist), diagnostics and exercise test to triage need for further specialist input, treatment or rehabilitation. It accepts referrals from three sources: (1) posthospitalised (PH): postadmission to UCLH with COVID-19; (2) non-hospitalised (NH): individuals referred from primary care with suspected long COVID ≥6 weeks post-SARS-CoV-2 infection; and (3) post emergency department (PED): referral for individuals with persistent symptoms at 4-6 weeks after attendance. As per the British Thoracic Society guidance, 20 postdischarge review in PH patients was at 6 weeks for those who received respiratory support via continuous positive airway pressure or invasive ventilation, or with chest imaging abnormality, and at 12 weeks in all other patients. PH patients under the care of other specialist services or without chest X-ray abnormalities were not routinely booked into the post-COVID-19 service.

Our analysis included all patients assessed at the UCLH post-COVID-19 service between 20 April 2020 and 25 April 2021 (figure 2), excluding follow-up assessments and individuals who did not attend. Due to restricted access to testing during the first wave of the pandemic, SARS-CoV-2 infection was defined by either laboratory confirmation (viral positive oropharyngeal/nasopharyngeal swab when tested by reverse-transcriptase PCR or anti-N antigen IgG detected on convalescent serum) or strong clinical suspicion (assessed by both the referring and consulting clinicians). 21 We followed the Strengthening the Reporting of Observational Studies in Epidemiology criteria (checklist). 22 Post-COVID-19 assessment Clinical assessment was developed by secondary care clinicians and therapists and consists of a consultation and multiprofessional assessment, delivered primarily face to face, or where necessary virtually. An EHR (Epic; Epic Systems Corporation, Wisconsin) structured assessment tool (accessible via the patient portal before the appointment and during assessment) was used to record the sociodemographics, medical history, current symptoms and functional status. Where appropriate, the following outcome measures were recorded: percentage of best health (as used in other tools; eg, EuroQoL-5 domain-5 level), symptom severity for breathlessness, fatigue, cough, sleep disturbance and palpitations, MRC (Medical Research Council) Dyspnoea Scale, Post-Traumatic Stress Disorder Scale (PTSD), Fatigue Assessment Scale, two-item Generalised Anxiety Disorder (GAD-2), and Open access two-item Patient Health Questionnaire (PHQ-2) 5 11 13 21 (online supplemental methods).

Selected patients underwent further investigation at the discretion of the clinician or following multidisciplinary team meetings with respiratory, cardiology and neurology input according to clinical need. These tests included full blood count, liver and renal function, D-dimer, troponin and NT pro-brain natriuretic peptide (NT-proBNP), as well as sit-to-stand test, chest X-ray, Computed Tomography Pulmonary Angiography (CTPA) with HRCT (High-Resolution Computed Tomography) precontrast, ECG, cardiac MRI (cMRI), brain MRI, echocardiography and Holter monitoring. Lung function testing was unavailable due to local infection control requirements.

After assessment, patients were either discharged to the community, booked for further clinical follow-up, and/ or referred for specialist opinion, physical rehabilitation, respiratory physiotherapy, fatigue management, vocational support and psychological support. Patients with elevated GAD-2 or PHQ-2 scores (≥3) were advised on self-referral to 'improving access to psychological therapies' services.

Demographic and clinical data at first assessment were extracted from the EHR. Age, time since symptom onset in days and self-reported percentage of best health were recorded as continuous variables, and the presence or absence of individual symptoms as binary variables. Selfreported ability to return to work, for employed individuals, was recorded on an ordinal scale ('Not at all' to 'Full time'). The Index of Multiple Deprivation (IMD) decile was derived from each patient's postcode. We used descriptive statistics to summarise the baseline characteristics. Continuous variables are reported as median with IQR, while categorical variables are reported as frequency (%). For group-wise comparison, we used the Kruskal-Wallis test for continuous variables and the χ 2 test or Fisher's exact test for categorical variables. We used multivariable logistic regression models, adjusted for age (modelled as a continuous variable) and gender (male vs female as the reference group), to investigate symptoms associated with (1) optimal (≥75%) patient-reported functional recovery at first presentation and (2) patientreported ability to return to full-time employment at first presentation. The model for returning to employment excluded those not employed or retired before COVID-19. Age and gender were included in the models and all recorded symptoms (represented as presence vs absence) were available for selection in a backwards stepwise selection process with a threshold of p<0.05. A sensitivity analysis also considered time since onset for selection in the models. Referral rates of local General Practices (GPs) (per 1000 practice population) were determined using locally available EHR data for practice size and referring practice. All analyses were performed using Python V.3.7.6.

The number of referrals to the UCLH post-COVID-19 clinic mirrored successive pandemic waves (figure 1). Excluding patients who did not attend and who cancelled appointments, 1325 patients were reviewed: PH, n=547; NH, n=566; and PED, n=212 (figure 2). Of the patients, 614 (46.3%) were tested for SARS-CoV-2 infection using RT-PCR(reverse transcription polymerase chain reaction), of whom 378 (61.6%) were positive, while among those who underwent serological testing (n=241, 18 

Hypertension (17.5%), asthma (13.4%), cardiovascular disease (12.5%), diabetes (11.8%) and thyroid disease (6.6%) were the most common comorbidities. Most premorbid chronic diseases were more common among PH patients, compared with NH and PED patients, except asthma (12.1% vs 14.0% and 15.6%), anxiety (3.5% vs 2.7% and 4.7%), depression (2.9% vs 3.0% and 5.7%) and chronic fatigue syndrome (0.0% vs 1.4% and 0.9%). Current smoking was uncommon (1.3% overall) (table 1). Overall, 86 PH patients died before a post-COVID-19 clinical assessment, with a further two PH patients dying after clinical review.

The median time from symptom onset (of acute SARS-CoV-2 infection) to first clinical assessment was 108 days (IQR 61-197), and was delayed in NH patients (194 (118-298) days) compared with PH patients (69 (51-111) days) and PED patients (76 (55-128) days) (p<0.001).

At first visit, the median (IQR) number of reported symptoms was 2 (1-4) overall (PH, NH and PED groups: 1 (0-2), 3 (2-5) and 2 (1-4), p<0.001). The most commonly Open access 2) .

In the PH, NH and PED groups, the median self-reported proportion with optimal health was 80% (65%-95%), 60% (50%-75%) and 75% (60%-90%), respectively, correlating negatively with symptom duration at the time of assessment (table 1 and online supplemental figure 3) . Overall, less than half of employed individuals felt able to return to work full time at first assessment (online supplemental table 1).

In the multivariable logistic regression analysis (table 3), younger age was associated with return to work (PH and NH) and male gender (PH and PED). For PH individuals, fatigue, brain fog, chest pain and breathlessness were associated with inability to work full time. Arthralgia and headache were associated with full-time return to work. For NH individuals, fatigue, brain fog and headache were associated with inability to return to work. For PED individuals, breathlessness and myalgia were associated with non-return to work, whereas cough and arthralgia were associated with return to work. For some included symptoms, the 95% CIs were wide, suggesting uncertainty about their effect, perhaps due to the small number of patients with that symptom. Older age and male gender were associated with return to optimal health status (≥75%). Fatigue and postural symptoms were significantly associated with suboptimal (<75%) health status in the PH and NH groups, and brain fog in the NH and PED groups Open access (table 3) . Postural symptoms were rare in PH patients, and few with this symptom achieved optimal health. The extreme OR probably reflected the small number recovering in this group, rather than the importance of this symptom. Sensitivity analyses including time since onset in the backwards selection process only changed the models for recovery in NH patients, where longer times since onset and disturbed sleep were associated with lower odds of recovery, replacing postural symptoms in the model. Our results underscore the patient and system need for comprehensive measurement and reporting of effects of SARS-CoV-2 infection in all individuals (PH and NH) on health, function and healthcare utilisation, and the profound ramifications for the individuals, their families and communities beyond measures of functional impairment and organ dysfunction. Patients with long COVID have called for 'recognition, research and rehabilitation', 23 but COVID-19 research and care have focused primarily on acute physiology, management and mortality among hospitalised individuals. It has been previously established that the burden of specific diseases can only be compared across population groups when morbidity in addition to mortality is accurately recorded. 24 The burden of long COVID must be documented in this way.

The extent of multimorbidity and functional impairment in long COVID requires cross-specialty, multiprofessional, integrated working, and development of broader clinical expertise, with transferable benefits to other conditions beyond the pandemic, 21 rather than siloed, organ-based approaches. 19 25 Such integrated care pathways have been effective in other diseases prepandemic 26 and could support rapid upskilling and skills transference needed for the wider workforce in post-COVID-19 clinical care. To enable a consistent, holistic approach, 

we developed structured EHR tools to capture functional and psychological impact. We implemented multispecialty, multidisciplinary meetings to enhance efficiency and share learning, seeking patient feedback from all encounters to improve services. Further analysis of the correlation between symptoms, functional consequences and investigations via data-driven approaches are essential to guide mechanistic studies, treatment approaches and risk stratification. Hospital-based and clinic-based analyses are important given the slow uptake of new long COVID coding in primary care. 27 As in other studies, we document severe functional impairment [11] [12] [13] and significant mortality risk post hospital discharge. We also document severe functional impairment in NH and PED individuals despite low predicted 2 and observed mortality risk. UK guidance for posthospital follow-up prioritised those requiring greater levels of organ support or with more severe chest imaging abnormality. 20 This focus risks lack of recognition of morbidity in patients with less severe acute respiratory presentations of SARS-CoV-2 infection. The multivariable models suggested that fatigue, brain fog, chest pain and breathlessness were the common factors for continued suboptimal health and not returning to work. Other factors were less consistently included in the models and some were associated in an unexpected direction, which may be due to a real effect or confounding with other symptoms. Underlying mechanisms and management require further research.

Like other studies, we show prolonged variation in symptoms and extent of diagnostic abnormality between different cohorts, suggesting different phenotypes of post-COVID-19 syndrome/long COVID. 28 Absence of a specific diagnostic test or biomarker 29 makes the balance between adequate investigation of significant symptoms and 'over-medicalising' challenging. For example, elevated D-dimer levels triggered frequent CTPA requests, but with low diagnostic yield in NH patients. Exercise testing showed oxygen desaturation most frequently in PH patients, but also in the NH group without clear evidence of lung or heart abnormalities. Echocardiography rarely showed abnormal findings despite frequent use to investigate chest pain and breathlessness. The clinical significance of detectable abnormalities on cMRI in patients with chest pain requires further evaluation. 30 Future research must determine whether and how diagnostic abnormalities relate to end-organ effects or mechanisms underlying long COVID.

Patients often needed further specialist opinion and onward referral to community rehabilitation and psychological support, with significant resource implication given such pathways are currently poorly defined. In addition to the ongoing waves of COVID-19 infection, threats of new variants and effects on non-COVID-19 services, 2 the 'long tail' of the pandemic in terms of long COVID is a concern for policy and health service planning in all countries. Rehabilitation needs are complex and likely to require novel multimodal therapy approaches which integrate psychological support and workforce capacity and capability, which are not currently in place. Expertise in fatigue management, treatment for disordered breathing patterns and programmes to support return to employment are particular priorities. Novel digital self-management solutions could be a useful adjunct but need further evaluation. Although different post-COVID-19 care models are evolving, 31 32 the evidence base is minimal, with few, large-scale, pragmatic trials of treatment and rehabilitation. Developing integrated, research-oriented pathways in EHR-enabled health systems could provide a platform for rapid evaluation of investigation, treatment and rehabilitation approaches alongside delivering care, which has been effective in acute COVID-19. 33 There are signs of inequitable access to care in our cohort. Although the observed ethnicity of NH patients reflected the catchment population, it contrasted with the disproportionate burden of acute SARS-CoV-2 in ethnic minorities. NH patients were also less likely to live in areas of deprivation and may have had easier access to referral. Varying referral rates by primary care provider were seen, requiring further investigation to understand contributing factors. Underdiagnosis of long COVID has been described in primary care in England. 32 NH patients had delayed referral. Consideration should be given to proactive follow-up of patients managed in the community, particularly given the severity of illness in patients referred. Follow-up strategies should also account for the needs of frail, elderly, comorbid and hard-to-reach patients, who were under-represented in our cohort.

Our findings have several limitations. We report outcomes from a single centre, unlikely to be representative of the whole UK population. As post-COVID-19 clinics are established around the UK and in other countries, prospective data collection and comparison will enable variations to be investigated. We used subjective symptom and functional status data, which may have self-reporting bias. We report real-world, clinical findings and therefore data regarding premorbid status, baseline characteristics, investigations and follow-up (particularly for patients with persistent disease for 12 months or more) are more limited than in dedicated research cohorts. NH patients were self-selecting while PH patients were included as part of routine follow-up. This selection bias precludes both making precise estimates of the burden of long COVID among NH patients and also making comparisons between NH patients and other patient groups. In our basic logistic regression models, we modelled age as a linear variable, which may have obscured true non-linear effects of age in these models. Our models were based on cross-sectional data at presentation to the clinic. We did not include a control population. Although it is possible that a proportion of patients would present with 'medically unexplained symptoms', 34 we only included patients referred to the post-COVID-19 assessment service with clinical or serological confirmation of SARS-CoV-2 infection. Moreover, there is evidence that long-term Open access symptoms are significantly higher in individuals who are PCR-positive for SARS-CoV-2, compared with PCRnegative individuals, 35 and higher in individuals with long COVID compared with postinfluenza. 36 Our findings have several implications for research and policy. First, we identified differences in the longerterm effects of SARS-CoV-2 infection in PH versus NH individuals, supporting the existence of a number of different phenotypes of long COVID. Further correlation of symptom clusters, functional impact and diagnostic information is required to better define phenotypes and to inform studies of underlying mechanisms and potential treatments. Second, a wide range of patient-reported outcome measures were required to capture the impact of long COVID on individuals. Development of a validated clinical assessment tool will further enable investigation of the natural history of the condition across larger data sets and differing EHR systems. Third, we identified the need for a novel model of rehabilitation, incorporating psychological support and urgent solutions to address the current workforce shortfalls. Fourth, the multisystem nature of the condition will require broadening of clinical expertise both within primary and secondary care and effective integrated pathways. Finally, given the severity of illness documented in all patient groups, our analysis supports the need for swift, equitable access to assessment for all patients suffering from ongoing illness after SARS-CoV-2 infection, as well as effective infection suppression policy for all.

Post-COVID-19 morbidity can be severe, regardless of severity of acute illness, and the scale of healthcare utilisation and inability to return to employment represent a major burden to individuals, healthcare and welfare systems, and economies. Definition of long COVID phenotypes and development and evaluation of diagnostic, treatment and rehabilitation approaches are urgently required. Dissemination of clinical expertise in the management of post-COVID-19 complications needs to occur across integrated care systems and policy change is required to improve equity of access by individuals to appropriate levels of care and support.

Patient views were incorporated in the development of the clinical pathways since inception, and two patients have been involved in the writing and review of the final manuscript (EA and LH). The views expressed by patient groups in meetings attended by MH and TEH (eg, NHS England's Long COVID Taskforce, Department of Health and Social Care's Long COVID Round Table) informed the study objectives and design, and through EA and LH the views of wider patient groups (ie, LongCOVIDSOS and UKDoctors#Longcovid) were also incorporated. Central and North West London NHS Foundation Trust, London, UK 5 UKDoctors#Longcovid, London, UK 6 Long COVID SOS, Oxford, UK 7 University of Central Lancashire, Preston, UK 8 Francis Crick Institute, London, UK 9 Barts Health NHS Trust, London, UK Contributors MH has led the UCLH post-COVID-19 service since inception, with TEH. MM, RL, HAR, RB, MZ, PMcN, EW, RE, AC, EB, PM and ED provided clinical support to the service. MH, TEH and AB wrote the first and final drafts of the manuscript. JP conducted the analyses, with input from MH, SC and AB, and statistical input from HM-D and GP. All authors provided critical feedback on earlier and final drafts of the manuscript. AB is guarantor for the study.

Funding The UCL/UCLH Biomedical Research Centre part-funded two research fellows who were involved in the clinical service delivery. The clinic was based at UCLH. AB, TEH, MZ, GP, EA, LH, EW and MH have received funding from the NIHR (LT2-0043) for the STIMULATE-ICP study.

Competing interests AB has received research grants from AstraZeneca, unrelated to this work. All other authors report no relevant conflicts of interest.

Patient consent for publication Not required.

Ethics approval This study was confirmed to be a service evaluation, and ethical approval was waived, by UCLH's Research and Development and Information Governance Directorates as part of the UCLH Data Access Committee set up in response to the COVID-19 pandemic (https://www. uclhospitals. brc. nihr. ac. uk/ clinical-research-informatics-unit/ data-explorer), following UK COVID-19 guidelines for use of patient data (https://www. hra. nhs. uk/ covid-19-research/ guidance-usingpatient-data/).

Provenance and peer review Not commissioned; externally peer reviewed.

Data availability statement All data relevant to the study are included in the article or uploaded as supplementary information.

Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.

Open access This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http:// creativecommons. org/ licenses/ by-nc/ 4. 0/.

Robert Bell http:// orcid. org/ 0000-0003-2199-2638 Amitava Banerjee http:// orcid. org/ 0000-0001-8741-3411

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