Introduction
COVID-19 was first described amongst a cluster of patients suffering from pneumonia in Wuhan, China [
1]. Fuelled by its viral novelty, high infectivity and global mobility [
2], COVID-19 rapidly spread around the world, and within just 3 months became a global pandemic. As a rapidly evolving and dynamic entity, the true global implications of COVID-19 remain unknown, and will probably only become clear in many years to come. As per 12th of November 2020, at least 1.27 million people have died from COVID-19. The tsunami-like ramifications of COVID-19 and the associated need for ‘lockdown’ and ‘social distancing’ have had a devastating impact on the global economy that is unprecedented in the modern era [
3].
COVID-19 has also had a unique and devastating impact on global healthcare infrastructures and administration, with multiple contributing factors. Although there are inevitable direct effects on service provision from increased hospital including intensive care admissions of patients with COVID-19, it is perhaps the multiple and insidious indirect effects of the COVID-19 pandemic that have most affected healthcare. During the COVID-19 era, there has been a dramatic reduction in the usage of NHS-based services [
4,
5], potential explanations including patient-based risk perceptions and the impact of government-based messages regarding lockdown and self-isolation [
5]. Coupled with this has been healthcare staff redeployment in many hospitals to manage the surge in hospital admissions with COVID-19, coupled with re-purposing of clinical areas for COVID-19 screening, with an associated and inevitable disruption to the provision of non-COVID-19 based, but nonetheless essential healthcare. To address these multiple and complex factors, much healthcare provision has been administered through remote media, such as phone calls and telehealth [
6]. The versatility and convenience of such remote healthcare provision promotes its likely ongoing usage for at least some aspects of service in the post-COVID-19 era.
Of particular concern has been the impact of COVID-19 on tumour services, including the impact of delayed and missed clinic appointments for the overall health of the populace [
7,
8]. Healthcare provision for neuroendocrine tumours (NETs) represents a specialised form of services that is typically administered by highly skilled multidisciplinary teams operating within s Centres of Excellence (CoE). Recently, guidance for the management of patients with NETs during the COVID-19 era was published [
9‐
11]. Given the nature of NET-based clinical services, the relatively small number of NET-based clinical centres and the vulnerability of many patients with NETs, it is important to explore the impact of the COVID-19 pandemic on patients with NETs, and the associated specialist provision of healthcare.
Our aim was to perform an assessment on the impact of COVID-19 on healthcare administration and care for patients with NETs, with cross-national comparisons between European Neuroendocrine Tumour Society (ENETS) CoE based in England and those in other countries.
Materials and methods
An electronic survey was distributed to all 11 ENETS CoE in England, via e-mail. A similar number of non-UK ENETS CoE were contacted, for comparison. The survey was designed using Google Forms and captured information in the following categories: (1) background/pre-COVID-19 state, (2) impact of COVID-19 on clinical services, (3) impact on operational service provision, (4) impact on research. Questions included in the survey comprised both semi-quantitative and qualitative response options. Qualitative analysis took the form of thematic analysis (and where appropriate, coding) of answers received. A full breakdown of the questions asked is shown in Appendix
1. The survey was analysed comparing ENETS CoE in England to ENETS CoE elsewhere, using both qualitative and semi-quantitative analysis approaches including qualitative analysis of free-text responses. Responses were received from the specialist NET healthcare professionals (Consultants/Centre leads) who consented to participate in this survey. Given that this was an international survey, ethics approval was pursued through the Institution with the shortest period of approval (Ethics Committee of the Laiko General Hospital, Athens, Greece; protocol number 10712, date of issue 6 July 2020).
Statistical analyses
Data are presented as means ± standard error, or percentages, as appropriate. Significance was defined as p < 0.05. One-way analysis of variance was used to compare study subgroups. Analyses were performed using SPSS version 25 (SPSS Inc., Chicago, IL).
Discussion
Our study is capturing ‘real life’ perceptions about the impact of the current COVID-19 pandemic on specialist NET services in ENETS CoE. In contrast to other recently published studies that had also included ‘low-activity’ (<100 neuroendocrine neoplasms (NEN) patients in follow-up) [
12,
13] and ‘mid-activity’ centres (100–300 NEN patients in follow-up) [
13], in our study we have exclusively focussed on the effects of the COVID-19 pandemic in typically ‘high activity’, University or University Teaching Hospital-based ENETS CoE. Our present findings demonstrate a significant disruption to NET services across all surveyed centres. Of note, this major disruption in specialist NET services included relevantly increased waiting times for both new and follow-up appointments, with an especially substantial delay of follow-up appointments in most of the surveyed centres. Similar findings were reported by a recent study in Italian NEN centres [
13] including also ‘low-’ and ‘mid-activity’ centres, whereas in a recent study in Germany, Austria and Switzerland disruption in outpatient appointments was more severe in the University setting as compared with non-university hospitals and private practice settings [
12]. We also observed a relevant disruption to diagnostic services. Similarly, specialised treatment of patients with NETs was delayed, which included a relevant delay in surgical treatment; and again, in agreement with the observations made in other countries such as Italy [
13]. In our survey, this included all types of NET, independent of the primary location and histological grading. Although many NETs are relatively slow growing, a delay in curative surgical treatment may result in disease spreading and clearly has the potential to increase anxiety levels in these patients, thereby further negatively impacting their quality of life [
14].
A COVID-19 pandemic-related delay in treatment with PRRT based on concerns, i.e., due to the frequently observed PRRT-associated lymphopenia may be somewhat overcautious, given that PRRT mainly appears to cause B-cell repletion (in 18–52% of patients treated with
177Lutetium-PRRT and some 75% of patients treated with
90Yttrium-PRRT) [
15,
16], but appears to have less severe effects on T cells and only minor effects on natural killer cells, explaining the absence of opportunistic infections following treatment with PRRT [
15]. However, both for planned surgical interventions and treatment with PRRT, hospital beds need to be ‘ring-fenced’, which can be problematic in times of a pandemic with overflowing Acute Medicine and A&E departments and the need to isolate numerous patients in one bed rooms.
Moreover, we observed a change in practice in the way of both new patient and follow-up appointments are provided, with all surveyed centres now providing more virtual appointments and most centres reporting that the majority of appointments had been converted to virtual appointments. This change in practice was more frequently reported in the ENETS CoE in England vs. other countries, possibly related to the availability and fast set-up of the required equipment. Feedback of clinicians to this change was mixed, with the main disadvantages mentioned being unable to physically examine the patients. However, perceived positive aspects included improved convenience for (stable) patients who do not live locally, and a reduced number of non-attenders.
Redeployment of both nursing and medical staff was reported in most of the surveyed centres, but the impact on the management of patients with NET was generally considered to be relatively minor. A reduction in the frequency of multidisciplinary meetings was reported in two thirds of the ENETS CoE outside England, but no such effect was reported in the ENETS CoE in England. However, across the surveyed centres nearly half of the centres now run their tumour board meetings virtually. The feedback of clinicians to this change was generally positive, although there can be barriers related to connection issues and the quality of the available equipment.
All but one of the non-UK centres reported that there was a negative impact of the COVID-19 pandemic on research activity. There was no difference in the disruption of research activity when comparing ENETS CoE in England vs. ENETS CoE elsewhere. However, the perceived impact of the COVID-19 pandemic on the availability of future research funding for the NET services in the respective centres was bleaker in the English ENETS CoE and significantly different between ENETS CoE in England and elsewhere. Our results suggest that ENETS CoE in England may face a longer road to restoration of NET services due to reduced research activity and particularly pessimistic predictions regarding future research funding. The impact on research funding is further important as it may coincide with greater funding difficulties related to the UK’s departure from the European Union (Brexit) [
17‐
19], suggesting that very significant efforts and mitigations would be required UK NET research centres now, to ensure that they can fully contribute to research in the future.
A limitation of our survey is that the data presented here, albeit novel and detailed, is from a small sample size of specialised ENETS CoE. Also, reporting bias cannot be excluded, i.e., some of the NET Centres worst affected by the COVID-19 pandemic may simply not have prioritised responding to our survey invitation. Finally, the fact that only one centre response for each of the other countries was received (also having in mind that in some of the contacted countries, only one ENETS CoE has been certified to date) is limiting how much one can interpret the data for individual countries other than England. The results should be interpreted in that context. However, despite these limitations, we believe there are important messages for both restoration of services and planning of future NET care and research approaches. Overall, it is important that such specialist areas are not being neglected in comparison to broader services. There is important further work that is needed to monitor and track the recovery of all services including NET services and research following the COVID-19 pandemic. Furthermore, it is important to assess the impact of COVID-19 and the related healthcare disruptions to services on patients themselves, both by capturing their perceptions of care during the pandemic and by monitoring for any worsening outcomes that may have occurred. One of the possible positives that appears to come from the pandemic is an exploration of the use of virtual and remote services.
To conclude, we report on the first study to assess the impact of COVID-19 on ENETS CoEs in England, and compare with data from a selection of ENETS CoEs from other western European countries. This survey has identified various deficiencies in the provision of NET services even in highly specialised set-up, as a result of the COVID-19 pandemic. The same may apply for tumour services in general, although it is possible that highly specialised services with relatively low numbers of patients could be particularly affected. Future assessment of the impact of COVID-19 on NET healthcare from a patient perspective is important. Based on our data, it is important to develop novel and unified approaches to future healthcare provision for patients with NETs. This may include critical review of possible widespread adoption of remote appointments and proper planning for future pandemic scenarios that minimises disruption to the provision of healthcare to this important and vulnerable group of patients with unique and highly specialised medical needs.
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