The Impact of the COVID-19 Pandemic on a Dedicated Vascular Emergency Clinic

Background Vascular Emergency Clinics (VEC) improve patient outcomes in chronic limb-threatening ischemia (CLTI). They provide a “1 stop” open access policy, whereby “suspicion of CLTI” by a healthcare professional or patient leads to a direct review. We assessed the resilience of the outpatient VEC model to the first year of the coronavirus disease (COVID-19) pandemic. Methods A retrospective review of a prospectively maintained database of all patients assessed in our VEC for lower limb pathologies between March 2020 and April 2021 was performed. This was cross-referenced to national and loco-regional Governmental COVID-19 data. Individuals with CLTI were further analysed to determine Peripheral Arterial Disease–Quality Improvement Framework compliance. Results Seven hundred and ninety one patients attended for 1,084 assessments (Male n = 484, 61%; Age 72.5 ± standard deviation 12.2 years; White British n = 645, 81.7%). In total, 322 patients were diagnosed with CLTI (40.7%). A total of 188 individuals (58.6%) underwent a first revascularization strategy (Endovascular n = 128, 39.8%; Hybrid n = 41, 12.7%; Open surgery n = 19, 5.9%; Conservative n = 134, 41.6%). Major lower limb amputation rate was 10.9% (n = 35) and mortality rate was 25.8% (n = 83) at 12 months of follow-up. Median referral to assessment time was 3 days (interquartile range: 1–5). For the nonadmitted patient with CLTI, the median assessment to intervention was 8 days (interquartile range: 6–15) and median referral to intervention time of 11 days (11–18). Conclusions The VEC model has demonstrated strong resilience to the COVID-19 pandemic with rapid treatment timelines maintained for patients with CLTI.


INTRODUCTION
Rapid service restructuring introduced in the United Kingdom during the coronavirus disease 2019 (COVID- 19) pandemic has been detrimental to the delivery of non-COVID-19erelated healthcare within the National Health Service (NHS); mean waiting time for all Consultant-led referral to elective treatment across NHS England services increased from 7.5 weeks in February 2020 to 12.6 weeks in February 2021. 1 The provision of vascular surgical services in particular has been negatively impacted by COVID-19, as a result of forced changes to outpatient referral pathways, access to operating theatres, and availability of perioperative high dependency care. Unfortunately, these changes have been seen worldwide. The COVID-19 Vascular sERvice study demonstrated that vascular surgery units in the United Kingdom had a more significant reduction in service compared to other services globally. 2 Guidance by the Vascular Society of Great Britain and Ireland (VSGBI) during the COVID-19 pandemic recommended urgent intervention for threatened legs, diversion to a hot clinic for those who were able, and consideration of a primary amputation rather than complex revascularization with multiple wound debridement. 3 This was reflected globally with a greater proportion of major lower limb amputations (MLLAs) or palliation carried out over revascularization and 60% of units reporting a move to an endovascular-first treatment for chronic limb-threatening ischemia (CLTI). 2 During the pre-COVID era, access to rapid assessment and treatment for patients with CLTI was inconsistent throughout the United Kingdom. 4 To address regional variations, the VSGBI released a ''deliberately challenging'' timeframe for the management of patients presenting with CLTI. 5 We have previously reported that a dedicated vascular limb salvage clinic facilitates rapid assessment and revascularization of patients with CLTI, that in turn leads to a reduction in MLLA rates. 6 To date, the ability of this model of limb salvage care to withstand unexpected and rapid changes in healthcare service provision and maintain rapid access and treatment for patients with CLTI has not been examined.
The aim of this study is to report the effect of the COVID-19 pandemic on our outpatient Vascular Emergency Clinic (VEC) for the management of suspected CLTI patients within one of the worst affected areas within the United Kingdom. We assess (1) the referral to assessment, and assessment to intervention timeline; (2) freedom from MLLA at 12 months; and (3) survival at 12 months all during the first year of the COVID-19 pandemic in the United Kingdom (March 13, 2020 to April 9, 2021).

MATERIALS AND METHODS
Details of the clinic have been described previously. 6 Briefly, the clinic opened in February 2018 providing a ''1 stop'' open access, urgent outpatient-based vascular limb salvage clinic for adult patients with suspected CLTI. The primary aim of the clinic was to reduce MLLA for patients with CLTI, through rapid assessment and intervention (within 14 days of referral). Pre-COVID-19, the clinic reported a 10% increase in the proportion of patients with CLTI who were free from MLLA at 12 months compared to a comparator group of patients seen prior to induction of the service. The median time from referral to treatment was just 8 days. 6 Response to COVID-19 On January 30, 2020, the World Health Organization declared the outbreak of COVID-19, a public health emergency of international concern, and called for testing, tracing, and social distancing. 7 The NHS Test and Trace in England, however, was not launched until May 28, 2020, resulting in an unknown number of COVID-19 cases during the first wave of the pandemic. 8 To date, the United Kingdom has the greatest number of COVID-19 deaths in Europe. 9 To reduce the number and transmission of cases throughout the pandemic, the UK Government imposed 3 national UK lockdowns, with the first being implemented on March 26, 2020 with people ordered to ''stay home''. In June 2020, Leicestershire experienced the highest number of ongoing community COVID-19 cases resulting in more strict and longer lockdown measures compared with the rest of the country. 10 The National Institute for Health and Care Excellence released guidance for the arrangement of patients requiring elective surgery and other planned treatments and procedures in July 2020. Patients were advised to self-isolate for 14 days prior to a planned procedure and have a COVID-19 polymerase chain reaction test 3 days before admissions. 11 Open access national and loco-regional Governmental COVID-19 data for the University Hospitals of Leicester (UHL) were collected to determine trends.

Impact of COVID-19 on Outpatient Clinic
During the first year of the COVID-19 pandemic, the vascular limb salvage clinic became the VEC and relocated from the inpatient vascular assessment ward to a dedicated outpatient setting. Referral pathways remained similar to pre-COVID with an ''open access'' policy, whereby ''suspicion of CLTI'' by a healthcare professional or patient led to direct review. During the pandemic we expanded the referral criteria to also allow patients referred with all vascular pathologies requiring urgent assessment, but not inpatient admission, to be assessed. These individuals were triaged by the on-call vascular team. The staffing of the clinic remained identical to pre-COVID-19, with 2 vascular specialist nurses reviewing all referrals and discussing with the on-call vascular team, if required. All initial assessments and documentation were carried out by the vascular specialist nurses. During the pandemic, a decision was made to have a dedicated consultant vascular surgeon present throughout the clinic time, with the aim to facilitate rapid clinical decisionmaking and minimize the length of time patients were exposed to the hospital environment.
Concurrently, access to vascular operating theatres and angiography suites were significantly reduced. Access to the vascular hybrid theatre was also impacted with this facility being requisitioned for 3 months during the study timeframe to facilitate ventilatory support for patients with COVID-19. Emergency theatre list was shared with other specialities ultimately resulting in a reduction in 60% of list space.

Study Design and Population
Data from a prospectively maintained vascular outpatient databases at the UHL were examined. All patients with suspected lower limb pathologies presenting in VEC between March 13, 2020 and April 9, 2021 were included. CLTI was defined as ischemic rest pain or tissue loss with objective evidence of peripheral arterial disease. Open access national and loco-regional Governmental COVID-19 data for UHL were examined between March 13, 2020 and April 9, 2021. 12 We included the following weekly numbers: number of deaths registered in Leicester involving COVID-19; the number of COVID-19 patients occupying a mechanical ventilation bed in UHL; the number of weekly COVID-19e related hospital admissions to UHL for Leicester residents; the number of COVID-19 patients at UHL; and the number of people in Leicester with a positive COVID-19 polymerase chain reaction test were included. Data from a historical (pre-COVID) cohort presenting to the Vascular Limb Salvage clinic (CLTI-only VEC) were used to assess whether the impacts of COVID-19 had resulted in worse limb-salvage rates.

Baseline Data
Patient electronic medical records were reviewed for baseline demographics including sex, age, ethnicity, diagnosis, referral, and assessment time. Patients with a diagnosis of CLTI underwent further data extraction including previous revascularization within 2 years, history of diabetes mellitus, hypertension, previous stroke or transient ischemic attack, ischemic heart disease, chronic kidney disease (as defined by The National Institute for Health and Care Excellence 13 ), chronic obstructive pulmonary disease, and smoking status. Best medical therapy at time of assessment were also extracted (antiplatelet and lipid lowering use). Length of symptoms and disease severity at assessment were recorded using Rutherford's classification and, where possible, the Wound, Ischemia, and foot Infection Classification System. 14,15 All patients diagnosed with CLTI were followed up for 12 months postassessment or until death (whichever came first). COVID-19 status from UHL records 30 days prior and 30 days after initial assessment were obtained. Details on subsequent crosssectional imaging, revascularization (endovascular, hybrid, and open surgery), and amputation type and time were collected. MLLA was defined as an amputation proximal to the ankle joint.

Statistical Analysis
Continuous baseline variables, treatment and assessment times, and Governmental COVID-19 data were examined for normality using histogram plots and subsequently presented as medians (with interquartile ranges [IQRs]). Categorical baseline variables were presented as frequencies with percentage. A negative binomial regression with log link was used to determine the association between weekly median referral to assessment and referral to intervention time compared with weekly COVID-19erelated hospital admissions in UHL for Leicester residents and weekly COVID-19epositive patients at UHL. A P value < 0.050 was considered statistically significant. Kaplan-Meier curves were presented with 95% confidence intervals (CIs) to determine survival estimates and freedom from MLLA, at 12 months for patients with CLTI. Comparisons of 1-year MLLA incidence between the COVID-19 and pre-COVID cohorts were made using Fine-Gray competing risk analysis (death as the competing risk), reported as subdistribution hazard ratios with 95% CI and presented in cumulative incidence plots. Kaplan-Meier and cumulative incidence plots were constructed and statistical analyses performed using Stata version 16

Ethical Approval
All data were collected and analysed as part of a local service improvement project and approved by the UHL NHS Trust's Clinical Audit department (reference 11,247). No additional ethical approval or individual participant consent was required.

Patient Demographics
Between March 13, 2020 and April 9, 2021, 791 patients attended for 1,084 lower limb assessments. The mean age of these patients was 72.5 years (standard deviation ± 12.2 years) and their baseline demographics are presented in Table I. Of these, 75 patients were admitted for inpatient treatment (9.4%). A total of 322 patients (40.7%) were found to have CLTI. This group underwent further data extraction and analysis (Table II).

Treatment Timings
All patients managed within VEC were assessed within a median of 3 days from referral (IQR 1e5), corresponding to 100% of patients being seen within the outpatient VSGBI timeframe. The median assessment to intervention for the admitted patient with CLTI was 5 days (IQR 2e7). For the nonadmitted patient with CLTI, the median assessment to intervention time was 8 days (IQR 6e15). The median referral to intervention time was 11 days (IQR 11e18) with a total of 66% of individuals undergoing revascularization within the 14day VSGBI target. The median time from referral to operation for those requiring minor amputation/debridement was 7 days (IQR 5e10).

Relation to COVID-19 Rates
The referral to assessment time for all assessments was calculated per week to determine associations with the COVID-19 pandemic (Fig. 3). The longest referral to assessment time was the week beginning September 8, 2021 (median 8 days; IQR 2e9). The mean number of assessments seen per week was 19 (standard deviation ± 6.3). However, after the first UK National lockdown on March 26, 2020, the mean number of assessments seen in the combined clinic was 6. After the first local Leicestershire lockdown on July 4, 2020, this rose to 15. This then rose again to 19 after the second National UK lockdown on November 5, 2020. As the pandemic progressed, we were able to reduce the assessment to referral time in days for those within VEC (Fig. 3). This was despite the overall greatest number of patients positive for COVID-19 at UHL being seen later in the pandemic in January 2021 (Fig. 3). 12 Overall, there was no association found between referral to assessment time and number of COVID-19epositive patients at UHL (P ¼ 0.238).
There was an observed association between the referral to assessment time and number of COVID-19 hospital admissions in UHL for individuals who lived in Leicester (P ¼ 0.049). There was a significant association between assessment to intervention time for CLTI patients and the number of COVID-19epositive patients at UHL (P < 0.001) and the number of COVID-19 hospital admissions in UHL for individuals who lived in Leicester (P ¼ 0.001). Altogether, only 9 patients with CLTI had a positive COVID-19 test undertaken in secondary care within 30 days of assessment (1.87%).

Comparison to Pre-COVID Cohort
The incidence of MLLA at 1-year postassessment in those seen during the first year of the Vascular Limb Salvage Clinic was 9.8% (15/153 patients). This was similar to the 1-year MLLA incidence of those seen in the VEC during the COVID-19 pandemic (subdistribution hazard ratio 1.16; 95% CI 0.61, 2.04; P ¼ 0.720) (Fig. 4).

DISCUSSION
The United Kingdom was greatly impacted by the COVID-19 pandemic. Leicestershire was one of the worst affected areas across the country with 13.9% of all COVID-19epositive patients in UHL requiring a mechanical ventilation bed during our timeframe. 12 Multiple changes were implemented during the COVID-19 pandemic to cope with increased pressures placed upon services. Despite these changes, our study demonstrates that a VEC was still effective and able to meet the VSGBI ''nonadmitted'' patient timeframe. The long-standing effect of the COVID-19 pandemic is currently unknown with health experts predicting an impact on the NHS for decades to come. Changes to rapid access outpatient clinics have already been seen with an 80% reduction in referrals to urgent 2-weekewait cancer referral pathways. 16 This drastic change has been thought to occur due to a change in health-seeking behaviours alongside the Governmental ''Stay at Home and Stay Alert'' health message meaning that patients only presented to primary care with urgent concerns. 10 Poor symptom recognition due to misunderstanding of the condition or poor patient education as well as healthcare-related factors such as difficulty in accessing specialist services have been shown to result in delay in referral. 17 This poses a grave concern for patients with CLTI, as patient education remains a significant barrier to intervention, with many patients unaware of the seriousness of the disease process. 18 Additionally, vascular UK institutions reported a reduction in face-to-face appointments and increase in telephone appointments during the COVID-19 pandemic. 19 Given that less than half of all adults aged 75 years and more are recent internet users and that the prevalence of CLTI increases with age, the move to digital platform consultations could lead to significant health inequality. 20 All of these factors including the governmental advice of ''Stay at Home and Stay Alert'' may have led to the significant delay in presentation of symptoms, seen within our institution, with the mean length of symptoms reported as 12 weeks (IQR 5e26). There may have been, however, other reasons for the delay in presentation and more must be Data are presented as n (%), mean ± standard deviation or median (interquartile range). IHD, ischemic heart disease; TIA, transient ischemic attack; COPD, chronic obstructive pulmonary disease; CKD, chronic kidney disease; BMT, best medical therapy (antiplatelet + lipid lowering agent).  (4) Data are presented as n (%). AKA, above-knee amputation; TKA, through-knee amputation; BKA, below-knee amputation.
done to quantify this in a bid to improve patient outcomes.
During the peak of the COVID-19 pandemic across Lombardy, the most common vascular presentation was for those with peripheral arterial occlusive disease (59% CLTI and 41% acute limb ischemia). Interestingly, their results showed that COVID-19epositive patients were at 2.2 times increased risk of rethrombosis after revascularization. 21 Only 1.85% of our patients were positive for COVID-19 within 30 days of assessment. However, data were only available from secondary care and this does not reflect those who tested positive in the community.
Our results demonstrated that 9.8% of patients presented with significant tissue loss (Rutherford 6) compared to only 2.5% during the first year of the clinic. 6 This shows a paradigm shift of patients presenting with more severe disease progression. The results of this are similar to work published elsewhere during the COVID-19 pandemic showing patients worldwide are presenting at later stages of disease progression. 22 This is of concern given the societal and individual implications that CLTI present most noticeably that of MLLA. Moreover, a quarter of our patients with CLTI had undergone a previous endovascular procedure demonstrating an increase in disease complexity upon representation to the clinic.
Nearly two-thirds of our patients presented with minor tissue loss. This is of key importance as delayed presentation to services and revascularization is associated with increased likelihood of MLLA. 17 Our 12-month freedom from MLLA has previously been reported as 90.5%. 6 During our current timeframe, our 12-month amputation rate was 10.9% with our Kaplan-Meier estimated freedom from MLLA of 89.1% and estimated freedom from mortality of 88%. Despite extraordinary pressures, reduction in inpatient beds and reduced operating lists, VEC demonstrated resilience against the COVID-19 pandemic and maintenance of an essential service.
CLTI proves a significant cost burden for the NHS with individuals often having a prolonged hospital stay, delayed discharge planning, rehabilitation requirements, and increased readmission rates. 23 Our VEC demonstrate that certain individuals with CLTI can be managed safely and effectively in the community. The outpatient management for patients with CLTI is notoriously challenging, however, with a recent UK survey demonstrating that only 14.3% of centres provide an outpatient consultation within the 7-day referral target. 24 The success of our outpatient clinics relied on the streamlining of patient care, with individuals undergoing a ''1 stop'' clinic that provided assessment and investigations. Additionally, all patients awaiting intervention were routinely swabbed for COVID-19 and methicillin-resistant Staphylococcus aureus to facilitate the use of day case angiogram slots and admission for open surgery procedures. Where possible, patients were managed as a day case to prevent admission to secondary care negating the requirement of an inpatient bed and risk of COVID-19 infection. This approach resulted in patients being managed safely and effectively within the community and promotes a significant reduction in the cost burden associated with an inpatient stay.
Prior to the COVID-19 pandemic, our centre demonstrated a median referral to assessment time of 2 days and assessment to intervention time of 6 days. 6 Our median referral to assessment time during the COVID-19 pandemic was 3 days and assessment to intervention time of 5 days for the admitted  patient with CLTI and 8 days for the nonadmitted patient with CLTI. Despite changes to our service during the pandemic and increasing number of patients, two-thirds of our patients were still able to meet the VSGBI ''nonadmitted'' patient timeframe. Additionally, our data demonstrate that as our number of individuals being assessed increased per week, we were still able to decrease the referral to assessment timeline as the pandemic progressed. This supports that as the pandemic progressed, we were able to respond to the increasing demands placed upon our services and adapt accordingly.
The number of patients with CLTI assessed prior to the COVID-19 pandemic during the first year of the clinic being opened was 158 compared to 322 during our timeframe. 6 Initially, referrals to the clinic were limited to those from a dedicated diabetic foot clinic and from those triaged by the on-call surgical team. During the first year, as the clinic became fully established, direct referrals from primary and secondary care as well as self-referral from patients were accepted. Additionally, advertisement of the clinic pathway at local conferences led to an increase in primary care education, engagement, and referrals. During the COVID-19 pandemic, the routine outpatient vascular clinic appointments were reduced and/or cancelled resulting in an increase in patients presenting to emergency care or via the VEC pathway. Roughly, a third of all assessments in VEC were for follow-up appointments (32.5%). This included a mixture of individuals seen in clinic which required a shorter follow-up time to an ordinary clinic appointment, were reviewed following discharge from hospital, or were being brought back to a clinic to decide further treatment options. The clinic facilitated early discharge and improved  patient flow through the vascular ward. It allowed for patients to have early wound care follow-up and reduced the number of inpatients. These factors resulted in an increase in numbers seen during the COVID-19 pandemic compared with prior. However, given that we were assessing the impact of COVID-19 on our outpatient VEC, we chose to compare our results with those assessed in 2019 to avoid follow-up being affected by COVID-19.

Strengths and Limitations
Our study describes the effect that the COVID-19 pandemic had upon our VEC. It describes data from one of the largest VEC across the United Kingdom and compares this to loco-regional Governmental COVID-19 rates to determine trends. It provides a real-life single-centre approach to an unpredictable landscape and demonstrates the difficult decisions that were required to keep a CLTI service operational during the COVID-19 pandemic. However, certain limitations exist. This was a retrospective data analysis requiring data collection from electronic patient records. Despite cross-checking with other databases, we were unable to obtain referral dates for all patients. Access to past medical history and current medication was also sometimes difficult to obtain due to lack of access to primary care records. As mentioned previously, COVID-19 status within 30 days of assessment was obtained from all patients. This, however, related to UHL results only as access to community swabs was unable to be sourced.

CONCLUSION
This study demonstrates the values of a VEC service for the rapid assessment and treatment of individuals with CLTI. Using an outpatient-based model, VEC maintained adherence to national guidelines for times to treatment despite the impact of the COVID-19 on departmental and regional health services. The VEC model of care is resilient in providing services for people with CLTI during periods of wider health service strain.