Abstract
Aim: This study retrospectively analyses the impact of the 1st year of the COVID-19 pandemic on route of presentation and staging in lung cancer compared to the 2 years before and after implementation of the Leicester Optimal Lung Cancer Pathway (LOLCP) in Leicester, United Kingdom. Method: Electronic databases and hospital records were used to identify all patients diagnosed with lung cancer in 2018 (pre-LOLCP), 2019 (post-LOLCP), and March 2020–2021 (post-COVID-19 lockdown). Information regarding patient characteristics, performance status, stage, and route of diagnosis was documented and analysed. Emergency presentation was defined as diagnosis of new lung cancer being made after unscheduled attendance to urgent or emergency care facility. Results: Following implementation of the LOLCP pathway, there was a significant decrease in emergency presentations from 26.8 to 19.6% (p = 0.002) with a stage shift from 33.9% early stage disease to 40.3%. These improved outcomes were annulled during the COVID-19 pandemic, with emergency presentations increasing to 38.9% (p < 0.001) and a reduction in early-stage lung cancer diagnoses to 31.5%. There was a 61% decline in 2 week wait referrals but no significant decline in the LOLCP direct-to-CT referrals. Conclusion: We have demonstrated a significant increase in late-stage lung cancer diagnoses and emergency presentations during the first year of the COVID-19 pandemic. The causes for these changes are likely to be multifactorial. The long-term effect on lung cancer mortality remains to be seen and is an important focus of future study.
Keywords: lung cancer, covid-19, optimal lung cancer pathway, lung cancer emergency presentations, referral pathway
Introduction
A significant number of lung cancer patients are first diagnosed after an emergency presentation to medical services. The UK has some of the worst lung cancer survival rates in Europe which may be due to patients presenting late, often as an emergency. 1 According to the UK National Clinical Intelligence Network report (2012), 40% of lung cancer patients were diagnosed via an emergency attendance, one of highest proportions for any tumour type. 2 Lung cancer emergency presentation is associated with advanced stage of disease, older age, increased co-morbidities and is a negative predictor for survival with increased healthcare costs.3,4
The National Optimal Lung Cancer Pathway (NOLCP) incorporates protocol-led triaging of lung cancer referrals, daily rapid access lung cancer clinics and faster turnaround times for all investigations aiming for a target of 28 days for diagnosis and 49 days for treatment of lung cancer. 5 The intended benefit of the NOLCP is to shorten the time to diagnosis, with the consequent additional benefit of lower ‘tumour, node, metastases’ (TNM) stage and better Eastern Cooperative Oncology Group (ECOG) performance status at diagnosis. Higher functional status improves eligibility for curative and systemic anticancer treatment, as well as reduces need for emergency hospitalisation. 4 Reducing lung cancer emergency presentation is therefore an important strategy for improving lung cancer survival, in conformity with the UK Lung Cancer Coalition’s (UKLCC) goal to improve 5-year lung cancer survival to 25% by 2025. 6
The Leicester Optimal Lung Cancer Pathway (LOLCP) was implemented in January 2019, reaching a population of 1.1 million people across the University Hospitals of Leicester (UHL) NHS Trust, a tertiary referral centre in the United Kingdom. The UHL NHS Trust operates across three sites, with Glenfield Hospital serving as the main hub for Respiratory Medicine and lung cancer care.
The LOLCP is the local adaptation of the NOLCP, and has a complex structure with multiple referral routes and a daily lung cancer triage meeting as its central component. The multidisciplinary triage team lead by a consultant respiratory physician reviews all lung cancer referrals within one working day and determines the plan for further investigation and review.
Community-based referrals arrive via two routes. The first is through the 2-week wait pathway, a national standard where cases of suspected cancer are referred urgently to specialist care with a 14-day target to first review from referral. The second is a direct-to-CT pathway, whereby patients with abnormal chest X-rays suggestive of lung cancer are automatically scheduled for CT, bypassing the need for GP review and 2-week-wait referral. The latter group of patients are assessed by a lung cancer specialist nurse at the time of CT scan. Any patient who requires further urgent review based on their symptoms and CT findings is seen by a respiratory physician on the same day. The daily triage meeting also reviews in-hospital referrals from the three sites across the Trust, guiding inpatient management and arranging prompt outpatient review to facilitate discharge planning.
After being virtually reviewed in triage meeting, patients are either discharged, given urgent Rapid Access Clinic appointments, or are diverted to the appropriate outpatient service depending on their CT result. Following review in rapid access lung cancer clinic and the relevant diagnostic tests, lung cancer patients are discussed at a weekly multidisciplinary team meeting (MDT) to devise an appropriate treatment plan. Figure 1 demonstrates flow of referrals along the LOLCP pathway.
Figure 1.
Leicester optimal lung cancer pathway structure.
The emergence of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) at the beginning of 2020 and the impact of the subsequent COVID-19 pandemic on the care of patients with lung cancer has been unclear. There have been significant changes in primary and secondary care services and the “stay at home, save lives, protect the NHS” messaging at the start of COVID-19 pandemic may have impacted healthcare seeking behaviours. The UKLCC has raised serious concerns about the adverse effects of the COVID-19 pandemic on survival and quality of life of lung cancer patients. 7 Moreover, due to local COVID-19 outbreaks, Leicester went through one of the longest lockdown periods in the United Kingdom.
Following the onset of the COVID-19 pandemic, the LOLCP structure remained unchanged, with daily triage meetings and lung cancer specialist nurse reviews at CT.
Our aim was to study the impact of the rapid and significant changes in service structure over three consecutive years on the route of presentation of lung cancer patients, in order to determine whether the LOLCP had a positive effect on emergency presentation rate both in normal operation and in a period of healthcare crisis.
Method
This is a single centre, observational follow-up study of all patients diagnosed with lung cancer between 1st January 2018 and 31st December 2019 and then for 1 year following the first COVID-19 lockdown on 23rd March 2020. The study was registered as a Service Evaluation Project with the local Clinical Audit team in accordance with local research governance policy, which waived the formal requirement for Research Ethics Committee approval.
Patients were recruited from our lung cancer database for three 1-year study periods: pre-LOLCP implementation (January-December 2018), post-LOLCP implementation (January-December 2019), and post-first COVID-19 UK lockdown (23rd March 2020–22nd March 2021). The lung cancer database takes into account all patients with MDT diagnosis of lung cancer from community referrals as well as in-hospital referrals from the three hospitals across the UHL NHS Trust. The local database is shared nationally for use in the UK National Lung Cancer Audit.
All patients with a new diagnosis of primary lung cancer were included. Exclusion criteria were lung cancer recurrences, and extra-pulmonary cancer, including mesothelioma.
Emergency presentation of a patient with lung cancer was defined as the diagnosis of new lung cancer made because of unscheduled attendance to an urgent or emergency care facility with symptoms directly related to the primary malignancy. ‘Elective’ referrals included scheduled urgent 2-week-wait and direct-to-CT pathway referrals as well as inpatient referrals for incidental lung cancer diagnoses during admissions for other pathology.
Data collected from the lung cancer database and electronic hospital records included demographic data on age and sex, baseline Eastern Cooperative Oncology Group (ECOG) performance status, and TNM staging. 8 Lung cancer is largely deemed treatable with curative intent when presenting in stages I-IIIA, and any stage IIIB or higher is arbitrarily deemed advanced-stage. 9 In order to facilitate statistical analysis, patients were divided into early-stage and advanced-stage groups.
Data from 2019 post-LOLCP implementation and post-COVID-19 lockdown was additionally reviewed for source of referral. This was not possible for the 2018 group as complete data for this was not captured locally prior to LOLCP implementation.
Statistical analysis
Following compilation, data was broken down into three groups spanning the study periods of pre-LOLCP implementation (1st January–31st December 2018), post-LOLCP (1st January–31st December 2019), and the year following the first COVID-19 UK lockdown (23rd March 2020–22nd March 2021). Each group was analysed for percentage proportions of emergency presentations within each period, as well as mean age, and sex and performance status distribution. ECOG performance status was grouped into 0–1, which indicates favourability for treatment, borderline performance status of 2, poor performance status of 3–4 which generally precludes active treatment, and 5, denoting patient death.
Data was further analysed for statistical significance using Microsoft Excel and SPSS software. The chi-square test was used to compare the ECOG performance status, TNM lung cancer staging and proportion of emergency presentations during all three periods. A significant p value was set at 0.05.
Results
The demographic characteristics of patients diagnosed with lung cancer during the three study periods are presented in Table 1. Patients were well-matched for age and sex across all routes of presentation. The proportion of patients having a favourable ECOG performance status (PS) of 0–1 was lower in the emergency presentation group compared to the elective route.
Table 1.
Study population characteristics.
| Year 2018 | Year 2019 | Post-COVID-19 lockdown a | |||||||
|---|---|---|---|---|---|---|---|---|---|
| Total | EP b | Elective | Total | EP | Elective | Total | EP | Elective | |
| No. of patients – n (%) | 604 | 162 (26.8) | 442 (73.2) | 667 | 131 (19.6) | 536 (80.4) | 447 | 174 (38.9) | 273 (61.1) |
| Male – n (%) | 340 (56.3) | 91 (56.2) | 249 (56.3) | 375 (56.2) | 75 (57.3) | 296 (55.2) | 254 (56.8) | 93 (56.3) | 156 (57.1) |
| Mean age (y) | 72.3 | 71.7 | 72.6 | 73 | 73.7 | 72.8 | 73.6 | 72.9 | 74 |
| ECOG PS | |||||||||
| 0–1 – n (%) | 266 (44) | 50 (30.9) | 216 (48.9) | 284 (42.6) | 35 (26.7) | 249 (46.5) | 181 (40.5) | 47 (27) | 134 (50.2) |
| 2 – n (%) | 96 (15.9) | 16 (9.9) | 80 (18.1) | 120 (18) | 24 (18.3) | 96 (17.9) | 94 (21) | 39 (22.4) | 55 (20.1) |
| 3–4 – n (%) | 209 | 80 (49.4) | 129 (29.2) | 235 (35.2) | 66 (50.1) | 169 (31.5) | 153 (34.2) | 80 (46) | 73 (26.7) |
| 5 – n (%) | 5 (0.8) | 5 (3.1) | 0 (0) | 11 (1.6) | 2 (15.3) | 9 (1.7) | 6 (1.3) | 4 (2.3) | 2 (0.7) |
| Not recorded – n (%) | 28 (4.6) | 11 (6.8) | 17 (3.8) | 17 (2.5) | 4 (3.1) | 13 (2.4) | 13 (2) | 4 (2.3) | 9 (3.3) |
| TNM8 stage | |||||||||
| IA-IIIA – n (%) | 205 (33.9) | 14 (8.6) | 191 (43.2) | 269 (40.3) | 13 (9.9) | 256 (47.8) | 141 (31.5) | 21 (12.1) | 120 (44) |
| IIIB-IVB – n (%) | 396 (65.6) | 148 (91.4) | 248 (56.1) | 393 (58.9) | 118 (90.1) | 275 (51.3) | 299 (66.9) | 150 (86.2) | 149 (54.6) |
| Not recorded | 3 (0.5) | 0 (0) | 3 (0.7) | 5 (0.7) | 0 (0) | 5 (0.9) | 7 (1.6) | 3 (1.7) | 4 (1.5) |
a23rd March 2020 – 22nd March 2021.
bEP: Emergency presentation.
A marked decrease in total number of lung cancer presentations can be appreciated in the year following onset of the COVID-19 pandemic, with 447 presentations accounting for 67% of the numbers seen in the year 2019.
Route of referral
In 2018, emergency presentations accounted for 26.8% of all lung cancer referrals, with a significant drop to 19.6% of total referrals in 2019 (p = 0.002). During the COVID-19 pandemic, this increased to 38.9% despite no disruption to our LOLCP pathway, as lung cancer services were preserved during the pandemic. This is significantly higher than emergency presentations seen both before (p < 0.001) and after (p < 0.001) the implementation of the LOLCP. Figure 1 shows the proportion of emergency cases compared to absolute numbers of lung cancer diagnoses by year.
Table 2 shows the results of analysis of referral source within the context of the LOLCP pathway pre- and post-pandemic. The percentage of 2-week-wait referrals fell almost by half following the start of the pandemic (p < 0.001). The proportion of direct-to-CT pathway patients did not significantly change, despite the absolute drop in service referrals. There was a significant increase in referrals originating from hospital, irrespective of whether directly related to lung cancer, from 39.9 to 53% (p < 0.001).
Table 2.
Analysis of referral sources in 2019 and post-COVID-19 lockdown groups.
| 2019 | Post-COVID-19 lockdown a | ||
|---|---|---|---|
| Two week wait | 121 (18.1%) | 43 (9.6%) | p < 0.001 |
| Direct to CT pathway | 134 (20.1%) | 85 (19%) | p = 0.66 |
| Hospital outpatient referrals | 131 (19.6%) | 72 (16.1%) | p = 0.13 |
| Hospital inpatient referrals of which emergency presentations | 266 (39.9%) | 237 (53%) | p < 0.001 |
| 131 | 174 | ||
| Data unavailable | 15 (2.2%) | 10 (2.2%) |
a23rd March 2020 – 22nd March 2021.
Lung cancer stage
In 2018, 33.9% of patients presented with early-stage lung cancer. This showed a statistically significant improvement to 40.3% in 2019 (p = 0.017) following implementation of the LOLCP pathway. In the year following COVID-19 lockdown, the proportion of early-stage lung cancer was seen to drop to 31.5% (p = 0.005), with no significant difference between post-COVID-19 and pre-LOLCP implementation (p = 0.52).
Discussion
To the authors’ knowledge, this is the only study that specifically looks at the impact of the COVID-19 pandemic early after uptake of the NOLCP in a tertiary referral centre. Following the start of the LOLCP, there was a statistically significant 31% decrease in emergency lung cancer presentations from 2018 to 2019 in our centre together with a significant increase in early-stage lung cancers. We believe that this downstaging is in part due to the lower emergency presentation rate, as in line with other studies, we demonstrated a higher stage and lower performance status in patients presenting via the emergency route.4,10
After the emergence of the SARS-CoV-2 pandemic we noted a 66% increase in emergency presentation rates, at levels exceeding those documented prior to the local implementation of the LOLCP, and a very worrying dip in the total number of cancer diagnoses. An analysis of 13,400 cancer-related emergency presentations in Northern Ireland from 2017 to 2020 demonstrated a decrease in absolute numbers of hospitalisations from cancer, with a 14.7% decline in lung cancer emergency presentations compared to pre-pandemic numbers. 11 Our study shows a different phenomenon, whereby there was an overall drop in cancer diagnoses but an increase in the absolute numbers of emergency presentations.
At first glance, this increase in emergency presentation is a worrying reversal of the LOLCP benefits, but we think there is a bigger picture to appreciate.
The high emergency presentation rate might be due to several reasons. Patients may have been reluctant to engage with the healthcare sector over fears of contracting COVID-19. There may also have been hesitancy to access primary healthcare due to the perception that resources were better served being directed towards the pandemic effort. Due to the overlap of some lung cancer symptoms with COVID-19, patients may have attributed red flag symptoms to infection. Shielding precautions may have led to isolation of patients from relatives who may have recognised lung cancer symptoms earlier. The strategic use of digital-based consultations was an excellent tool for maintaining primary healthcare service provision 12 but may have led to inequalities in accessing healthcare. Furthermore, a reduction in the number of people undergoing elective cross-sectional imaging for unrelated causes might have led to less patients being referred with an incidental finding of lung cancer.
Analysis of referral sources confirms the significant decline in two-week-wait referrals which reflects the immense strain on primary healthcare caused by the pandemic as well as a possible shift in healthcare-seeking behaviour. The data also shows that in the context of increased primary healthcare traffic, the direct-to-CT pathway reduces pressure on community GPs by being an additional safeguard measure and ensuring timely referral to cancer services.
Given the increase in emergency presentations following the start of the first wave, it is unsurprising that we have also noticed a significant stage shift towards advanced lung cancer presentations to pre-LOLCP implementation rates. The study demonstrates the usefulness of the NOLCP in decreasing advanced lung cancer rates, with a 10% decrease in just 1 year post-implementation in the absence of a local lung cancer screening programme.
We acknowledge that our study had a number of weaknesses. Firstly, this is a retrospective analysis relying on data obtained from the MDT database. Due to the retrospective nature of data collection, there were some gaps in the captured data. This especially limited our ability to compare referral pathways in 2018, when data collection within our service was not as robust as the period following LOLCP implementation. This gap also prevented further analysis and comparison of data regarding treatment decision, which would have provided additional insight into the impact of NOLCP implementation and the COVID pandemic on the whole trajectory of lung cancer care.
This study has not investigated mortality as it was deemed too premature to comment just 1 year post-lockdown. However, in a population-based modelling study in the UK, 1235 to 1372 additional lung cancer-related deaths due to the COVID-19 pandemic are predicted, signifying a 4.8–5.3% excess mortality over next 5 years mainly due to delays in diagnosis. 13
We predict that the increased emergency presentations and later diagnoses of lung cancer due to COVID-19 will potentially lead to increased pressure on already stretched emergency services, poorer lung cancer survival rates and increased healthcare costs. There is no single and easy solution to reduce the complex problem of emergency admissions with lung cancer. Multiple strategies are required including public health campaigns, faster and streamlined lung cancer pathways, implementation of a nationwide lung cancer screening programme10,14 and equitable access to all diagnostic and treatment modalities. Certainly, we have noticed a significant improvement in early lung cancer diagnoses and reduction in emergency presentations following implementation of the LOLCP.
This study demonstrates a decline in overall number of lung cancer presentations in the first wave of the COVID-19 pandemic together significant increase in emergency and advanced-stage presentations, comparable to numbers seen prior to the implementation of the NOLCP pathway locally. This study reinforces the strength of the NOLCP in reducing emergency presentation in lung cancer and suggests that it may have been a mitigating factor in the local response to the pandemic. Further long-term analysis of the impact of COVID-19 on lung cancer diagnosis and outcomes remains to emerge.
Acknowledgements
We would like to thank lung cancer team at Glenfield hospital especially Professor Samreen Ahmed, Dr Neil Greening, Mr Apostolos Nakas, Mr Muhammed Fiyaz Chowdhry, Dr Rakesh Panchal, Dr Cathy Richards, Dr Sridhar Thiagarajan, Dr Indrajeet Das and Dr Prajakta Pingley for technical editing and proofreading.
Footnotes
Author contributions: CV, WP, AA, and SAJ were responsible for acquisition and analysis of data. All authors (MT, CV, WP, AA, SA, RS, SAG, JB) contributed to design, interpretation and writing of the work.
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
ORCID iDs
Claire Vella https://orcid.org/0000-0002-1965-5408
Syed Ajmal https://orcid.org/0000-0001-6048-9424
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