With the aim of reducing referral and diagnosis intervals to improve survival in cancer patients, over the first two decades of the 2000s multiple countries in Europe created various urgent Routes to Diagnosis for Cancer (RtDC) models. The most extensively described models are the 2-week-wait (2WW) in the United Kingdom and the cancer patient pathways (CPP) in Denmark, Sweden, and Norway.1–4 Both routes select patients with organ-specific symptoms suspected to be cancer in accordance with clinical referral guidelines. A new emerging route created in Denmark, subsequently implemented in other countries due to its diagnostic yield, is the CPP for patients with non-specific symptoms and signs of cancer (NSSC-CPP).5–8 Quick diagnosis units (QDU) as an alternative to hospitalisation, despite being created to prevent unnecessary hospitalisation, share the goal of quickly diagnosing potentially serious diseases, particularly those indicative of cancer.9–11 Their efficacy as a diagnostic tool for cancer and potentially serious benign processes has been widely demonstrated.12,13

During the initial stages of the new coronavirus pandemic (SARS-CoV-2), health care activity focused on patients with the coronavirus-19 illness (COVID-19). The situation caused unprecedented disruption to care, particularly to access to care, delayed visits, care for vulnerable groups, surgical scheduling, and diagnostic processes.14–16 While the impact of the pandemic on the cancer population has been reported in short-term studies, there are few medium-term descriptions or reports from urgent RtDC, including QDU.

The objective of this study was to analyse the impact, after two years of the pandemic, on the volume of registries, referral and diagnosis times, incidence and stages of patients with cancer and diagnoses of benign diseases.

A total of 3184 patients were recorded during the three-year study. A total of 147 (3.1%) were excluded, 91 due to the need for hospitalisation, 53 due to losses and 3 died, resulting in a final study population of 3037 patients (Fig. 1).

Figure 1.

Study flow chart.

(0.15MB).

Referrals decreased by 4.2% in the FYP and increased by 17.7% in the SYP. A decrease in referrals was only observed in the first wave (-32.6%), with an increase of 8.1% between the second wave and the end of the FYP. The general characteristics are listed in Table 2. Over the two years of the pandemic, there was a sustained increase in the FVI and PC referrals and a decrease in emergency referrals. In the FYP, there was a decrease in patients from the CRC screening program who required an endoscopic exam (−73.3%) and CRC diagnoses via this route (−68.7%), with an incomplete recovery (−14.7%) observed in the SYP compared to the PPY.

Suspected CRC, anaemia, and radiological alterations indicative of malignancy were the main reasons for consultation, representing ∼60% of the patients. The most common diseases were: digestive (44–46.5 %), pulmonary (11.8–14.2 %), haematological (5.7–7.8 %), and infectious (5.2−8.1%). Digestive tract tumours, anaemia due to digestive losses, and blood disorders were the most common benign processes.

Patients diagnosed with cancer increased during the two pandemic years (FYP: +2.7%; SYP: +15.7%), exceeding the PPY rate (18.7%) with 20% in the FYP and 19.2% in the SYP. The conversion rates for the main reasons for consultation were: suspected CRC (16–25.7 %), suspected lung cancer (36.5–42.1 %), and radiological alterations indicative of malignancy (22.3–36.4 %). Table 3 details the characteristics of this patient group. In the FYP there was a significant increase in referrals from PC and a reduction in referrals from CRC screening and emergency referrals. The median FVI saw an increase in the FYP and an incomplete recovery in the SYP. In the three years of the study, the mean FVI was lower in patients with cancer (PPY: 8±5.04 days vs. 10.09±6.27 days: p<0.0001; FYP: 10.56±6.38 days vs. 13.53±8.79 days: p<0.0001; SYP: 9.16±5.85 days vs. 12.91±10.1 days: p<0.0001). No variations were observed in the reason for referrals and the cancer locations. In terms of stages, the only significant finding was the reduction of stage 0 CRC in the FYP. While the DI increased in the SYP, the median did not exceed 15 days. In patients with cancer, the mean DI was shorter than for benign processes (PPY: 15.44 days vs. 18.25 days: p=0.060; FYP: 14.03 days vs. 21.61 days: p<0.0001; SYP: 17.65 days vs. 19.53 days: p=0.181). The interval times according to the main locations are listed in Table 4. In the majority of locations, the FVI increased during the FYP and recovered in the SYP. A DI>15 days was only identified in lung cancer and lymphoproliferative syndromes. With the exception of lymphoproliferative syndromes, the median FVDI was less than 28 days.

The interpretation of the results must be contextualised within the setting of a regional study at a multidisciplinary QDU over a two-year period. Our study features various aspects of interest. On the one hand, it offers the possibility to highlight the benefits of urgent use of RtDC and, on the other hand, to evaluate and compare with similar studies the changes attributable to the pandemic in terms of volume and source of referrals, diagnostic cancer yield, and delays in intervals.

In 2012 Ellis-Brookes et al.18, in a study with 739,667 patients with cancer (2006−2008) taken from the United Kingdom National Cancer Data Repository, categorised RtDC into 8 groups: screening, emergency PC referrals in the 2WW route, emergency, regular or emergency PC referrals not following the 2WW route, hospitalisation, outpatient, death certificate, and unknown. The study identified three predominant routes, the 2WW (26%), emergency (24%), and PC referrals not following the 2WW route (21%). In 2021 Danckert et al.19 in a study of 144,635 cases from the Danish cancer registry (2014–2017), modified the original categorisation by adding two emergency routes, which included CPPs and NSSC-CPPs in patients referred from PC and SC, and replacing the emergency route with unplanned hospital admission due to acute processes in the 30 days prior to cancer diagnosis. In the study it was observed that 66.3% of patients had followed an emergency route, 46.2% were referred from PC, and 20.1% from SC. Both authors agreed on the variability of prognosis according to the route followed, reporting higher mortality in the emergency route (20–40 %)18 and in the unplanned hospitalisation (53%) and unknown routes (33,7%), as compared to the urgent PC (15.6%) and SC routes (22.6%).19

The diagnostic yield shows differences according to the RtDC model. Due to the strict referral criteria and variability in compliance, the 2WW route is the organ-specific CPP with the lowest conversion rate (8–11%).15 On the other hand, in the NSSC-CPP route, rates between 7 and 12% have been reported in the United Kingdom and 11–22.1% in Scandinavian countries. The Danish model stands out due to its higher predictive value as it includes an initial study phase in PC with computed tomography.5–8 By including non-specific and specific signs and symptoms among the reasons for referral, QDUs achieve higher conversion rates (19–26.4%) than most urgent RtDC.10,11

Different studies during the first two waves of the pandemic confirmed serious disruption in cancer care, including decreases in new diagnoses, treatment delays, fewer clinical trials, and fewer participants in screening programs.15,16,20 In a systematic review, Riera et al.16 reported a decrease of between 10 and 78% in the number of expected new cases. While the trend after two years of pandemic has been one of gradual recovery, recent studies show that pre-pandemic numbers have not yet been reached.16,21,22 Ribes et al.21 described in the Catalan pathology registry from March 2020 to January 2022 a 12% decrease in new diagnoses compared to the pre-pandemic period.

The impact of the SARS-CoV-2 pandemic on QDUs has only been reported in one Barcelona university hospital by Bosch et al.23–25 Two short-term studies confirmed a decrease in PC referrals during the lockdown period (36.6%) and in cancer diagnoses in patients coming from PC (-54%) and emergency routes compared to the pre-pandemic period (5.7% vs. 21.3%).23,24 These data are similar to those reported in various other studies of rapid diagnosis routes for cancer during the first two waves of the pandemic.26–30 While our results are similar to those reported in the first wave, they differ starting with the second wave, when an increase in cancer referrals and diagnoses was observed. This may be attributable to delays in identifying and referring potentially severe processes during the lockdown period, redirecting patients who under other circumstances would have followed other diagnostic routes, and the accessibility of the unit.

The decrease in participants in the CRC screening program coincides with that observed in the Mazidimoradi et al.31 systematic review, which quantified the decrease at between 28–100%, with full operational capacity only maintained at 2–2.5% of centres.

The diagnostic yield in suspected CRC and lung cancer falls in line with the quick diagnosis pathways in Catalonia, which reported rates between 28.7% and 40% in CRC and 40.2% and 51.5% in lung cancer.32 Studies conducted during the first waves showed an increase in stages, although some showed a later trend towards recovery.25,33–35 Bosch et al.25 observed a higher proportion of stage IV disease in pancreas, lung and stomach cancers limited to the second and third wave. The lack of variation in stages in our cancer population, although of undeniable value in lung and CRC, must be interpreted with caution due to the length of the study and the low incidence of diverse locations such as the pancreas, head and neck, and cancer of unknown primary origin.

In patients with cancer, extended interval times are associated with more advanced stages and higher mortality.36 We agree with the study from Bosch et al.25 on the change in all these intervals. Despite the increase in DI, the global median was below the standard (≤15 days) recommended by our National Healthcare System.17 The 15 days was only surpassed in lung cancer and lymphoproliferative syndromes, locations that tend to require broader staging. The small increase in DI was due to prioritising, due to its high predictive value, the three primary reasons for referral (suspected CRC, suspected lung cancer, and radiological alterations indicative of malignancy) which tend to represent ∼60% of all cancers. For the majority of the locations, even during the pandemic period, our FVDI was shorter than those reported by Petrova et al.36 in a broad meta-analysis on intervals in patients with cancer conducted prior to the pandemic.

The efficacy and efficiency of QDUs has been widely verified.9–12,37–39 Our study corroborates its use as an alternative to hospitalisation and as a route for patients with suspected cancer thanks to its diagnostic yield, even during the pandemic.

The main study limitations where its length in terms of the still uncertain evolution of the pandemic, and the comparison of the data with the only QDU that reported impact and with cancer registries that do not detail the diagnosis routes used. The bias attributable to the low number of exclusions represents a relative limitation in the interpretation of the results. It was not possible to compare and correlate the changes identified in the study with those that occurred in the overall care provided at our centre (hospitalisation, external consultations, and emergency), which would have enabled an improved evaluation of the trends of the parameters analysed in relation to the total population seen at the hospital.

In conclusion, the pandemic did not produce significant clinical changes, with the exception of a higher proportion of cancer diagnoses due to the increase in referrals starting in the second wave. We consider the increase in PC referrals, to the detriment of the emergency route, to be relevant due to its prognostic significance, should the trend continue. Despite the increase in the time intervals, the DI always stayed within the recommended standards. The study verifies the participation and consolidation of QDUs as urgent RtDC, representing a diagnostic route that supplements those already established by the national health systems.

This study was conducted in compliance with the World Medical Association Code of Ethics (Declaration of Helsinki), the ethics of scientific publishing, and with the approval of the relevant Clinical Research Ethics Committee.

This research did not receive any specific funding from agencies from the public sector, commercial sector, or not-for-profit organisations.

The authors declare that they do not have any conflicts of interest.