The results of our study show a 1.5-fold increase in the rate of cancer patients with advanced disease at staging FDG PET/CT in 2020, following the national lockdown due to the COVID-19 pandemic, compared to 2019. In addition, we found an approximately 2-fold increase in the rate of cancer patients with nodal involvement or metastatic disease at staging, as well as in the rate of patients with a greater number of involved nodes or distant metastases. Compared to 2019, patients with lung cancer and lymphoma showed a significant (1.9 to 2.6-fold) increase in advanced disease rate at staging, nodal/extranodal involvement, metastatic status, and number of nodal stations and metastatic/extranodal sites in 2020. Additionally, gynaecological cancers showed a significant increase in advanced disease rate at staging in 2020 vs 2019 as well as gastrointestinal cancer for the rate of N + patients.
This retrospective observational study indirectly analyses the impact of the first wave of the COVID-19 pandemic and national lockdown on the extent of cancer disease at staging using whole body FDG PET/CT as a surrogate marker. Oncological FDG PET/CT is known to be the most accurate non-invasive technique for cancer staging in most histotypes because of its superiority over radiological imaging, mainly in assessing lymph node involvement and distant metastases [12]. From our data, more cancer patients showed an advanced stage of disease at staging FDG PET/CT in 2020, after the national lockdown, compared with the same reference period in 2019. An increase rate of patients with nodal involvement and metastatic disease was also demonstrated. Such increase should be mainly due to delays in accessing cancer diagnosis for many patients with the onset of the COVID-19 pandemic. The first phase of the emergency determined a reduction in inpatient and outpatient services provided to non-COVID patients i.e. the delay or suspension of important screening programs, the limitation of some diagnostic tests such as CT to the emergency context and the cancellation or delay of specialist visits and some elective procedures such as biopsies or surgeries [26–30]. Several European Countries reported that cancer diagnosis rates plummeted when the pandemic began, between 15% and 40%. In Italy, approximately 1.4 million fewer screening exams were performed in the first 5 months of 2020 compared to the same period in 2019 [31]. Surgery was the most affected modality having been delayed or cancelled in over 10% of patients in 34% of European Centers [11]. In Italy, a significant decrease (20%-50%) in the volumes of screening tests, outpatient specialist visits and oncological interventions was reported in 2020 compared to 2019, even in the geographical areas where a lower incidence of the SARS-CoV‐2 was recorded during the first wave of the pandemic [31]. In addition to the limited diagnostic capacity and hospital taking-charge patients, many subjects were reluctant to visit hospitals for fear of being infected or preferred to stay at home according to public health messages encouraging people to postpone elective care. The quarantine and financial difficulties due to lockdown had also an impact on travel and care-seeking behaviours. In fact, the incidence of cancer has not changed in recent years, and, in our context, the number of PET exams performed at our Center has not significantly changed in 2020 compared to 2019 as well as the planning of staging FDG PET/CT exams which are generally performed within 7 days of receiving the request form. We have only recorded a slight reduction in PET/CT requests for patients on treatment, due to cancellation or postponement of the examination, with a consequent greater availability of performing examinations for staging or restaging purposes.
Such delays in cancer diagnosis led to more patients being diagnosed at a more advanced stage of their disease, as demonstrated by our study. This means both that these patients could require more complex treatments than they otherwise should have and that there will be more deaths from cancer. The exact extent of the effects on survival and healthcare costs will only become evident in the next few years. After the first peak of the pandemic, forecasts on the impact of these delays on cancer diagnosis and patient survival were provided. The severity of the indirect effects of the COVID-19 pandemic was clear in November 2020 when a 4-week treatment delay was reported to be associated with a 6 to 17% increased risk of death depending on type of cancer. Delays of up to 12 weeks further increase this risk [32–35]. The real challenge now is, on the one hand, to prevent new waves of the pandemic from limiting access to cancer diagnosis and treatment and, on the other, to think of a health system that adequately responds to the needs of these advanced stage patients both during and soon post-pandemic. We hope that, with the support of all stakeholders in cancer diagnosis, treatment and health planning process, the detrimental impact of the COVID-19 pandemic on cancer patients could be mitigated.
This study has some limitations. First, its retrospective nature which indirectly allowed us to take a snapshot of real events of such an emergency period. Secondly, we focused on patients with FDG-avid tumours only and excluded other cancers such as prostate cancer or neuroendocrine tumours that are usually studied with radiopharmaceuticals other than FDG. Nevertheless, the FDG is the radiopharmaceutical most frequently used for PET and FDG-avid tumours are the most aggressive ones for which a delay in diagnosis and initiation of treatment could have the worst consequences on patients' outcome [36]. Finally, the analysis by tumour type was not feasible or the results were not significant in some tumours, mainly due to the small sample size. Further studies confirming our results are desirable, even more complex with the impact on patient outcome, survival, and healthcare costs.