key: cord-0969096-faovzb92 authors: Johansson, Anna L. V.; Larønningen, Siri; Skovlund, Charlotte Wessel; Kristiansen, Marnar Fríðheim; Mørch, Lina Steinrud; Friis, Søren; Johannesen, Tom Børge; Myklebust, Tor Åge; Skog, Anna; Pettersson, David; Birgisson, Helgi; Virtanen, Anni; Malila, Nea; Pitkäniemi, Janne; Tanskanen, Tomas; Tryggvadóttir, Laufey; Ursin, Giske; Lambe, Mats title: The impact of the COVID‐19 pandemic on cancer diagnosis based on pathology notifications: A comparison across the Nordic countries during 2020 date: 2022-04-25 journal: Int J Cancer DOI: 10.1002/ijc.34029 sha: b7ce8f89081ba34cd2deb5da7eb2aee917a3eebb doc_id: 969096 cord_uid: faovzb92 The severity of the COVID‐19 pandemic and subsequent mitigation strategies have varied across the Nordic countries. In a joint Nordic population‐based effort, we compared patterns of new cancer cases and notifications between the Nordic countries during 2020. We used pathology notifications to cancer registries in Denmark, the Faroe Islands, Finland, Iceland, Norway and Sweden to determine monthly numbers of pathology notifications of malignant and in situ tumours from January to December 2020 compared to 2019 (2017‐2019 for Iceland and the Faroe Islands). We compared new cancer cases per month based on unique individuals with pathology notifications. In April and May 2020, the numbers of new malignant cases declined in all Nordic countries, except the Faroe Islands, compared to previous year(s). The largest reduction was observed in Sweden (May: −31.2%, 95% CI −33.9, −28.3), followed by significant declines in Finland, Denmark and Norway, and a nonsignificant decline in Iceland. In Denmark, Norway, Sweden and Finland the reporting rates during the second half of 2020 rose to almost the same level as in 2019. However, in Sweden and Finland, the increase did not compensate for the spring decline (annual reduction −6.2% and −3.6%, respectively). Overall, similar patterns were observed for in situ tumours. The COVID‐19 pandemic led to a decline in rates of new cancer cases in Sweden, Finland, Denmark and Norway, with the most pronounced reduction in Sweden. Possible explanations include the severity of the pandemic, temporary halting of screening activities and changes in healthcare seeking behaviour. The COVID-19 pandemic has had profound global impacts on public health and delivery of healthcare, including reports of fewer patients seeking care for life-threatening conditions. 1 For cancer, there have been reports of declines in number of newly diagnosed cases during the pandemic, patterns that are likely to reflect postponement of seeking healthcare, lower diagnostic activity and lower attendance in outreach screening programmes. [2] [3] [4] Several countries temporarily halted screening activities in the first half of 2020, with effects on rates of newly diagnosed cancer cases. 2, [5] [6] [7] [8] [9] Pandemic mitigation efforts, including bans on large gatherings and closing of schools, workplaces and restaurants, were implemented to varying degrees in all Nordic countries (Denmark, Norway, Sweden, Finland, Iceland and the Faroe Islands) in March 2020 following the first reported COVID-19 cases (Table S1 ). In Across the Nordic countries, there were marked differences in COVID-19 incidence, hospitalisations and deaths during 2020 (Table S2) . Although testing strategies differed between the countries, Sweden had markedly higher rates of infection, hospitalisation and mortality than the other Nordic countries. By the end of 2020, more than 9800 COVID-19 related deaths were reported in Sweden corresponding to a mortality rate of 97.2 per 100 000 compared to 22 .4 (Denmark), 11.4 (Finland), 8.5 (Norway), 8.5 (Iceland) and 1.7 (the Faroe Islands) ( Table S2 ). The Nordic region has a combined population of 27.2 million with an annual number of new cancer cases of 179 166 in 2019 and the five most common cancers being prostate, breast, colorectal, hematologic and lung cancer ( Table 1 ). All Nordic countries have similar taxfunded healthcare systems, with universal access to care for all residents, including national screening programmes for breast and cervical cancer (and colorectal cancer in Denmark, the Faroe Islands and regionally in Sweden). During March-April 2020, screening activities were fully or partly halted due to impact of the pandemic in Norway, Sweden and Iceland, while they remained operational although with lower attendance rates in Denmark and Finland. The Faroe Islands reported no reductions in either screening activities or attendance during 2020. Since the pandemic has had profound affects across all levels of healthcare, we aimed to assess both the impact on diagnostic activity and new cancer cases using data from pathology notifications. The aim of our study was therefore to compare patterns of cancer notifications and new cases during 2020, the first year of the COVID-19 pandemic, across the Nordic countries that experienced marked differences in COVID-19 infection rates and related deaths. For this purpose, we took advantage of similar systems for collection of high quality population-based cancer registry data in the Nordic region. 10 In this population-based study, we used pathology notifications to assess patterns of diagnostic activity and new cancer cases during 2020 in the Nordic countries. For this purpose, we used two separate measures: the "number of notifications" as an indicator of diagnostic activity and the "number of new cases" as an indicator of incidence. It should be noted that a case definition based on pathology notifications is not the same as the definition used in official cancer incidence statistics that is based on additional notifications other than pathology and includes additional quality assurance. 10 Hence, in the present study the 'number of new cases' represents a proxy for cancer incidence. In all Nordic countries, the law mandates notification of cancer to the national cancer registries. Cancer notifications originate from several clinical sources of which pathology notifications represent the most rapid data source reaching the cancer registries. 10 The pathology notifications are based on cytology (including fine needle biopsy and other malignant cytology), biopsies (including core biopsy, true cut and excisions) and surgery. We included pathology notifications to the Nordic national cancer registries covering 100% of the population in Denmark, the Faroe Islands, Finland, Iceland and Norway from January 1, 2020 until December 31, 2020. For Sweden, where national cancer registration is decentralised to six Regional Cancer Centers, we included pathology notifications from 15 out of 31 laboratories with electronic reporting (covering approximately 55% of population), and pathological and/or clinical notifications (to cover 100% of population) to estimate new cancer cases during 2020 (Table S3). The comparison period was from January until December 2019 for all countries except for Iceland and the Faroe Islands where average numbers across 2017 to 2019 were used to reduce random variation due to low numbers. During diagnostic work-up, one cancer case may generate several pathology notifications. We used two separate counts of pathology notifications to describe the diagnostic activity and the number of new cases (Table S3) . First, the "number of notifications" per month was counted as all pathology notifications in a given month (regardless of previous history of cancer or previous notifications in these individuals .012 Mar À2.0 (À10.8, 7.8) À19. .216 TOTAL Jan-Dec The cumulative deficit of new malignant cases and notifications to the Nordic cancer registries across months in 2020 compared to a reference year was largest in Sweden, followed by Finland (Figure 2 ). At the end of 2020, the total decline in new malignant cases in Sweden was À6.2% (95% CI À7.2, À5.1) and À3.6% (À5.1, À2.1) in Finland, while there was no deficit in Denmark, Norway and the Faroe Islands, and a nonsignificant surplus in Iceland (+4.2%; À2.4, 11.3) ( Table 2 ). The cumulative deficit of new in situ cases was also largest in Sweden, with a total decline at the end of 2020 of À10.9% (À12.3, À9.4) . The underlying reported monthly numbers are presented in Figures S1 and S2 . To assess how the percentage change influenced absolute numbers of new cases and notifications to the Nordic cancer registries, the total annual numbers and percentage change by sex and age groups are presented in Table 3 and Due to demographic shifts, the number of cancer cases is expected to rise between 1.2% and 2.2% in the Nordic countries each year. 11 At the end of 2020, reporting in Sweden had not compensated for the spring deficit leading to an overall À6.2% decline in malignant cases for the entire year despite an expected annual increase of around 1.4%. In Denmark and Norway, with an expected yearly increase of around 1.6% to 2.2%, the reporting is unlikely to have been fully recovered since the yearly accumulated reporting ended around 0% to 1%. In Iceland, we observed a complete recovery with an increase in cancer reporting of 4.2% that was higher than expected. In Finland, with an expected annual increase of around 1.4%, the annual deficit was À3.6%. The overall patterns of reported notifications followed the patterns for cases, indicating that the reductions are likely to reflect fewer patients seeking care, reduced screening and lower attendance. Fewer patients seeking care will likely mostly affect the detection of malignant tumours, while lower screening activity will have the highest impact on in situ diagnoses and early stage invasive tumours. However, in all countries, the overall patterns of reporting during 2020 was similar for malignant and in situ tumours. Of special note was that the in situ reporting in Sweden during the autumn of 2020 was markedly lower than the reporting of malignant tumours. While the available data did not allow for a direct assessment of Declines were also observed in other Nordic countries. 14,15 Our findings corroborate previous reports of cancer reporting patterns in the Nordic countries and are also broadly in line with results from other countries. [16] [17] [18] [19] [20] [21] [22] In both Europe and the United States, there have been reports of marked reductions in the number of newly diagnosed cancer cases, particularly during the first phase of the pandemic between March and May 2, 2020, 4, 6, 8, 9, [23] [24] [25] [26] [27] [28] [29] [30] Only a few studies have compared the stage distribution of newly diagnosed cancer before, during and following the first wave of the pandemic. In the Netherlands, marked reductions were observed for in situ (cTis, DCIS) and early stage (cT1, stage I) breast tumours early in the pandemic with no evidence of a shift to advanced stage breast cancer in early autumn 2020 following restart of screening. 33 Similarly, Dutch data on colorectal cancer found decreases in incidence, particularly for stage I tumours. 34 From the UK, a shift towards more advanced breast cancer stages was reported between May and October 2020 after a substantial drop from 43.8% to 9.2% screendetected cases compared to 2019. 35 Another study from the UK reported reductions in number of low-stage cases of cervical cancer in the early phase of 2020, 36 while no difference in pathological stage of skin cancer was found in the autumn of 2020 (Oct-Dec) when referral rates where back to normal levels. 37 In Denmark, a recent study did not find any significant changes in stage distribution across seven major cancer sites between 2019 and 2020. 22 In Denmark, Norway and Sweden, we found particularly large cumulative annual declines of malignant cases in screening ages 50 to 69 years, indicating that the large reductions in the spring were not fully compensated during the summer and autumn with lower COVID-19 infection rates. By the end of 2020, there was a deficit in the number of new malignant cases in both sexes in Sweden, while the reduction of in situ cases was confined to women, representing a substantial deficit of undetected cases in line with a previous national report. 16 Breast cancer and cervical cancer screening was temporarily halted or reduced, albeit with large regional variations within Sweden. Following resumptions of services, several breast cancer screening units in Sweden reported remaining back-logs in the autumn 2020. 38 In December 2020, 10 out of 21 Swedish healthcare regions reported cervical cancer screening deficits (personal communication). Similarly, six regions reported a decline of more than 30% of screendetected breast cancer in 2020. 16 In conclusion, despite marked differences between the Nordic coun- Our study was based on national and regional cancer registry data. The data are available from each national and regional cancer registry under the use of appropriate ethical and legal permissions, including the GDPR. Further details and other data that support the findings of our study are available from the corresponding author upon request. Denmark: Legal approval to use data was obtained from The Danish Health Data Authority. Ethical review is not required for register-based studies in Denmark. The Faroe Islands: The data collection for this project has been approved by the Faroese Data Protection Authority. 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The authors declare no potential conflict of interests. our study. The FCR has permission to collect, process and report statistical data without the need to seek consent. Iceland: The Icelandic Cancer Registry (ICR) provided statistical data for our study. The ICR has permission to collect, process and report statistical data without the need to seek consent. Norway: The Norwegian Cancer Registry provided statistical data for our study. The CRN has permission to collect, process and report statistical data without the need to seek consent. This project also has an ethical permission in Norway (REK