Impact of the COVID-19 pandemic on breast cancer screening indicators in a Spanish population-based program: a cohort study

  1. Guillermo Bosch
  2. Margarita Posso  Is a corresponding author
  3. Javier Louro
  4. Marta Roman
  5. Miquel Porta
  6. Xavier Castells
  7. Francesc Macià
  1. Institut Hospital del Mar d'Investigacions Mèdiques, Spain
  2. Autonomous University of Barcelona, Spain

Abstract

Background: To assess the effect of the COVID-19 pandemic on performance indicators in the population-based breast cancer screening program of Parc de Salut Mar (PSMAR), Barcelona, Spain.

Methods: We conducted a before-and-after, study to evaluate participation, recall, false-positives, the cancer detection rate, and cancer characteristics in our screening population from March 2020 to March 2021 compared with the four previous rounds (2012-2019). Using multi-level logistic regression models, we estimated the adjusted odds ratios (aOR) of each of the performance indicators for the COVID-19 period, controlling by type of screening (prevalent or incident), socioeconomic index, family history of breast cancer, and menopausal status. We analyzed 144,779 invitations from 47,571 women.

Results: During the COVID-19 period, the odds of participation were lower in first-time invitees (aOR=0.90[95%CI=0.84-0.96]) and in those who had previously participated regularly and irregularly (aOR=0.63 [95%CI=0.59-0.67] and aOR=0.95 [95%CI=0.86-1.05], respectively). Participation showed a modest increase in women not attending any of the previous rounds (aOR=1.10 [95%CI=1.01-1.20]). The recall rate decreased in both prevalent and incident screening (aOR=0.74 [95%CI 0.56-0.99] and aOR=0.80 [95%CI 0.68-0.95], respectively). False positives also decreased in both groups (prevalent aOR=0.92 [95%CI 0.66-1.28] and incident aOR=0.72 [95%CI 0.59-0.88]. No significant differences were observed in compliance with recall (OR= 1.26, 95%CI 0.76-2.23), cancer detection rate (aOR=0.91 [95%CI=0.69-1.18]) or cancer stages.

Conclusions: The COVID-19 pandemic negatively affected screening attendance, especially in previous participants and newcomers. We found a reduction in recall and false-positives and no marked differences in cancer detection, indicating the robustness of the program. There is a need for further evaluations of interval cancers and potential diagnostic delays.

Funding: This study has received funding by grantsPI19/00007 and PI21/00058, funded by Instituto de Salud Carlos III (ISCIII) and co-funded by the European Union and Grant RD21/0016/0020 funded by Instituto de Salud Carlos III and by the European Union NextGenerationEU, Mecanismo para la Recuperación y la Resiliencia (MRR).

Data availability

Source data form all tables and figures can be found in the following Dataset:BOSCH, GUILLERMO, 2022, "Breast cancer screening program invitations (2012-2021)", https://doi.org/10.7910/DVN/VVQNWM, Harvard Dataverse, V1, UNF:6:CaW3sEp4tMsg13z2I1eZbQ== [fileUNF]Data from "Impact on covid19 dataset invited women.sav" was used in tables 1 and 2 and figures 1,2 and 3. Data from "cancer characteristics database.tab" was used in table 3.

Article and author information

Author details

  1. Guillermo Bosch

    Department of Epidemiology and Evaluation, Institut Hospital del Mar d'Investigacions Mèdiques, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  2. Margarita Posso

    Department of Epidemiology and Evaluation, Institut Hospital del Mar d'Investigacions Mèdiques, Barcelona, Spain
    For correspondence
    mposso@parcdesalutmar.cat
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5053-257X
  3. Javier Louro

    Department of Epidemiology and Evaluation, Institut Hospital del Mar d'Investigacions Mèdiques, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Marta Roman

    Department of Epidemiology and Evaluation, Institut Hospital del Mar d'Investigacions Mèdiques, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Miquel Porta

    Autonomous University of Barcelona, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. Xavier Castells

    Department of Epidemiology and Evaluation, Institut Hospital del Mar d'Investigacions Mèdiques, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Francesc Macià

    Department of Epidemiology and Evaluation, Institut Hospital del Mar d'Investigacions Mèdiques, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.

Funding

Instituto de Salud Carlos III (PI19/00007)

  • Margarita Posso

Instituto de Salud Carlos III (PI21/00058)

  • Guillermo Bosch

Instituto de Salud Carlos III (PI21/00058)

  • Javier Louro

Instituto de Salud Carlos III (PI21/00058)

  • Marta Roman

Instituto de Salud Carlos III (PI21/00058)

  • Francesc Macià

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: Due to the retrospective nature of the study and the absence of direct contact with women, which did not affect their relationship with the program, informed consent was waived by the Ethics Committee of PSMAR, which approved the study (reg.2021/9866). The study guaranteed Spain's legal regulations on data confidentiality (law 15/99 of December 13 on the protection of personal data).

Reviewing Editor

  1. Talía Malagón, McGill University, Canada

Publication history

  1. Received: January 29, 2022
  2. Preprint posted: March 7, 2022 (view preprint)
  3. Accepted: June 9, 2022
  4. Accepted Manuscript published: June 10, 2022 (version 1)
  5. Version of Record published: June 21, 2022 (version 2)

Copyright

© 2022, Bosch et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Guillermo Bosch
  2. Margarita Posso
  3. Javier Louro
  4. Marta Roman
  5. Miquel Porta
  6. Xavier Castells
  7. Francesc Macià
(2022)
Impact of the COVID-19 pandemic on breast cancer screening indicators in a Spanish population-based program: a cohort study
eLife 11:e77434.
https://doi.org/10.7554/eLife.77434

Further reading

    1. Epidemiology and Global Health
    Katharine Sherratt, Hugo Gruson ... Sebastian Funk
    Research Article Updated

    Background:

    Short-term forecasts of infectious disease burden can contribute to situational awareness and aid capacity planning. Based on best practice in other fields and recent insights in infectious disease epidemiology, one can maximise the predictive performance of such forecasts if multiple models are combined into an ensemble. Here, we report on the performance of ensembles in predicting COVID-19 cases and deaths across Europe between 08 March 2021 and 07 March 2022.

    Methods:

    We used open-source tools to develop a public European COVID-19 Forecast Hub. We invited groups globally to contribute weekly forecasts for COVID-19 cases and deaths reported by a standardised source for 32 countries over the next 1–4 weeks. Teams submitted forecasts from March 2021 using standardised quantiles of the predictive distribution. Each week we created an ensemble forecast, where each predictive quantile was calculated as the equally-weighted average (initially the mean and then from 26th July the median) of all individual models’ predictive quantiles. We measured the performance of each model using the relative Weighted Interval Score (WIS), comparing models’ forecast accuracy relative to all other models. We retrospectively explored alternative methods for ensemble forecasts, including weighted averages based on models’ past predictive performance.

    Results:

    Over 52 weeks, we collected forecasts from 48 unique models. We evaluated 29 models’ forecast scores in comparison to the ensemble model. We found a weekly ensemble had a consistently strong performance across countries over time. Across all horizons and locations, the ensemble performed better on relative WIS than 83% of participating models’ forecasts of incident cases (with a total N=886 predictions from 23 unique models), and 91% of participating models’ forecasts of deaths (N=763 predictions from 20 models). Across a 1–4 week time horizon, ensemble performance declined with longer forecast periods when forecasting cases, but remained stable over 4 weeks for incident death forecasts. In every forecast across 32 countries, the ensemble outperformed most contributing models when forecasting either cases or deaths, frequently outperforming all of its individual component models. Among several choices of ensemble methods we found that the most influential and best choice was to use a median average of models instead of using the mean, regardless of methods of weighting component forecast models.

    Conclusions:

    Our results support the use of combining forecasts from individual models into an ensemble in order to improve predictive performance across epidemiological targets and populations during infectious disease epidemics. Our findings further suggest that median ensemble methods yield better predictive performance more than ones based on means. Our findings also highlight that forecast consumers should place more weight on incident death forecasts than incident case forecasts at forecast horizons greater than 2 weeks.

    Funding:

    AA, BH, BL, LWa, MMa, PP, SV funded by National Institutes of Health (NIH) Grant 1R01GM109718, NSF BIG DATA Grant IIS-1633028, NSF Grant No.: OAC-1916805, NSF Expeditions in Computing Grant CCF-1918656, CCF-1917819, NSF RAPID CNS-2028004, NSF RAPID OAC-2027541, US Centers for Disease Control and Prevention 75D30119C05935, a grant from Google, University of Virginia Strategic Investment Fund award number SIF160, Defense Threat Reduction Agency (DTRA) under Contract No. HDTRA1-19-D-0007, and respectively Virginia Dept of Health Grant VDH-21-501-0141, VDH-21-501-0143, VDH-21-501-0147, VDH-21-501-0145, VDH-21-501-0146, VDH-21-501-0142, VDH-21-501-0148. AF, AMa, GL funded by SMIGE - Modelli statistici inferenziali per governare l'epidemia, FISR 2020-Covid-19 I Fase, FISR2020IP-00156, Codice Progetto: PRJ-0695. AM, BK, FD, FR, JK, JN, JZ, KN, MG, MR, MS, RB funded by Ministry of Science and Higher Education of Poland with grant 28/WFSN/2021 to the University of Warsaw. BRe, CPe, JLAz funded by Ministerio de Sanidad/ISCIII. BT, PG funded by PERISCOPE European H2020 project, contract number 101016233. CP, DL, EA, MC, SA funded by European Commission - Directorate-General for Communications Networks, Content and Technology through the contract LC-01485746, and Ministerio de Ciencia, Innovacion y Universidades and FEDER, with the project PGC2018-095456-B-I00. DE., MGu funded by Spanish Ministry of Health / REACT-UE (FEDER). DO, GF, IMi, LC funded by Laboratory Directed Research and Development program of Los Alamos National Laboratory (LANL) under project number 20200700ER. DS, ELR, GG, NGR, NW, YW funded by National Institutes of General Medical Sciences (R35GM119582; the content is solely the responsibility of the authors and does not necessarily represent the official views of NIGMS or the National Institutes of Health). FB, FP funded by InPresa, Lombardy Region, Italy. HG, KS funded by European Centre for Disease Prevention and Control. IV funded by Agencia de Qualitat i Avaluacio Sanitaries de Catalunya (AQuAS) through contract 2021-021OE. JDe, SMo, VP funded by Netzwerk Universitatsmedizin (NUM) project egePan (01KX2021). JPB, SH, TH funded by Federal Ministry of Education and Research (BMBF; grant 05M18SIA). KH, MSc, YKh funded by Project SaxoCOV, funded by the German Free State of Saxony. Presentation of data, model results and simulations also funded by the NFDI4Health Task Force COVID-19 (https://www.nfdi4health.de/task-force-covid-19-2) within the framework of a DFG-project (LO-342/17-1). LP, VE funded by Mathematical and Statistical modelling project (MUNI/A/1615/2020), Online platform for real-time monitoring, analysis and management of epidemic situations (MUNI/11/02202001/2020); VE also supported by RECETOX research infrastructure (Ministry of Education, Youth and Sports of the Czech Republic: LM2018121), the CETOCOEN EXCELLENCE (CZ.02.1.01/0.0/0.0/17-043/0009632), RECETOX RI project (CZ.02.1.01/0.0/0.0/16-013/0001761). NIB funded by Health Protection Research Unit (grant code NIHR200908). SAb, SF funded by Wellcome Trust (210758/Z/18/Z).

    1. Epidemiology and Global Health
    Ekaterina Schneider, Dora Hopf ... Beate Ditzen
    Research Article

    Background:

    Affectionate touch, which is vital for mental and physical health, was restricted during the Covid-19 pandemic. This study investigated the association between momentary affectionate touch and subjective well-being, as well as salivary oxytocin and cortisol in everyday life during the pandemic.

    Methods:

    In the first step, we measured anxiety and depression symptoms, loneliness and attitudes toward social touch in a large cross-sectional online survey (N = 1050). From this sample, N = 247 participants completed ecological momentary assessments over 2 days with six daily assessments by answering smartphone-based questions on affectionate touch and momentary mental state, and providing concomitant saliva samples for cortisol and oxytocin assessment.

    Results:

    Multilevel models showed that on a within-person level, affectionate touch was associated with decreased self-reported anxiety, general burden, stress, and increased oxytocin levels. On a between-person level, affectionate touch was associated with decreased cortisol levels and higher happiness. Moreover, individuals with a positive attitude toward social touch experiencing loneliness reported more mental health problems.

    Conclusions:

    Our results suggest that affectionate touch is linked to higher endogenous oxytocin in times of pandemic and lockdown and might buffer stress on a subjective and hormonal level. These findings might have implications for preventing mental burden during social contact restrictions.

    Funding:

    The study was funded by the German Research Foundation, the German Psychological Society, and German Academic Exchange Service.