Estimating COVID-19-Related Excess Mortality Excluding Seasonal Phenomena in Belgium
Main Article Content
Abstract
Excess mortality, rather than reported COVID-19 deaths has been suggested to evaluate the impact of the SARS-CoV-2 induced Corona Virus Disease (COVID-19) pandemic on mortality. However, the relationship between excess mortality and COVID-19 mortality is perturbed by seasonal phenomena, such as extreme temperatures and seasonal influenza. Models used to estimate excess mortality often ignore these underlying patterns. We propose a dynamic linear state-space model to estimate all-cause mortality, which accounts for extreme temperatures above 25°C and seasonal influenza via the Goldstein index. The state-space model prediction of the excess mortality that is not explained by heat waves and seasonal influenza coincides with the reported COVID-19 mortality in the year 2020 in Belgium.
Keywords:
all-cause mortality, COVID-19, excess mortality, heat wave, seasonal influenza, state-space model
Article Details
How to Cite
VERBEECK, Johan et al.
Estimating COVID-19-Related Excess Mortality Excluding Seasonal Phenomena in Belgium.
Medical Research Archives, [S.l.], v. 10, n. 9, sep. 2022.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/3077>. Date accessed: 22 dec. 2024.
doi: https://doi.org/10.18103/mra.v10i9.3077.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Giattino C, Ritchie H, Roser M, Ortiz-Ospina E, Hasell J. Excess mortality during the Coronavirus pandemic (COVID-19); 2021. https://ourworldindata.org/excess-mortality-covid.
2. Nørgaard SK, Vestergaard LS, Nielsen J, Richter L, Schmid D, Bustos N, Braye T, Athanasiadou M, Lytras T, Denissov G, Veideman T, Luomala O, Möttönen T, Fouillet A, Caserio-Schönemann C, An der Heiden M, Uphoff H, Gkolfinopoulou K, Bobvos J, Paldy A, Rotem N, Kornilenko I, Domegan L, O'Donnell J, Donato F, Scortichini M, Hoffmann P, Velez T, England K, Calleja N, van Asten L, Stoeldraijer L, White RA, Paulsen TH, da Silva SP, Rodrigues AP, Klepac P, Zaletel M, Fafangel M, Larrauri A, León I, Farah A, Galanis I, Junker C, Perisa D, Sinnathamby M, Andrews N, O'Doherty MG, Irwin D, Kennedy S, McMenamin J, Adlhoch C, Bundle N, Penttinen P, Pukkila J, Pebody R, Krause TG, Mølbak K. Real-time monitoring shows substantial excess all-cause mortality during second wave of COVID-19 in Europe, October to December 2020. Euro Surveill. 2021 Jan;26(2):2002023. doi: 10.2807/1560-7917.ES.2021.26.1.2002023.
3. Molenberghs G, Faes C, Verbeeck J, Deboosere P, Abrams S, Willem L, Aerts J, Theeten H, Devleesschauwer B, Bustos Sierra N, Renard F, Herzog S, Lusyne P, Van der Heyden J, Van Oyen H, Van Damme P, Hens N. COVID-19 mortality, excess mortality, deaths per million and infection fatality ratio, Belgium, 9 March 2020 to 28 June 2020. Euro Surveill. 2022 Feb;27(7):2002060. doi: 10.2807/1560-7917.ES.2022.27.7.2002060.
4. Bustos Sierra N, Bossuyt N, Braeye T, Leroy M, Moyersoen I, Peeters I, Scohy A, Van der Heyden J, Van Oyen H, Renard F. All-cause mortality supports the COVID-19 mortality in Belgium and comparison with major fatal events of the last century. Arch Public Health. 2020 Nov 13;78(1):117. doi: 10.1186/s13690-020-00496-x.
5. Aron J, Giattino C, Muellbauer J, and Ritchie H. A pandemic primer on excess mortality statistics and their comparability across countries; 2020. https://ourworldindata.org/covid-excess-mortality
6. Morgan D, Ino J, Di Paolantonio G, and Murtin F. Excess mortality: Measuring the direct and indirect impact of COVID-19. OECD. 2020; https://dx.doi.org/10.1787/c5dc0c50-en
7. Beaney T, Clarke JM, Jain V, Golestaneh AK, Lyons G, Salman D, Majeed A. Excess mortality: the gold standard in measuring the impact of COVID-19 worldwide? J R Soc Med. 2020 Sep;113(9):329-334. doi: 10.1177/0141076820956802.
8. Verbeeck J, Faes C, Neyens T, Hens N, Verbeke G, Deboosere P, Molenberghs G. A linear mixed model to estimate COVID-19-induced excess mortality. Biometrics. 2021 Oct 25:10.1111/biom.13578. doi: 10.1111/biom.13578.
9. Michelozzi P, de'Donato F, Scortichini M, Pezzotti P, Stafoggia M, De Sario M, Costa G, Noccioli F, Riccardo F, Bella A, Demaria M, Rossi P, Brusaferro S, Rezza G, Davoli M. Temporal dynamics in total excess mortality and COVID-19 deaths in Italian cities. BMC Public Health. 2020 Aug 14;20(1):1238. doi: 10.1186/s12889-020-09335-8.
10. Modig K, Ahlbom A, Ebeling M. Excess mortality from COVID-19: weekly excess death rates by age and sex for Sweden and its most affected region. Eur J Public Health. 2021 Feb 1;31(1):17-22. doi: 10.1093/eurpub/ckaa218.
11. Stang A, Standl F, Kowall B, Brune B, Böttcher J, Brinkmann M, Dittmer U, Jöckel KH. Excess mortality due to COVID-19 in Germany. J Infect. 2020 Nov;81(5):797-801. doi: 10.1016/j.jinf.2020.09.012.
12. The Economist. Tracking COVID-19 excess deaths across countries.2020; https://www.economist.com/graphic-detail/2020/07/15/ tracking-covid-19-excess-deaths-across-countries
13. The New York Times. The pandemic’s hidden toll: half a million deaths. 2020; https://www.nytimes.com/interactive/2020/04/21/world/coronavirus-missing-deaths.html
14. Faust JS, Krumholz HM, Du C, Mayes KD, Lin Z, Gilman C, Walensky RP. All-Cause Excess Mortality and COVID-19-Related Mortality Among US Adults Aged 25-44 Years, March-July 2020. JAMA. 2021 Feb 23;325(8):785-787. doi: 10.1001/jama.2020.24243.
15. Scortichini M, Schneider Dos Santos R, De' Donato F, De Sario M, Michelozzi P, Davoli M, Masselot P, Sera F, Gasparrini A. Excess mortality during the COVID-19 outbreak in Italy: a two-stage interrupted time-series analysis. Int J Epidemiol. 2021 Jan 23;49(6):1909-1917. doi: 10.1093/ije/dyaa169.
16. Blangiardo M, Cameletti M, Pirani M, Corsetti G, Battaglini M, Baio G. Estimating weekly excess mortality at sub-national level in Italy during the COVID-19 pandemic. PLoS One. 2020 Oct 9;15(10):e0240286. doi: 10.1371/journal.pone.0240286.
17. Vestergaard LS, Nielsen J, Richter L, Schmid D, Bustos N, Braeye T, Denissov G, Veideman T, Luomala O, Möttönen T, Fouillet A, Caserio-Schönemann C, An der Heiden M, Uphoff H, Lytras T, Gkolfinopoulou K, Paldy A, Domegan L, O'Donnell J, De' Donato F, Noccioli F, Hoffmann P, Velez T, England K, van Asten L, White RA, Tønnessen R, da Silva SP, Rodrigues AP, Larrauri A, Delgado-Sanz C, Farah A, Galanis I, Junker C, Perisa D, Sinnathamby M, Andrews N, O'Doherty M, Marquess DF, Kennedy S, Olsen SJ, Pebody R; ECDC Public Health Emergency Team for COVID-19, Krause TG, Mølbak K. Excess all-cause mortality during the COVID-19 pandemic in Europe - preliminary pooled estimates from the EuroMOMO network, March to April 2020. Euro Surveill. 2020 Jul;25(26):2001214. doi: 10.2807/1560-7917.ES.2020.25.26.2001214.
18. Fouillet A, Pontais I, Caserio-Schönemann C. Excess all-cause mortality during the first wave of the COVID-19 epidemic in France, March to May 2020. Euro Surveill. 2020 Aug;25(34):2001485. doi: 10.2807/1560-7917.ES.2020.25.34.2001485.
19. Cox B, Wuillaume F, Van Oyen H, Maes S. Monitoring of all-cause mortality in Belgium (Be-MOMO): a new and automated system for the early detection and quantification of the mortality impact of public health events. Int J Public Health. 2010 Aug;55(4):251-9. doi: 10.1007/s00038-010-0135-6.
20. Nielsen J, Krause TG, Mølbak K. Influenza-associated mortality determined from all-cause mortality, Denmark 2010/11-2016/17: The FluMOMO model. Influenza Other Respir Viruses. 2018 Sep;12(5):591-604. doi: 10.1111/irv.12564.
21. Nielsen J, Rod NH, Vestergaard LS, Lange T. Estimates of mortality attributable to COVID-19: a statistical model for monitoring COVID-19 and seasonal influenza, Denmark, spring 2020. Euro Surveill. 2021 Feb;26(8):2001646. doi: 10.2807/1560-7917.ES.2021.26.8.2001646.
22. Harvey SJ. Forecasting, structural time series models and the Kalman filter. 1st edition Cambridge University Press, New York; 1989.
23. Durbin J and Koopman SJ. Time series analysis by state space methods. 2nd edition Oxford University Press, Oxford; 2012.
24. STATBEL. Number of deaths per day, sex, age, region, province, district. 2020. https://statbel.fgov.be/en/open-data/number-deaths-day-sex-district-age.
25. EPISTAT: COVID-19. Sciensano. 2020. https://epistat.wiv-isp.be/covid/
26. Renard F, Scohy A, Van der Heyden J, Peeters I, Dequeker S, Vandael E, Van Goethem N, Dubourg D, De Viron L, Kongs A, Hammami N, Devleesschauwer B, Sasse A, Rebolledo Gonzalez J, Bustos Sierra N. Establishing an ad hoc COVID-19 mortality surveillance during the first epidemic wave in Belgium, 1 March to 21 June 2020. Euro Surveill. 2021 Dec;26(48):2001402. doi: 10.2807/1560-7917.ES.2021.26.48.2001402.
27. Goldstein E, Cobey S, Takahashi S, Miller JC, Lipsitch M. Predicting the epidemic sizes of influenza A/H1N1, A/H3N2, and B: a statistical method. PLoS Med. 2011 Jul;8(7):e1001051. doi: 10.1371/journal.pmed.1001051.
28. Goldstein E, Viboud C, Charu V, Lipsitch M. Improving the estimation of influenza-related mortality over a seasonal baseline. Epidemiology. 2012 Nov;23(6):829-38. doi: 10.1097/EDE.0b013e31826c2dda.
29. Royal Meteorological Institute. 2021. https://www.meteo.be/en/belgium.
30. Gasparrini A, Armstrong B. The impact of heat waves on mortality. Epidemiology. 2011 Jan;22(1):68-73. doi: 10.1097/EDE.0b013e3181fdcd99.
31. Li L, Wong JY, Wu P, Bond HS, Lau EHY, Sullivan SG, Cowling BJ. Heterogeneity in Estimates of the Impact of Influenza on Population Mortality: A Systematic Review. Am J Epidemiol. 2018 Feb 1;187(2):378-388. doi: 10.1093/aje/kwx270.
32. Leroy M, Dupont Y, Braeye T, Bossuyt N, Bustos Sierra N. EPISTAT, Belgian mortality monitoring (BE-MOMO), Sciensano. 2021. https://epistat.wiv-isp.be/momo/.
33. COVID-19 Excess Mortality Collaborators. Estimating excess mortality due to the COVID-19 pandemic: a systematic analysis of COVID-19-related mortality, 2020-21. Lancet. 2022 Apr 16;399(10334):1513-1536. doi: 10.1016/S0140-6736(21)02796-3.
34. Karlinsky A, Kobak D. Tracking excess mortality across countries during the COVID-19 pandemic with the World Mortality Dataset. Elife. 2021 Jun 30;10:e69336. doi: 10.7554/eLife.69336.
35. Xu Z, FitzGerald G, Guo Y, Jalaludin B, Tong S. Impact of heatwave on mortality under different heatwave definitions: A systematic review and meta-analysis. Environ Int. 2016;89-90:193-203.
2. Nørgaard SK, Vestergaard LS, Nielsen J, Richter L, Schmid D, Bustos N, Braye T, Athanasiadou M, Lytras T, Denissov G, Veideman T, Luomala O, Möttönen T, Fouillet A, Caserio-Schönemann C, An der Heiden M, Uphoff H, Gkolfinopoulou K, Bobvos J, Paldy A, Rotem N, Kornilenko I, Domegan L, O'Donnell J, Donato F, Scortichini M, Hoffmann P, Velez T, England K, Calleja N, van Asten L, Stoeldraijer L, White RA, Paulsen TH, da Silva SP, Rodrigues AP, Klepac P, Zaletel M, Fafangel M, Larrauri A, León I, Farah A, Galanis I, Junker C, Perisa D, Sinnathamby M, Andrews N, O'Doherty MG, Irwin D, Kennedy S, McMenamin J, Adlhoch C, Bundle N, Penttinen P, Pukkila J, Pebody R, Krause TG, Mølbak K. Real-time monitoring shows substantial excess all-cause mortality during second wave of COVID-19 in Europe, October to December 2020. Euro Surveill. 2021 Jan;26(2):2002023. doi: 10.2807/1560-7917.ES.2021.26.1.2002023.
3. Molenberghs G, Faes C, Verbeeck J, Deboosere P, Abrams S, Willem L, Aerts J, Theeten H, Devleesschauwer B, Bustos Sierra N, Renard F, Herzog S, Lusyne P, Van der Heyden J, Van Oyen H, Van Damme P, Hens N. COVID-19 mortality, excess mortality, deaths per million and infection fatality ratio, Belgium, 9 March 2020 to 28 June 2020. Euro Surveill. 2022 Feb;27(7):2002060. doi: 10.2807/1560-7917.ES.2022.27.7.2002060.
4. Bustos Sierra N, Bossuyt N, Braeye T, Leroy M, Moyersoen I, Peeters I, Scohy A, Van der Heyden J, Van Oyen H, Renard F. All-cause mortality supports the COVID-19 mortality in Belgium and comparison with major fatal events of the last century. Arch Public Health. 2020 Nov 13;78(1):117. doi: 10.1186/s13690-020-00496-x.
5. Aron J, Giattino C, Muellbauer J, and Ritchie H. A pandemic primer on excess mortality statistics and their comparability across countries; 2020. https://ourworldindata.org/covid-excess-mortality
6. Morgan D, Ino J, Di Paolantonio G, and Murtin F. Excess mortality: Measuring the direct and indirect impact of COVID-19. OECD. 2020; https://dx.doi.org/10.1787/c5dc0c50-en
7. Beaney T, Clarke JM, Jain V, Golestaneh AK, Lyons G, Salman D, Majeed A. Excess mortality: the gold standard in measuring the impact of COVID-19 worldwide? J R Soc Med. 2020 Sep;113(9):329-334. doi: 10.1177/0141076820956802.
8. Verbeeck J, Faes C, Neyens T, Hens N, Verbeke G, Deboosere P, Molenberghs G. A linear mixed model to estimate COVID-19-induced excess mortality. Biometrics. 2021 Oct 25:10.1111/biom.13578. doi: 10.1111/biom.13578.
9. Michelozzi P, de'Donato F, Scortichini M, Pezzotti P, Stafoggia M, De Sario M, Costa G, Noccioli F, Riccardo F, Bella A, Demaria M, Rossi P, Brusaferro S, Rezza G, Davoli M. Temporal dynamics in total excess mortality and COVID-19 deaths in Italian cities. BMC Public Health. 2020 Aug 14;20(1):1238. doi: 10.1186/s12889-020-09335-8.
10. Modig K, Ahlbom A, Ebeling M. Excess mortality from COVID-19: weekly excess death rates by age and sex for Sweden and its most affected region. Eur J Public Health. 2021 Feb 1;31(1):17-22. doi: 10.1093/eurpub/ckaa218.
11. Stang A, Standl F, Kowall B, Brune B, Böttcher J, Brinkmann M, Dittmer U, Jöckel KH. Excess mortality due to COVID-19 in Germany. J Infect. 2020 Nov;81(5):797-801. doi: 10.1016/j.jinf.2020.09.012.
12. The Economist. Tracking COVID-19 excess deaths across countries.2020; https://www.economist.com/graphic-detail/2020/07/15/ tracking-covid-19-excess-deaths-across-countries
13. The New York Times. The pandemic’s hidden toll: half a million deaths. 2020; https://www.nytimes.com/interactive/2020/04/21/world/coronavirus-missing-deaths.html
14. Faust JS, Krumholz HM, Du C, Mayes KD, Lin Z, Gilman C, Walensky RP. All-Cause Excess Mortality and COVID-19-Related Mortality Among US Adults Aged 25-44 Years, March-July 2020. JAMA. 2021 Feb 23;325(8):785-787. doi: 10.1001/jama.2020.24243.
15. Scortichini M, Schneider Dos Santos R, De' Donato F, De Sario M, Michelozzi P, Davoli M, Masselot P, Sera F, Gasparrini A. Excess mortality during the COVID-19 outbreak in Italy: a two-stage interrupted time-series analysis. Int J Epidemiol. 2021 Jan 23;49(6):1909-1917. doi: 10.1093/ije/dyaa169.
16. Blangiardo M, Cameletti M, Pirani M, Corsetti G, Battaglini M, Baio G. Estimating weekly excess mortality at sub-national level in Italy during the COVID-19 pandemic. PLoS One. 2020 Oct 9;15(10):e0240286. doi: 10.1371/journal.pone.0240286.
17. Vestergaard LS, Nielsen J, Richter L, Schmid D, Bustos N, Braeye T, Denissov G, Veideman T, Luomala O, Möttönen T, Fouillet A, Caserio-Schönemann C, An der Heiden M, Uphoff H, Lytras T, Gkolfinopoulou K, Paldy A, Domegan L, O'Donnell J, De' Donato F, Noccioli F, Hoffmann P, Velez T, England K, van Asten L, White RA, Tønnessen R, da Silva SP, Rodrigues AP, Larrauri A, Delgado-Sanz C, Farah A, Galanis I, Junker C, Perisa D, Sinnathamby M, Andrews N, O'Doherty M, Marquess DF, Kennedy S, Olsen SJ, Pebody R; ECDC Public Health Emergency Team for COVID-19, Krause TG, Mølbak K. Excess all-cause mortality during the COVID-19 pandemic in Europe - preliminary pooled estimates from the EuroMOMO network, March to April 2020. Euro Surveill. 2020 Jul;25(26):2001214. doi: 10.2807/1560-7917.ES.2020.25.26.2001214.
18. Fouillet A, Pontais I, Caserio-Schönemann C. Excess all-cause mortality during the first wave of the COVID-19 epidemic in France, March to May 2020. Euro Surveill. 2020 Aug;25(34):2001485. doi: 10.2807/1560-7917.ES.2020.25.34.2001485.
19. Cox B, Wuillaume F, Van Oyen H, Maes S. Monitoring of all-cause mortality in Belgium (Be-MOMO): a new and automated system for the early detection and quantification of the mortality impact of public health events. Int J Public Health. 2010 Aug;55(4):251-9. doi: 10.1007/s00038-010-0135-6.
20. Nielsen J, Krause TG, Mølbak K. Influenza-associated mortality determined from all-cause mortality, Denmark 2010/11-2016/17: The FluMOMO model. Influenza Other Respir Viruses. 2018 Sep;12(5):591-604. doi: 10.1111/irv.12564.
21. Nielsen J, Rod NH, Vestergaard LS, Lange T. Estimates of mortality attributable to COVID-19: a statistical model for monitoring COVID-19 and seasonal influenza, Denmark, spring 2020. Euro Surveill. 2021 Feb;26(8):2001646. doi: 10.2807/1560-7917.ES.2021.26.8.2001646.
22. Harvey SJ. Forecasting, structural time series models and the Kalman filter. 1st edition Cambridge University Press, New York; 1989.
23. Durbin J and Koopman SJ. Time series analysis by state space methods. 2nd edition Oxford University Press, Oxford; 2012.
24. STATBEL. Number of deaths per day, sex, age, region, province, district. 2020. https://statbel.fgov.be/en/open-data/number-deaths-day-sex-district-age.
25. EPISTAT: COVID-19. Sciensano. 2020. https://epistat.wiv-isp.be/covid/
26. Renard F, Scohy A, Van der Heyden J, Peeters I, Dequeker S, Vandael E, Van Goethem N, Dubourg D, De Viron L, Kongs A, Hammami N, Devleesschauwer B, Sasse A, Rebolledo Gonzalez J, Bustos Sierra N. Establishing an ad hoc COVID-19 mortality surveillance during the first epidemic wave in Belgium, 1 March to 21 June 2020. Euro Surveill. 2021 Dec;26(48):2001402. doi: 10.2807/1560-7917.ES.2021.26.48.2001402.
27. Goldstein E, Cobey S, Takahashi S, Miller JC, Lipsitch M. Predicting the epidemic sizes of influenza A/H1N1, A/H3N2, and B: a statistical method. PLoS Med. 2011 Jul;8(7):e1001051. doi: 10.1371/journal.pmed.1001051.
28. Goldstein E, Viboud C, Charu V, Lipsitch M. Improving the estimation of influenza-related mortality over a seasonal baseline. Epidemiology. 2012 Nov;23(6):829-38. doi: 10.1097/EDE.0b013e31826c2dda.
29. Royal Meteorological Institute. 2021. https://www.meteo.be/en/belgium.
30. Gasparrini A, Armstrong B. The impact of heat waves on mortality. Epidemiology. 2011 Jan;22(1):68-73. doi: 10.1097/EDE.0b013e3181fdcd99.
31. Li L, Wong JY, Wu P, Bond HS, Lau EHY, Sullivan SG, Cowling BJ. Heterogeneity in Estimates of the Impact of Influenza on Population Mortality: A Systematic Review. Am J Epidemiol. 2018 Feb 1;187(2):378-388. doi: 10.1093/aje/kwx270.
32. Leroy M, Dupont Y, Braeye T, Bossuyt N, Bustos Sierra N. EPISTAT, Belgian mortality monitoring (BE-MOMO), Sciensano. 2021. https://epistat.wiv-isp.be/momo/.
33. COVID-19 Excess Mortality Collaborators. Estimating excess mortality due to the COVID-19 pandemic: a systematic analysis of COVID-19-related mortality, 2020-21. Lancet. 2022 Apr 16;399(10334):1513-1536. doi: 10.1016/S0140-6736(21)02796-3.
34. Karlinsky A, Kobak D. Tracking excess mortality across countries during the COVID-19 pandemic with the World Mortality Dataset. Elife. 2021 Jun 30;10:e69336. doi: 10.7554/eLife.69336.
35. Xu Z, FitzGerald G, Guo Y, Jalaludin B, Tong S. Impact of heatwave on mortality under different heatwave definitions: A systematic review and meta-analysis. Environ Int. 2016;89-90:193-203.