It has been argued that coronavirus disease 2019 (COVID-19) mortality rates exceed those from the influenza pandemic in 1918–19,1 but comparisons can be misleading unless marked differences in age-specific mortality2 and changes in population age structure in the past century3 are taken into account. The need for application of fundamental epidemiological approaches in understanding COVID-19 has also been recognized.4
We used indirect age standardization to calculate standardized mortality ratios (SMRs) for the 1918–19 winter influenza pandemic wave, with the reference mortality rate being COVID-19 death rates for New York City.5 Population estimates were obtained from the United States (US) Census Bureau website and interpolated between censuses where necessary. Mortality in New York City for the 1918–19 winter pandemic influenza wave was obtained from Olson et al. (2005).6 We also used published US influenza mortality data for the 1918–19 and 2009 pandemics and the severe 2017–18 season as comparators.2,7,8
This study used only aggregate statistics from public websites and published literature and was therefore exempt from ethics review by our institution.
Of 21,649 cumulative confirmed and probable COVID-19 deaths in New York City as at 2 June 2020,5 21,450 (99%) had a known age at death, of which 0.065%, 3.7%, 22%, 24% and 49% were in the ≤17, 18–44, 45–64, 65–74 and ≥75 year age groups, respectively. The corresponding death rates per 100 000 population were 0.80, 24, 230, 740 and 2000, respectively, making crude, all-age mortality of 258 per 100 000 population almost uninterpretable for younger and older age groups.
In New York City, the age-adjusted, all-age mortality rate for the 1918–19 winter wave of the influenza pandemic was 6.7 times higher than COVID-19 cumulative mortality rates to 2 June 2020. In <45-year-olds, the SMR was 42; that is, 42 times higher for influenza in 1918–19 than for COVID in 2020. In ≥45-year-olds, the SMR was 0.56; that is, 44% lower in 1918–19 than for COVID in 2020 (Table 1).
Table 1.
Standardized mortality ratios (SMR) of the 1918–19 winter wave of pandemic influenza6 relative to the first 2020 wave of COVID-19 infection in New York Citya
| Age group (years) | Observed deaths | Expected deaths | Crude mortality ratio | SMR |
|---|---|---|---|---|
| All ages | 29 200 | 4372 | 2.1 | 6.7 |
| <45 | 26 200 | 629 | 38 | 42 |
| ≥45 | 2100 | 3743 | 0.33 | 0.56 |
2020 COVID-19 confirmed and probable death rates by age (as at 2 June 2020).5 Of 21 649 deaths, 1 (0.0046%) death with unknown age and 198 (0.91%) with incomplete age information were excluded.
Applying these methods to more contemporary influenza data, the SMR for children (aged ≤17 years) for the 2009 H1N1 influenza pandemic in the USA is 2.1; that is, double the mortality for COVID-19 in New York City in the first 2020 wave. For older age groups, the SMR is less than 0.05, or more than 20-fold lower (Table 2).
Table 2.
Standardized mortality ratios (SMR) of comparator pandemics and epidemics in the USA relative to the first 2020 wave of COVID-19 infection in New York Citya
| Period | Outcome | Age group (years) | Observed deaths | Expected deaths | Crude mortality ratio | SMR |
|---|---|---|---|---|---|---|
| 1918–192 | Estimated influenza pandemic excess pneumonia and influenza deaths | All ages | 546 000 | 102 194 | 2.1 | 5.3 |
| <65 | 538 000 | 48 914 | 7.0 | 11 | ||
| ≥65 | 8000 | 53 280 | 0.13 | 0.15 | ||
| April 2009- April 20107 | Estimated pandemic influenza A(H1N1)pdm09 deaths | All ages | 12 469 | 730 956 | 0.016 | 0.017 |
| ≤17 | 1282 | 597 | 2.1 | 2.1 | ||
| 18-64 | 9565 | 212 473 | 0.048 | 0.045 | ||
| ≥65 | 1621 | 517 886 | 0.0032 | 0.0031 | ||
| 2017–18 influenza season8 | Estimated (preliminary) seasonal influenza deaths | All ages | 61 099 | 857 505 | 0.073 | 0.071 |
| ≤17 | 643 | 592 | 1.1 | 1.1 | ||
| 18-64 | 9554 | 222 400 | 0.046 | 0.043 | ||
| ≥65 | 50 903 | 634 513 | 0.079 | 0.080 |
2020 COVID-19 confirmed and probable death rates by age (as at 2 June 2020).5 Of 21 649 deaths, 1 (0.0046%) death with unknown age and 198 (0.91%) with incomplete age information were excluded.
In New York City, all-age COVID-19 mortality rates remain substantially lower than those documented in the 1918–19 influenza pandemic, recognizing that 1918–19 mortality was inflated by lack of now routine treatments, such as antibiotics, supplemental oxygen and ventilatory support. In children, recent severe seasonal influenza mortality was similar to, and 2009 pandemic mortality double, that documented in the first 3 months of the COVID-19 epidemic. In older people, COVID-19 mortality is more than 10-fold higher than a severe influenza season, and more than 300-fold higher than the 2009–10 influenza pandemic.
Limitations of this study include that deaths from COVID-19 in New York City continue to be reported, so SMRs may change, and ascertainment of COVID-19 deaths may have been reduced by insensitivity of earlier COVID-19 diagnostics,9 with evidence of under-ascertainment of COVID-19-attributable deaths by routine surveillance.10 It is also unknown whether changes in exposure and consequent immunity over time and by place will have an impact on the age-specific risk of severe illness, if infection by this new human coronavirus is sustained in human populations. Observed differences in clinical severity and mortality risk by age among emerging pandemic strains or coronaviruses or influenza viruses may reflect herd immunity conferred on different age cohorts by exposure to previously circulating strains of the same virus.11
In New York City in 1918–19, measures invoked included isolation of infected individuals, enhanced disease surveillance, and education campaigns but, unlike in 2020, not school closures.12,13 Comparisons with 1918–19 must also take into account the prominent role of secondary bacterial infection in influenza mortality and the lack of now routine treatments. However, it seems unlikely that these factors could fully explain a 40-fold lower mortality below 45 years of age for COVID-19 in New York City. Notwithstanding the substantial burden of less severe infections due to both influenza and COVID-19 in different age groups, and the possibility that risk of death may vary over time, the higher age-specific mortality in the young in both the 1918–19 and 2009 influenza pandemics compared with COVID-19 is an important factor for decisions about whole-of-population versus age-targeted vaccination strategies.
Funding
No specific funding was received for this project.
Acknowledgements
The authors would like to acknowledge Donald R Olson for helpful advice on the manuscript.
Author contributions
P.B.M. conceived of the study. D.J.M. conceived of and conducted the analysis and drafted the manuscript. Both authors contributed to the drafting of the manuscript.
Conflict of Interest
None declared.
References
- 1. Plotkin SA, Caplan A. Extraordinary diseases require extraordinary solutions. Vaccine 2020;38:3987–88. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. Simonsen L, Clarke MJ, Schonberger LB, Arden NH, Cox NJ, Fukuda K. Pandemic versus epidemic influenza mortality: a pattern of changing age distribution. J Infect Dis 1998;178:53–60. [DOI] [PubMed] [Google Scholar]
- 3. United States Census Bureau. A Century of Population Change in the Age and Sex Composition of the Nation. 2013. https://www.census.gov/dataviz/visualizations/055/ (10 June 2020, date last accessed).
- 4. Pearce N, Lawlor DA, Brickley EB. Comparisons between countries are essential for the control of COVID-19. Int J Epidemiol 2020, June 29. doi: 10.1093/ije/dyaa108. Online ahead of print. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. NYC Health. COVID-19: Data 2020. https://www1.nyc.gov/site/doh/covid/covid-19-data.page (2 June 2020, date last accessed).
- 6. Olson DR, Simonsen L, Edelson PJ, Morse SS. Epidemiological evidence of an early wave of the 1918 influenza pandemic in New York City. Proc Natl Acad Sci USA 2005;102:11059–63. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Shrestha SS, Swerdlow DL, Borse RH. et al. Estimating the burden of 2009 pandemic influenza A (H1N1) in the United States (April 2009–April 2010). Clin Infect Dis 2011;52:S75–S82. [DOI] [PubMed] [Google Scholar]
- 8. CDC. 2017–2018 Estimated Influenza Illnesses, Medical Visits, Hospitalizations, and Deaths and Estimated Influenza Illnesses, Medical Visits, Hospitalizations, and Deaths Averted by Vaccination in the United States.2019. https://www.cdc.gov/flu/about/burden-averted/2017-2018.htm (10 June 2020, date last accessed).
- 9. Sethuraman N, Jeremiah SS, Ryo A. Interpreting diagnostic tests for SARS-CoV-2. JAMA 2020;323:2249–51. [DOI] [PubMed] [Google Scholar]
- 10. New York City Department of Health and Mental Hygiene (DOHMH) COVID-19 Response Team. Preliminary estimate of excess mortality during the COVID-19 outbreak—New York City, March 11–May 2, 2020. MMWR Morb Mortal Wkly Rep 2020;69:603–05. [DOI] [PubMed] [Google Scholar]
- 11. Lee K-Y, Rhim J-W, Kang J-H. Immunopathogenesis of COVID-19 and early immunomodulators. Clin Exp Pediatr 2020;63:239–50. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Aimone F. The 1918 influenza epidemic in New York City: a review of the public health response. Public Health Rep 2010;125:71–79. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. NYC Health. COVID-19: Prevention and Groups at Higher Risk. 2020. https://www1.nyc.gov/site/doh/covid/covid-19-prevention-and-care.page (4 June 2020, date last accessed).