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. 2002 Jun 1;324(7349):1337. doi: 10.1136/bmj.324.7349.1337

Excess winter mortality

Method of calculating mortality attributed to influenza is disputed

D M Fleming 1,2,3, K W Cross 1,2,3, J M Watson 1,2,3, N Q Verlander 1,2,3
PMCID: PMC1123286  PMID: 12039836

Editor—We challenge the method that Donaldson and Keatinge used to calculate mortality due to influenza.1 Data covering the period 1970-99 were used, but the authors state that the regression analysis started on 1 January 1990. On the basis of the 10 year analysis, they estimate an average of 1265 per million excess winter deaths from all causes, equivalent to 67 000 nationally in England and Wales. They say that 2.4% of this excess (equivalent to a national average of 1620 deaths per year) is attributable to influenza.. This estimate contrasts with those obtained by other groups: Tillett et al estimated an annual average of 12 000 deaths (1968-9 to1977-8)2, Nicholson 13 800 (1975-6 to1989-90)3, and Fleming 12 500 (1989-90 to 1998-9).4 The estimate of 12 500 is equivalent to 19% of the 67 000 total excess winter deaths, rather than 2.4%.

Donaldson and Keatinge estimated total deaths attributable to influenza from deaths certified as due to influenza. They presumably used deaths allocated to influenza as the primary cause of death according to the national protocol for allocating deaths by cause. Several points are relevant.

Firstly, the attribution of deaths from influenza varied considerably over the 30 years reported. Furthermore, the coding of mortality by primary cause involved procedural changes in 1984 and 1993, such that the numbers of deaths allocated to respiratory causes between these years were roughly half those before 1984 and after 1993.5

Secondly, the data are based on south east England, but this area and population size are not defined. The 10 year average of 5.1 deaths per million equates to 50 deaths a year (distributed over 365 days) in a 10 million population. The authors indicate that 143 deaths per million were registered as due to influenza in 1976, 30 times their estimate of the annual average; a difference so large as to question the credibility of the methods used to estimate the average.

We do not accept that the number of deaths attributed to influenza provides a reliable indication of the extent of deaths related to influenza. Mortality from influenza needs to be examined in relation to virus circulation, the epidemic periods in which it is circulating, and the impact on all-cause mortality.

References

  • 1.Donaldson GC, Keatinge WR. Excess winter mortality: influenza or cold stress? Observational study. BMJ. 2002;324:89–90. doi: 10.1136/bmj.324.7329.89. . (12 January.) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Tillett HE, Smith JWG, Gooch CD. Excess deaths attributable to influenza in England and Wales: age at death and certified cause. Int J Epidemiol. 1983;12:344–352. doi: 10.1093/ije/12.3.344. [DOI] [PubMed] [Google Scholar]
  • 3.Nicholson KG. Impact of influenza and respiratory syncytial virus on mortality in England and Wales from January 1975 to December 1990. Epidemiol Infect. 1996;116:51–63. doi: 10.1017/s0950268800058957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Fleming DM. The contribution of influenza to combined acute respiratory infections, hospital admissions and deaths in winter. Commun Dis Public Health. 2000;3:32–38. [PubMed] [Google Scholar]
  • 5.Office of Population Censuses and Surveys. Mortality statistics: cause 1993 (revised) and 1994. London: HMSO; 1996. : xxv-xxvii. (Series DH2 No 21.) [Google Scholar]
BMJ. 2002 Jun 1;324(7349):1337.

Authors' reply

G C Donaldson 1, W R Keatinge 1

Editor—Influenza epidemics usually occur in particularly cold weather. The key difference between our analysis and the usual assessments of mortality attributable to influenza is that ours makes allowance for the excess deaths that would have been caused, in the absence of an influenza epidemic, by low daily temperatures.

Deaths from influenza were extracted before 1979 as ICD-8 codes 470-474 and thereafter as ICD-9 code 487; allowance was made for changes in coding instructions outside 1984-92 by using the specific conversion factor 0.997 for influenza,1-1 not the larger adjustment for the broad category of respiratory deaths mentioned by Fleming et al. Fleming et al ask what we define as south east England. It comprises Greater London, Hertfordshire, Essex, Kent, Sussex, Hampshire, Surrey, Berkshire, Oxfordshire, Buckinghamshire, and Bedfordshire.

Yes, the regression analysis started from 1970, although we focused on results since 1990. We used deaths certified as primarily due to influenza as the explanatory variable in the regression to calculate total deaths related to influenza. A theoretical alternative is to use the prevalence of influenza. Viral sampling is important, but we could find no systematic daily measurement of that in the whole population throughout the last 30 years. It would in any case be difficult to allow for different lethalities of different strains of influenza and for different sensitivities and immunities of particular age groups to them. Variation with time in the tendency to certify doubtful deaths as being due to influenza might produce some error in our analysis, but hardly one large enough to affect our conclusion. This was that deaths related to influenza over the past 10 years accounted for only a small fraction of total mortality related to cold.

A check for any major error can be made by seeing whether our estimated rise in mortality related to influenza in an epidemic year corresponds with the rise in total excess winter mortality that year. Our paper shows that it did, most clearly in the major epidemic year 1976. Both mortalities increased by a similar amount that year, compared with the preceding and following years. This is consistent with deaths related to influenza being at or near the number we calculated and not at the higher figures sometimes suggested previously. It is, we think, common ground that before 1970 epidemics of influenza were more frequent and more lethal than they are now.

References

  • 1-1.Office of Population Censuses and Surveys. Mortality statistics: cause. London: OPCS; 1996. : table 4. (Series DH2 No 11.) [Google Scholar]

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