Excess winter mortality: influenza or cold stress? Observational study
BMJ 2002; 324 doi: https://doi.org/10.1136/bmj.324.7329.89 (Published 12 January 2002) Cite this as: BMJ 2002;324:89All rapid responses
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Dear Editor
Re GC Donaldson, WR Keatinge Excess winter mortality: influenza or
cold stress? Observational study. BMJ 2002;324:89-90
We write to challenge the method of calculation of influenza
attributed mortality due to influenza in the paper published by Donaldson
and Keatinge. Data were used covering the period 1970 to 1999 but the
regression analysis was stated to start on 1 January 1990 and (unless a
misprint) thus has only explored the relationship in the last ten years.
The authors conclude by suggesting that 2.4% of winter excess
mortality in south-east England is attributed to influenza and
quantitatively this, if it can be extrapolated, is equivalent to a
national average for England and Wales (population 53 million) of
approximately 1620 deaths per year. This estimate contrasts with those
obtained by other groups using different methodologies: Tillett et al
estimated an average of 12000 deaths attributable to influenza between
1968/69 and 1977/781; Nicholson estimated an annual average of 13800
deaths between 1975/76 and 1989/902; and Fleming estimated an annual
average of 12500 deaths between 1989/90 and 1998/993.
Donaldson and Keatinge have estimated total deaths attributable to
influenza from deaths certified as due to influenza. They have
presumably used deaths allocated to influenza as a primary cause according
to the national protocol for allocating deaths by cause. Several points
are relevant.
1 The data base extended over thirty years. There has been
considerable variation in the attribution of deaths from influenza by
doctors over this period. In addition, primary cause mortality from
respiratory disease has been affected by coding procedural changes in 1984
and 1993, such that in this intervening ten year period the numbers of
deaths allocated to respiratory causes was approximately half those in the
period before 1984 and the period subsequent to 19934.
2 The data are based on south east England, but this area and
population size is not defined. An average of 5.1 deaths per million
(estimated average over the last ten years) is equivalent to approximately
50 deaths per year distributed over 365 days in a population of 10
million. The authors indicate that 143 deaths per million were registered
as due to influenza in 1976. There is an implication therefore that the
acknowledged deaths in that year were thirty times those in the average of
the last ten years. While there are recognized to be substantial
differences between influenza activity (and related mortality) between
“epidemic” years and “average” years, the difference would not be expected
to be as large as this. This finding questions the credibility of the
methods used to estimate the average in the last ten years.
3 Crucially, we do not accept that the number of deaths attributed
specifically to influenza provides a reliable indication of the extent of
occurrence of influenza related deaths. Influenza mortality needs to be
examined in relation to influenza virus circulation and epidemic periods.
Data are not presented in the paper on the distribution of influenza
reported deaths in relation to these periods.
Based on the authors’ estimate of excess winter deaths from all
causes (an average of 1265 per million over the last ten years, equivalent
to 67000 nationally in England and Wales), our estimate of 12500 deaths
attributable to influenza is equivalent to 19% rather than 2.4%, of
total excess winter deaths.
Yours sincerely
DM Fleming*
KW Cross*
J M Watson**
NQ Verlander**
*The Birmingham Research Unit of The Royal College of General
Practitioners, Lordswood House, 54 Lordswood Road, Harborne, Birmingham
B17 9DB.
**PHLS Communicable Disease Surveillance Centre, 61 Colindale Avenue,
London NW9 5EQ
1. Tillett HE, Smith JWG, Gooch CD. (1983) Excess deaths
attributable to influenza in England and Wales: age at death and certified
cause. Int J Epidemiol 1983;12:344-52.
2. 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.
3. Fleming DM. The contribution of influenza to combined acute
respiratory infections, hospital admissions and deaths in winter. Commun
Dis Public Health 2000; 3:32-8.
4. OPCS. Mortality statistics: cause 1993 (revised) and 1994, series
DH2 no 21 1996. ppxxv-xxvii. HMSO, London.
Competing interests: No competing interests
Authors' reply
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.
G C Donaldson
senior research associate
W R Keatinge
emeritus professor
Medical Sciences, Queen Mary and Westfield College (University of
London), London E1 4NS
w.r.keatinge@qmw.ac.uk
1 Office of Population Censuses and Surveys. Mortality statistics:
cause. London: OPCS, 1996: table 4. (Series DH2 No 11.)
Competing interests: No competing interests