(Stroke. 2008;39:2197.)
© 2008 American Heart Association, Inc.
Original Contributions |
From the Unit of Health-Care Epidemiology, Department of Public Health (M.J.G., M.D., M.G.), University of Oxford; and the University Department of Clinical Neurology (P.M.R.), Radcliffe Infirmary, Oxford, UK.
Correspondence to Professor Michael J. Goldacre, Unit of Health-Care Epidemiology, Department of Public Health, University of Oxford, Old Road Campus, Old Road, Oxford OX3 7LF, United Kingdom. E-mail michael.goldacre{at}dphpc.ox.ac.uk
| Abstract |
|---|
|
|
|---|
Methods— Analysis of datasets that include both the underlying cause and all other mentioned causes of death (together, termed "all mentions"): the Oxford Record Linkage Study from 1979 to 2004 and English national data from 1996 to 2004.
Results— Mortality rates based on underlying cause and based on all mentions showed similar downward trends. Mortality based on underlying cause alone misses about one quarter of all stroke-related deaths. Changes during the period in the national rules for selecting the underlying cause of death had a significant but fairly small effect on the trend. Overall, mortality fell by an average annual rate of 2.3% (95% confidence interval 2.1% to 2.5%) for stroke excluding subarachnoid hemorrhage; and by 2.1% (1.7% to 2.6%) per annum for subarachnoid hemorrhage. Coding of stroke as hemorrhagic, occlusive, or unspecified varied substantially across the study period. As a result, rates for hemorrhagic and occlusive stroke, affected by artifact, seemed to fall substantially in the first part of the study period and then leveled off.
Conclusion— Studies of stroke mortality should include all mentions as well as the certified underlying cause, otherwise the burden of stroke will be underestimated. Studies of stroke mortality that include strokes specified as hemorrhagic or occlusive, without also considering stroke overall, are likely to be misleading. Stroke mortality in the Oxford region halved between 1979 and 2004.
Key Words: stroke mortality death certificate England
| Introduction |
|---|
|
|
|---|
In contrast, UK stroke mortality rates based on death certification have declined steeply in recent decades.2,27 The decline in the UK appears to be consistent with a 40% decline in population-based stroke incidence and mortality in Oxfordshire, UK, between 1981 to 2004 and 2002 to 2004,28 but national mortality data could have overestimated the time trends in the UK as a whole because of changes in the practice of death certification. Conventional mortality statistics are based on the selection of 1 underlying cause from each death certificate. For some deaths where stroke is regarded by the certifying physician as contributing to death, stroke may not be certified as the underlying cause. Until the mid-1990s, the underlying cause of death was the only measure routinely coded and analyzed for national mortality statistics in England: before then, other causes of death on death certificates were generally disregarded. Because of this, routine statistics, based on underlying cause alone, tend to underestimate mortality attributable to each individual disease. A further potential problem in using data on the underlying cause of death alone is that the coding rules for selecting the underlying cause of death change from time to time. An important example was the rigorous implementation in England in 1984 of rule 3 of the ninth revision of the International Classification of Diseases.29,30 This rule specified that certain diseases, which can be modes of dying (such as pneumonia or heart failure) rather than causes of death, should not be selected as the underlying cause of death if another "primary condition" (such as stroke) is present. The instructions for the compilers of official statistics specify that, if the disease that is certified by the doctor as the underlying cause of death "can be considered a direct sequel of another reported condition, select this primary condition" as the underlying cause.29 There were further changes to the rules for selecting the underlying cause of death in England in 1993 and 2001.31,32
All certified causes of death in the former Oxford Regional Health Authority population were routinely coded from 1979 as part of the Oxford Record Linkage Study (though they did not become available for England as a whole until the 1990s).33 To better understand the apparently large decline in stroke mortality in England, we were therefore able to analyze stroke mortality overall and by subtype, and report on trends in mortality for all mentions of deaths certified as stroke, as well as underlying cause, in Oxford from 1979 and in England from 1996.
| Methods |
|---|
|
|
|---|
The English national data were analyzed from mortality files supplied by the English Office for National Statistics (ONS); the files cover the period 1996 to 2005. Some deaths that occur within a year are not registered until after the end of the year. For that reason, we identified deaths in 2004 when they were in the dataset for 2005; but we confined the analysis presented here, both for England and for Oxford, to an end-year of 2004. Deaths were coded to the ninth revision of the International Classification of Diseases (ICD9) for the years 1979 to 2000 and to ICD10 for 2001 to 2004 for both datasets.29,32
Analysis
For each population, we selected all certificates with a mention of subarachnoid hemorrhage (SAH) (ICD9 430, ICD10 I60), other hemorrhagic stroke (ICD9 431 to 432, ICD10 I61 to I62), occlusive stroke (ICD9 433 to 434, ICD10 I63), unspecified stroke (ICD9 436, ICD10 I64), all cerebrovascular disease including SAH (ICD9 430 to 434,436,438; ICD10 I60 to I64,I69) and all cerebrovascular disease excluding SAH (ICD9 431 to 434,436,438; ICD10 I61 to I64,I69). In the grouped analyses, a death with 2 stroke diagnoses in the group on the death certificate was counted once only as a death from the grouped diagnosis. We age-standardized overall and within broad age groups by applying the age-specific death rates, in 5-year age groups up to the age of 85 years, in each population in each year to the European standard population to calculate standardized rates for each calendar year or group of years. Population denominators were not available in 5-year age groups over 85 years. We also calculated the 95% confidence intervals on the rates. To assess long-term trends and their significance, we calculated the average annual percentage change over time in mortality rates for mentions by fitting regression models to the logarithms of the annual death rates. In the case of the Oxford population, we also grouped the rates into 3 broad time periods defined by differences between them in the national rules for the selection of underlying causes of death—1979 to 1983, 1984 to 1992 and 1993 to 2004.30,31
| Results |
|---|
|
|
|---|
|
Stroke (Excluding Subarachnoid Hemorrhage)
Analysis of death by underlying cause identified only about three-quarters of all certified stroke deaths (Table 1
). The percentage varied significantly according to time period (Table 1
). In the Oxford region, analysis by underlying cause identified 80% (10 749/13 480) of deaths in 1979 to 1983, 84% (20 459/24 236) in 1983 to 1992, and only 75% (23 737/31 689) in 1993 to 2004. As measured by mentions (Figure b, upper line), there was a decline in stroke mortality that was substantial, steady, and consistent over time. As measured by underlying cause alone (Figure b, lower line), in addition to the steady decline there was a downward shift in the death rate between the years 1984 to 1992 and 1993 to 2000 and a smaller upward shift in 2001 to 2004. The downward shift is an artifact attributable to changes in coding rules: it reflects the reduction in stroke deaths that were coded with stroke as the underlying cause (Table 1
). The upward shift in 2001 reflects changes that followed the adoption of the 10th revision of the International Classification of Diseases. The shifts in underlying cause of death are noteworthy because mortality rates based on the underlying cause alone are generally the only rates available for stroke in official English mortality statistics.
|
|
Mortality rates for stroke (excluding SAH) were higher in men than women in each age group up to 85 years (Table 1
). The apparent convergence of rates for men and women in the highest age group probably reflects the fact that we were unable to age-standardize within the over 85s, combined with the fact that there are many more elderly women than men in the population. In the Oxford region from 1979 to 2004, death rates based on mentions fell significantly by an average of 2.3% per year overall. There were larger falls of 3.3% to 4.1% in the age groups 55 to 64 and 65 to 74 years. The decline in mortality rates in people aged 75 years and over was significantly smaller than that in the 55 to 64 and 65 to 74 age groups (as shown by the fact that the confidence intervals on the percentage changes do not overlap; Table 1
). A significant average annual fall of 3.5% overall, based on mentions, was seen in England from 1996 to 2004 (3.7% for men and 3.2% for women). Mortality rates for stroke were about 7% lower in the Oxford region than in England, both for underlying cause (658.4 and 702.7 deaths per million) and mentions (898.2 and 957.7 deaths per million), but the general pattern of decline was similar in the 2 populations.
Specific Types of Stroke as a Percentage of All Stroke
There was substantial variation over the years in the percentage of deaths from stroke where the type of stroke was specified. When a change in stroke mortality overall coincides with a change in the percentage of strokes that are of specified type, the change in mortality for the specified types of stroke may be hard to interpret. For example, in the Oxford region, the type of stroke—occlusive or hemorrhagic—was specified in 41% of all underlying cause stroke deaths in 1979, falling to 33% in 1984, 20% in 1994, and then increasing to 30% in 2004. It follows that, when a fall in overall stroke mortality coincides with an decrease in the percentage of deaths in which the type of stroke is specified, the decline in rates for the individual type of stroke are artifactually exaggerated. This is seen in the first half of the period (Figure d and e) when there was a substantial apparent fall in mortality rates for strokes specified as hemorrhagic or occlusive. When a fall in overall stroke mortality coincides with an increase in the percentage of stroke with specification of type, the fall seen overall will not be reflected as much (if at all) in the trends for the individual types of stroke. This is what is seen for hemorrhagic and occlusive stroke from the late 1980s (Figure d and e) when the mortality rates for each type of stroke appeared to level out.
Table 2 shows summarized mortality rates for occlusive and hemorrhagic stroke subtypes, and for all stroke, in the first and second parts of the study period. The apparent fall in hemorrhagic and occlusive stroke in the first period is exaggerated by changes in certification practice; and the apparent leveling off in the second period is attributable, at least in part, to further changes in practice in recording stroke type on death certificates. Consideration of the individual components in combination—hemorrhagic stroke, occlusive stroke, and stroke of unspecified type (Figure d, e, c)—shows the steady downward trend overall (Figure b; Table 2).
|
Subarachnoid Hemorrhage
Analysis of underlying cause of death identified more than 90% of all deaths with SAH on the death certificate (93.1% 2918/3133 of the deaths in Oxford, 91.1% 20 961/23 003 of those in England; Table 3
). SAH rates, measured as underlying cause, were affected by the coding changes of 1984 and 1993 (Table 3
). The percentage of deaths with SAH on the certificate, that were coded as the underlying cause, was significantly higher in 1984 to 1992 than in the periods before and after.
|
|
Mortality rates for SAH fell substantially in Oxford from 1979 to the late 1980s (Figure f; Table 2). For several years after that, the profile is somewhat inconsistent with a hint of a rise, a plateau, and then a further fall (Figure f). However, numbers of deaths in each year are fairly small and confidence intervals are wide. Considering the period 1992 to 2004 overall (Table 2), there was a significant fall in death rates for SAH. From the late 1990s, the data for SAH mortality both for Oxford and England show a consistent fall. Rates in England fell from 1996 to 2004 with an average annual change, similar in men and women, of –1.8% (95% confidence interval –0.9 to –2.7).
Mortality rates for SAH in people aged 55 years and over were substantially higher in women than men (Table 3
) and, in this respect, show a striking contrast with the higher rates in men than women in other stroke (Table 1
). In people aged less than 55, SAH comprised 36.7% of all SAH and other stroke combined (951/2588 deaths). In people aged 55 years and over, SAH comprised 1.9% of deaths from the combined cerebrovascular diseases (2182/111 792).
| Discussion |
|---|
|
|
|---|
Our data show that deaths attributable to stroke, if considered as only the underlying cause, miss about a quarter of all deaths with stroke as a certified cause. Consequently, in using data on underlying cause of death alone, as the commonly used measure, the population "burden" of stroke as a cause of death is substantially underestimated. However, it is also possible that some mentions might include deaths in people who have had a stroke in the past but where the stroke had little causal relevance to the death. This is particularly likely with long-time intervals between stroke and death.35
The impact of coding changes on death certification is not widely recognized. The coding rule changes in the UK in 1984, 1993, and 2001 had some impact on death certification of stroke as the underlying cause of death, but the effect was fairly small. Nonetheless, because data about all certified causes of death are now available, it is prudent to consider numbers and rates based on mentions as well as those for underlying cause in studies of trends in stroke mortality.
Improvements in stroke prevention and stroke care appear to be largely responsible for the substantial decrease in mortality observed. The Oxford Vascular Study (2004) found reductions in stroke incidence and mortality between 1981 and 2004 to be associated with significant increases in the use of preventive treatments such as antihypertensives and cholesterol lowering drugs and major reductions in premorbid risk factors such as smoking and cholesterol levels.28 The implementation of the National Stroke Audit Program in England should result in continued improvements in care and survival.36
The majority of stroke deaths in the UK do not have the type of stroke on the death certificate (with the exception of subarachnoid hemorrhage). The extent to which stroke is certified without specification of type, and therefore classified and coded as stroke "unspecified," has varied over time and no doubt varies from place to place. It follows that considerable caution is needed in interpreting mortality data for occlusive and hemorrhagic stroke rather than stroke overall. In the past decade the pattern of stroke, overall, better mirrors that of unspecified stroke than that of the subtypes. We can only speculate about why doctors have changed their practice of attributing stroke deaths to particular types of stroke or to stroke generically. It is possible that the introduction of scanning led initially to an increasing tendency to certify subtypes; and that thereafter, paradoxically, experience with scanning led to the recognition in the 1990s that clinical presentation did not necessarily reliably predict pathological subtypes. This might have influenced a shift back to generic certification.
In summary, after considering the impact of artifact, there has been a steady and consistent decline in stroke mortality in England, year on year, over the past 25 years with no evidence of any slow-down.
| Acknowledgments |
|---|
The Unit of Health-Care Epidemiology is funded by the English Department of Healths National Co-ordinating Centre for Research Capacity Development.
Disclosures
None.
Received November 12, 2007; revision received December 17, 2007; accepted December 19, 2007.
| References |
|---|
|
|
|---|
2. Sarti C, Rastenyte D, Cepaitis Z, Tuomilehto J. International trends in mortality from stroke, 1968 to 1994. Stroke. 2000; 31: 1588–1601.
3. Stegmayr B, Asplund K. Exploring the declining case fatality in acute stroke. Population-based observations in the northern Sweden MONICA Project. J Intern Med. 1996; 240: 143–149.[CrossRef][Medline] [Order article via Infotrieve]
4. Gillum RF, Sempos CT. The end of the long-term decline in stroke mortality in the United States. Stroke. 1997; 28: 1527–1529.
5. Reitsma JB, Limburg M, Kleijnen J, Bonsel GJ, Tijssen JG. Epidemiology of stroke in The Netherlands from 1992 to 1994: the end of the decline in stroke mortality. Neuroepidemiology. 1998; 17: 121–131.[CrossRef][Medline] [Order article via Infotrieve]
6. McGovern PG, Burke GL, Sprafka JM, Xue S, Folsom AR, Blackburn H. Trends in mortality, morbidity and risk factor levels for stroke from 1960 through 1990: The Minnesota Heart Survey. JAMA. 1992; 268: 753–759.
7. Broderick JP. Stroke trends in Rochester, Minnesota, 1945 to 1984. Ann Epidemiol. 1993; 3: 476–479.[Medline] [Order article via Infotrieve]
8. Kodama K. Stroke trends in Japan. Ann Epidemiol. 1993; 3: 524–528.[Medline] [Order article via Infotrieve]
9. Feigin VL, Wiebers DO, Whisnant JP, O'Fallon WM. Stroke incidence and 30-day case- fatality rates in Novosibirsk, Russia, 1982 through 1992. Stroke. 1995; 26: 924–929.
10. Tuomilehto J, Sarti C, Torppa J, Salmi K, Puska P. Trends in stroke mortality and incidence in Finland in the 1970s and 1980s. Ann Epidemiol. 1993; 3: 519–523.[Medline] [Order article via Infotrieve]
11. Numminen H, Kotila M, Waltimo O, Aho K, Kaste M. Declining incidence and mortality rates of stroke in Finland from 1972 to 1991. Results of 3 population-based stroke registers. Stroke. 1996; 27: 1487–1491.
12. Stegmayr B, Asplund K, Wester PO. Trends in incidence, case fatality rate, and severity of stroke in Northern Sweden, 1985–1991. Stroke. 1994; 25: 1738–1745.[Abstract]
13. Wolf PA, D'Agostino RB, O'Neal MA, Sytkowski P, Kase CS, Belanger AJ, Kannel WB. Secular trends in stroke incidence and mortality. The Framingham Study. Stroke. 1992; 23: 1551–1555.
14. Harmsen P, Tsipogianni A, Wilhelmsen L. Stroke incidence rates were unchanged, while fatality rates declined, during 1971–1987 in Göteborg, Sweden. Stroke. 1992; 23: 28–32.
15. Bonita R, Broad JB, Beaglehole R. Changes in stroke incidence and case-fatality in Auckland, New Zealand, 1981–91. Lancet. 1993; 342: 1470–1473.[CrossRef][Medline] [Order article via Infotrieve]
16. Feigin VL, Lawes CM, Bennett DA, Anderson CS. Stroke epidemiology: a review of population-based studies of incidence, prevalence and case-fatality in the late 20th century. Lancet Neurol. 2003; 2: 43–53.[CrossRef][Medline] [Order article via Infotrieve]
17. Terént A. Increasing incidence of stroke among Swedish women. Stroke. 1988; 19: 598–603.
18. Jørgensen HS, Plesner A-M, Hübbe P, Larsen K. Marked increase of stroke incidence in men between 1972 and 1990 in Frederiksberg, Denmark. Stroke. 1992; 23: 1701–1704.
19. Eisenblätter D, Heinemann L, ClaBen E. Community-based stroke incidence trends from the 1970s through the 1980s in East Germany. Stroke. 1995; 26: 919–923.
20. Brown RD, Whisnant JP, Sicks JD, O'Fallon WM, Wiebers DO. Stroke incidence, prevalence, and survival: secular trends in Rochester, Minnesota, through 1989. Stroke. 1996; 27: 373–380.[Medline] [Order article via Infotrieve]
21. Kôrv J, Roose MD, Kaasik AE. Changed incidence and case-fatality rates of first-ever stroke between 1970 and 1993 in Tartu, Estonia. Stroke. 1996; 27: 199–203.
22. Rastenyte D, Tuomilehto J, Sarti C, Cepaitis Z, Bluzhas J. Trends in the incidence and mortality of stroke in Kaunas, Lithuania, 1986–1993. Cerebrovasc Dis. 1996; 6: 13–20.[Medline] [Order article via Infotrieve]
23. Medin J, Nordlund A, Ekberg K. Increasing stroke incidence in Sweden between 1989 and 2000 among persons aged 30 to 65 years: evidence from the Swedish Hospital Discharge Register. Stroke. 2004; 35: 1047–1051.
24. Johansson B, Norrving B, Lindgren A. Increased stroke incidence in Lund-Orup, Sweden, between 1983 to 1985 and 1993 to 1995. Stroke. 2000; 31: 481–486.
25. Lemesle M, Milan C, Faivre J, Moreau T, Giroud M, Dumas R. Incidence trends of ischaemic stroke and transient ischaemic attacks in a well-defined French population from 1985 through 1994. Stroke. 1999; 30: 371–377.
26. Marini C, Triggiani N, Cimini N, De Santis I, Ciancarelli I. Carolei. Increasing incidence of first stroke in a population study. Cerebrovasc Dis. 2000; 10: 1.[Medline] [Order article via Infotrieve]
27. Charlton J, Murphy M, Khaw K, Ebrahim, S, Davey Smith G. Cardiovascular diseases. In: Charlton J, Murphy M, eds. The Health of Adult Britain 1841–1994. London: The Stationary Office. 1997; 2: 60–81.
28. Rothwell PM, Coull AJ, Giles MF, Howard SC, Silver LE, Bull LM, Gutnikov SA, Edwards P, Mant D, Sackley CM, Farmer A, Sandercock PA, Dennis MS, Warlow CP, Bamford JM, Anslow P. Change in stroke incidence, mortality, case-fatality, severity and risk factors in Oxfordshire, UK from 1981 to 2004 (Oxford Vascular Study). Lancet. 2004; 363: 1925–1933.[CrossRef][Medline] [Order article via Infotrieve]
29. World Health Organisation Manual of the international statistical classification of diseases, injuries, and causes of death. 1975 Revision. Geneva: World Health Organisation, volume 1. 1977; 699–706.
30. Office of Population Censuses and Surveys (1985) Mortality Statistics. Cause 1984. Series DH2 (11). London: HMSO: v–ix.
31. Office for National Statistics (1996) Mortality Statistics. Cause 1993 (revised) and 1994. Series DH2 (21). London: HMSO: xxv–xxxiii.
32. World Health Organization. International Statistical Classification of Diseases and Related Health Problems. Tenth Revision. Geneva: World Health Organization, 1993, volume 2: 30–88.
33. Goldacre MJ, Duncan ME, Cook-Mozaffari P, Griffith Ml. Trends in mortality rates comparing underlying-cause and multiple-cause coding in an English population 1979–1998. J Public Health Med. 2003; 25: 249–253.
34. Sturgeon JD, Folsom AR. Trends in hospitalization rate, hospital case fatality, and mortality rate of stroke by subtype in Minneapolis-St. Paul, 1980–2002. Neuroepidemiology. 2007; 28: 39–45.[CrossRef][Medline] [Order article via Infotrieve]
35. Halkes PH, Van Gijn, Kappelle LJ, Koudstaal PJ, Algra A. Classification of cause of death after stroke in clinical research. Stroke. 2006; 37: 1521–1524.
36. Royal College of Physicians. National Clinical Guidelines for Stroke, II Edition. Prepared by the Intercollegiate Stroke Working Party. London: RCP, 2004.
This article has been cited by other articles:
![]() |
J. D. Lewsey, P. S. Jhund, M. Gillies, J. W.T. Chalmers, A. Redpath, L. Kelso, A. Briggs, M. Walters, P. Langhorne, S. Capewell, et al. Age- and Sex-Specific Trends in Fatal Incidence and Hospitalized Incidence of Stroke in Scotland, 1986 to 2005 Circ Cardiovasc Qual Outcomes, September 1, 2009; 2(5): 475 - 483. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Harmsen, L. Wilhelmsen, and A. Jacobsson Stroke Incidence and Mortality Rates 1987 to 2006 Related to Secular Trends of Cardiovascular Risk Factors in Gothenburg, Sweden Stroke, August 1, 2009; 40(8): 2691 - 2697. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. B. Slot, E. Berge, P. Sandercock, S. C. Lewis, P. Dorman, M. Dennis, and on behalf of the Oxfordshire Community Stroke Proj Causes of Death by Level of Dependency at 6 Months After Ischemic Stroke in 3 Large Cohorts Stroke, May 1, 2009; 40(5): 1585 - 1589. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. D. Lewsey, M. Gillies, P. S. Jhund, J. W.T. Chalmers, A. Redpath, A. Briggs, M. Walters, P. Langhorne, S. Capewell, J. J.V. McMurray, et al. Sex Differences in Incidence, Mortality, and Survival in Individuals With Stroke in Scotland, 1986 to 2005 Stroke, April 1, 2009; 40(4): 1038 - 1043. [Abstract] [Full Text] [PDF] |
||||
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
|
Stroke Home | Subscriptions | Archives | Feedback | Authors | Help | AHA Journals Home | Search Copyright © 2008 American Heart Association, Inc. All rights reserved. Unauthorized use prohibited. |