(Stroke. 2001;32:613.)
© 2001 American Heart Association, Inc.
Original Contributions |
Is There a Temporal Pattern in the Occurrence of Subarachnoid Hemorrhage in the Southern Hemisphere?
Pooled Data From 3 Large, Population-Based Incidence Studies in Australasia, 1981 to 1997
From the Clinical Trials Research Unit, University of Auckland, Auckland, New Zealand. See Appendix for a complete list of study participants.
Correspondence to Prof Valery Feigin, Clinical Trials Research Unit, University of Auckland, Private Bag 92019, Auckland, New Zealand. E-mail v.feigin{at}ctru.auckland.ac.nz
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionAppendix 1References |
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Background and Purpose—Publications on the temporal pattern of the occurrence of subarachnoid hemorrhage (SAH) have produced conflicting results. Variations between studies may relate to the relatively small numbers of SAH cases analyzed, including those in meta-analyses.
Methods—We identified all cases of SAH from 3 well-designed population-based studies in Australia (Adelaide, Hobart, and Perth) and New Zealand (Auckland) during 3 periods between 1981 and 1997. The diagnosis of SAH was confirmed with CT, cerebral angiography, cerebrospinal fluid analysis, or autopsy in all cases. Information on the time of occurrence of each event was obtained. Risk ratios (RRs) and 95% CIs were calculated using Poisson regression, with age, sex, smoking status, and history of hypertension entered in the model as covariates.
Results—A total of 783 cases of SAH were registered. Age- and sex-adjusted RRs of SAH occurrence were highest in the period between 6 AM and 12 MIDNIGHT (RR 3.2, 95% CI 2.4–4.3) and in winter and spring (RR 1.3, 95% CI 1.1–1.5; RR 1.3, 95% CI 1.1–1.5; respectively). No particular pattern of SAH occurrence was observed according to the day of the week. Restriction of the analyses to proved aneurysmal SAH did not substantially change the point estimates.
Conclusions—Circadian and circaseptan (weekly) fluctuations of SAH occurrence in the southern hemisphere are similar to those in the northern hemisphere, but the occurrence of SAH in Australasia exhibits clear seasonal (winter and spring) peaks.
Key Words: chronobiology • circadian rhythm • epidemiology • subarachnoid hemorrhage
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionAppendix 1References |
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Knowledge of the temporal pattern of the occurrence of subarachnoid hemorrhage (SAH) may provide insight into triggering factors and lead to the development of new preventive strategies for this devastating disorder. Previous studies1 2 3 4 have yielded inconsistent and/or inconclusive results on diurnal and seasonal variations in the occurrence of SAH in various countries. This can be explained by differences in study designs (hospital-based studies versus population-based studies), by differences between the countries in environmental conditions5 and stroke risk factor profiles, and by relatively small numbers of events available for analysis. The use of hospital-based data to study temporal patterns of SAH occurrence is prone to bias because it does not include a substantial proportion (
12%)6 of patients who
die from SAH before reaching the hospital. Another limitation of
previous studies is that they were restricted primarily to populations
in Europe and North America. It remains unclear whether temporal
patterns of SAH occurrence observed in these countries can be applied
to populations from other parts of the world with less extremes in
climatic conditions. The purpose of the present study was to determine whether there is a particular circadian (diurnal), circaseptan (weekly), or circannual (monthly, seasonal) pattern in the occurrence of SAH and whether these temporal variations of SAH occurrence in Australasian populations are different from those in other populations. To address these issues, we pooled data from several population-based SAH incidence studies from the Australasian Co-operative Research on Subarachnoid Haemorrhage Study (ACROSS) and 2 stroke registry studies in Auckland.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionAppendix 1References |
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The ACROSS (1995 to 1998) and Auckland (1981 to 1983 and 1991 to 1993) stroke incidence studies are population-based prospective registers7 8 that were performed in 4 major centers in Australia and New Zealand: Adelaide (South Australia), Hobart (Tasmania), Perth (Western Australia), and Auckland (New Zealand), which have a current total population of >3 million residents. The populations are well defined administratively and have similar health care systems, allowing the registration of all incident cases of SAH (whether hospitalized or nonhospitalized, fatal or nonfatal). National census data (by sex and 5-year age band strata) for the study periods were available for each of the cities. Attention was given to cross-checking of all potential sources of information about incident cases of SAH, including inpatient and outpatient medical record forms, computerized hospital separation data, and official death records for the study areas.
According to standard
criteria,9 SAH was defined as
an abrupt onset of severe headache and/or loss of consciousness, with
or without focal neurological signs; CT, autopsy, or lumbar
puncture revealed focal or generalized blood in the
subarachnoid space. Excluded from the analysis were
patients with SAH definitely originating from sources other than an
intracranial aneurysm, including primary
intracerebral hemorrhage, arteriovenous
malformations, trauma, infections, bleeding diatheses, and neoplasms.
Patients in whom an aneurysm could be identified with cerebral
angiography, autopsy, or the presence of a localized collection
of blood in a fissure on CT were included and analyzed
separately. Each event during the study period was further classified
as being the patient’s first-ever or a recurrent SAH. For patients
with multiple events, the index event was defined as that event that
occurred nearest to the time when the patient was first registered. A
recurrent event was one in which SAH occurred 
28 days after the onset
of the index event. In this study, we analyzed first-ever and
recurrent SAH events together.
In the studies analyzed, all patients had a known day of onset of SAH. Every attempt was made to establish the exact time of onset of SAH (abrupt onset of headache and/or loss of consciousness). For patients with SAH who were found on awakening, the time of awakening was used as the time of onset. Patients with unknown time of SAH onset were not included in the analysis on circadian rhythm of SAH occurrence. The time of onset was categorized into 4 periods of 6 hours (night 00:00 to 05:59 AM, morning 06:00 to 11:59 AM, afternoon 12:00 NOON to 17:59 PM, and evening 18:00 to 23:59 PM) and 12 intervals of 2 hours. Months of onset were categorized into 4 seasons: summer (December to February), autumn (March to May), winter (June to August), and spring (September to November).
Statistical Analysis
Two strategies were used to evaluate temporal pattern
of SAH onset. The first strategy was based on a calculation of rate
ratios (RRs) using Poisson regression to allow for
underdispersion and overdispersion, in which incidence rates of SAH
occurrence for a particular time interval were compared with that of a
reference interval and corresponding 95% CIs were estimated. The
population at risk was included in the models as offsets. Because
previous studies showed age and sex-specific fluctuations in the
occurrence of
SAH1 10 and blood
pressure
levels,11 12 we
evaluated effects of age and sex by means of stratified
analyses and adjustment (age of the patients was conventionally
dichotomized into 2 groups: 15 to 64 years and 65+ years). Data on
smoking status (ever smoked in past year or not) and reported
hypertension (ever told of having high blood pressure or not) were
included as covariates. Information on smoking, history of
hypertension, and the time of SAH onset was obtained from self- or
(proxy) report, hospital records, and other sources where available
(eg, coroner’s report). For statistical analyses, SAH patients
with missing information on smoking status (42 subjects, or 5.4%) were
assumed to be nonsmokers, and patients with missing information on
hypertension (41 subjects, 5.2%) were assumed to be normotensive;
these assumptions deviated effect estimates toward the null hypothesis.
In the second strategy, a similar analysis was conducted with
generalized additive
models.13 The time of day
was split into 24 periods of 1 hour, and the year was split into 12
months. SAH events with unknown time of onset during the 24-hour day
were excluded from analysis of circadian fluctuation of SAH
occurrence. Months and time of day were smoothed by means of a periodic
spline and introduced into the Poisson regression as covariates (the
functions for constructing the periodic spline bases in S-PLUS are
available at
http://www.biostat.wustl.edu/s-news/s-news-archive/199906/msg00241.html).
The corresponding rate ratios and curves at ±2 SEs were plotted. The
population at risk was also included in the model as an offset. All
calculations were performed with SAS
6.1214 and S-PLUS 2000
Professional Release 215
(for Windows) software.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionAppendix 1References |
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Overall, 783 cases of SAH were recorded in the ACROSS study and Auckland stroke incidence studies. The mean±SD age of the patients was 54.5±16.3 years (range of means between studies 50.9 to 56.7 years). Most events (560, or 72%) occurred in patients aged
64 years. Overall, the female-to-male ratio was 2:1 and did not
change significantly during the study period or differ between
centers.
The exact time of onset of SAH during the day was not known
in 44 women (8.9%) and in 30 men (10.4%) who were alone at the onset
and were found dead or unconscious, but circumstances in which these
patients were found (where known) suggest that the majority of them
developed SAH during the daytime.
Table 1
and
Figure 1 show that the majority of the events occurred in
the morning between 8 AM
and 12 NOON, whereas the
lowest frequency of the events was observed between 12
MIDNIGHT and 6
AM This pattern was most
pronounced in older subjects, especially in women. Differences in the
risk of SAH during the 2-hour periods were more masked than those for
6-hour periods. The incidence of SAH was almost evenly distributed
throughout the week
(Table 2) in all age- and sex-specific strata. The incidence
of SAH was highest in June and July
(Table 3 and
Figure 2). The seasonal distribution of SAH indicates that
the highest incidence rates were observed in the winter (10.3 cases per
100,000 person-years: 12.8 in women, 7.8 in men) and spring (10.3 cases
per 100,000 person-years: 12.4 in women, 8.1 in men), whereas in the
summer and autumn, these rates were 8.2 (10.0 and 6.2) and 8.9 (11.3
and 6.3), respectively. The degree of fluctuations by month and season
in older patients was more prominent than that in younger
patients.
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Table 4 shows crude and age- and sex-adjusted risks of SAH
occurrence by time of day, day of the week, and season. The risk of SAH
occurrence was significantly higher in late morning (RR 3.3, 95% CI
2.4–4.3), afternoon (RR 2.7, 95% CI 2.0–3.6), and evening (RR 2.2,
95% CI 1.7–3.0) compared with early morning. The risk of SAH
occurrence in the late morning was more pronounced in older women and
younger men. Although analyses stratified by age and sex of the
patients showed only a marginally significant increase in the risk of
SAH occurrence in the winter in men and spring in women, age- and
sex-adjusted rates indicated that the risk of SAH is significantly
higher in these seasons than in the summer. Additional adjustment for
hypertension and smoking status resulted in a decrease in the risk of
SAH in the spring, although the risk remained statistically significant
(RR 1.27, 95% CI 1.03–1.57). In all age- and sex-specific strata, the
risk of SAH occurrence was almost equally distributed during the week,
but on Sundays, the risk of SAH was higher than that on other days (RR
1.3, 95% CI 1.0–1.6). Throughout the week, older subjects had a
slightly higher risk than younger subjects. Restriction of the sample
population to only SAH patients who had proven aneurysm rupture
(75% of all patients in ACROSS) as well as adjustment for smoking
status and hypertension did not significantly change the point
estimates for any of the time intervals studied. Recoding of patients
with missing values of smoking and hypertension as
nonsmokers/normotensives, or the reverse, made little difference in the
temporal relative risks.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionAppendix 1References |
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This population-based study in part confirms and extends previous findings. The results indicate that SAH occurrence in the southern hemisphere exhibits clear circadian (late morning peak) and circannual (winter and spring peaks) patterns, but there is no particular circaseptan pattern of SAH occurrence in this part of the world. Although circannual and circaseptan patterns of SAH in the southern hemisphere are similar to those in the northern hemisphere, the observed seasonal fluctuations of SAH occurrence have reached a significant level, with the most pronounced risk of SAH in the winter. Given similar circadian and circannual patterns observed in other ecological studies on ischemic stroke,3 16 17 18 19 20 21 22 intracerebral hemorrhage,3 16 17 20 21 22 23 and acute myocardial infarction,24 25 26 27 28 29 30 31 our data suggest that the occurrence of all major vascular events may be influenced by common triggering factors. On the other hand, the absence of a circaseptan pattern in the occurrence of SAH and a substantial risk of an event during working hours and late afternoon are suggestive of differences in circadian triggering factors for this disorder as opposed to other stroke subtypes and myocardial infarction. Because blood pressure levels exhibit similar diurnal fluctuations, with an increase on awakening and during working activity,11 12 32 33 34 35 36 an increase in blood pressure may be a factor for aneurysm formation and/or rupture (in our study,
75% of patients had proven
aneurysm rupture as the cause for SAH). Increased exposure to
smoking, physical activity, and alcohol while awake have been
shown11 12 32 35
to be associated with an elevation in blood pressure and may trigger
rupture of a critically weakened aneurysm wall. The risk of SAH occurrence was highest during late morning and was moderate during early and late afternoon. These findings are somewhat different from results of a recently published meta-analysis by Vermeer et al,37 in which no significant risk of SAH occurrence was observed in the late afternoon, a nadir of the risk was found around noon, and a late morning peak in the occurrence of SAH was not that attenuated. These subtle discrepancies in results of the studies can be attributed to the fact that the meta-analysis was based primarily on hospital-based series, in which selection bias was unavoidably introduced. However, our findings of a low risk of SAH occurrence at night (early morning hours) and of no particular rhythm in its occurrence by day of the week are in line with the meta-analysis suggesting that weekly patterns of SAH occurrence are not affected by selection biases and weekend stress. Results of another meta-analysis20 based on 31 published studies indicated that there is an increased risk of the onset of acute ischemic/hemorrhagic stroke during the late morning and that there is a significantly lower risk of stroke during the night. However, the authors did not analyze SAH separately from intracerebral hemorrhage. Our data suggest that sex and age may contribute differently to the circadian pattern of SAH occurrence. The risk of SAH during wakening hours was more pronounced in younger men and older women, although the differences were not statistically significant. This may be related to differences in variability of blood pressure and exposure to lifestyle/environmental factors, such as smoking11 32 and physical activity,35 between the groups. Hemorrhages that did not waken the person or were not apparent until morning were considered to have occurred at the time of awakening. This did not influence the result that most hemorrhages occur during the morning, as there were very few patients in this category.
Our study is the first to show significant seasonal fluctuation in the occurrence of SAH. That there is no statistically significant difference in the seasonal risk of SAH between various age- and sex-specific analyzed strata suggests that men and women of younger and older age groups have a similar susceptibility to seasonal environmental factors. However, the peak of SAH occurrence in younger people was most prominent in the spring, whereas in older persons, the peak was most prominent in the winter. Data from the Oxfordshire Community Stroke Project23 (n=33) indicated that there was a tendency for SAH to occur during the spring, but overall seasonality was nonsignificant. No clear seasonal variations in the incidence of SAH were observed in another small (n=64) population-based study of SAH in Russia.38 However, when data on larger patient groups were reported, a more certain seasonal pattern emerged. In the largest population-based study of SAH to date (1105 events) in Finland,16 the occurrence of SAH tended to be higher during the winter than during other seasons, but even this study was underpowered to detect a significant difference between the seasons. A clear seasonal pattern in the admission of patients with SAH was observed in several large hospital-based studies in the northern hemisphere39 40 41 and in our large population-based study in the southern hemisphere. The consistent seasonal variations between the hemispheres support the hypothesis that environmental changes play a significant role in the occurrence of SAH. In this regard, elevated blood pressure during the winter42 and other months with low ambient temperature43 may play important roles as triggers for SAH. This suggestion is further corroborated by the relatively infrequent use of heating of houses in Australasia during the winter and spring. Results of a recent hospital-based study in Italy44 suggest that the higher incidence of intracerebral hemorrhage in the colder months is due to the effect of low temperature on blood pressure. Although no relationship between SAH occurrence and weather parameters (ambient temperature, relative humidity, and air pressure) was revealed in a recent small population-based study in Russia,45 the total number of SAH cases in the study was too small (n=64) to allow any definite conclusions to be made. Some studies suggest that temperature may nonspuriously influence stroke incidence or mortality rates17 18 46 and that infection and inflammation contribute to the seasonal variation in stroke mortality rates46 and may be an important predisposing risk factor for brain infarction.47 48 49 50 Although no one factor is likely to explain a winter/spring peak for SAH, a close resemblance to the circadian variations of respiratory diseases in Australasia51 and risk of SAH occurrence suggests that inflammation may be a risk factor for growth and rupture of an intracranial aneurysm. Of course, seasons may also alter human behavioral response to climatic conditions (eg, indoor smoking, physical activity, and alcohol intake).
In summary, our study suggests that the risk of SAH occurrence in the southern hemisphere exhibits clear circadian (late morning peak) and circannual (winter and spring peaks) patterns but no particular circaseptan pattern. The avoidance of low environmental temperatures in the winter and spring (through the use of well-warmed houses) may reduce the risk of SAH. Our study also confirms and extends findings from previous ecological studies on SAH and other stroke subtypes in the northern hemisphere that suggest all stroke subtypes have common triggering biological and/or environmental factors. Available information suggests that in a population at high risk for SAH, variation in certain lifestyle and environmental factors might act as a synchronizer to endogenous circannual and circadian rhythms. To identify potentially preventive factors that precipitate SAH, further studies are warranted to investigate relationships among weather parameters, behavioral factors, diet, respiratory disease, and circadian/circannual variations in the incidence of aneurysmal and nonaneurysmal SAH. If the rhythmic processes that drive the circadian/circannual rhythm of SAH onset can be identified, their modification may delay or prevent the occurrence of SAH.
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Appendix 1 |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionAppendix 1References |
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Committee Members, Principal Investigators, and Study Coordinators of ACROSS: Steering Committee
C. Anderson (study chair); N. Anderson, R. Bonita, D. Dunbabin, G. Hankey, and K. Jamrozik. Study coordinators: J. Bennett (study manager), D. Healy, and S. Rubenach (Adelaide); J Sansom and J. Flecker (Hobart); J. Harvey, J. Linto, G. Mann, and K. White (Perth); and S. Hawkins and C. Mulholland (Auckland). Neurosurgical investigators: B. Brophy (Flinders Medical Centre), J. Liddell (Royal Hobart Hospital), E. Mee (Auckland Hospital), G. McCulloch (Queen Elizabeth Hospital), N. Knuckey (Sir Charles Gairdner Hospital), and P. Reilly (Royal Adelaide Hospital).
Auckland Stroke Study Investigators
R. Bonita, J. Broad, R. Beaglehole, and N.
Anderson.
Clinical Centres for the Two Studies
Ashord Hospital, Flinders Medical Centre, Memorial
Hospital, Repatriation General Hospital, Queen Elizabeth Hospital, and
the Royal Adelaide Hospital (Adelaide,
South Australia); the Royal Hobart Hospital, Calvary
Hospital, and St Helen’s Private Hospital
(Hobart, Tasmania); Fremantle
Hospital, Royal Perth Hospital, St John of God Hospital Subiaco, St
John of God Hospital Murdoch, and Sir Charles Gairdner Hospital
(Perth, Western Australia); and Auckland
Hospital, North Shore Hospital, Middlemore Hospital, Green Lane
Hospital, and Waitakare Hospital
(Auckland, New Zealand).
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Acknowledgments |
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This work was supported by grants from the National Health and Medical Research Council of Australia, the Health Research Council of New Zealand, the National Heart Foundation of New Zealand, and the Sylvia and Charles Viertel Charitable Foundation of Queensland, Australia. We thank Dr Henrik Aalborg Nielsen (Department of Mathematical Modelling, Technical University of Denmark), who provided the functions to construct the periodic spline bases in S-PLUS. We are indebted to the study investigators and coordinators for their dedication and performance and the help provided from nursing, administration, and medical records staff of the clinical centers.
Received July 27, 2000; revision received November 17, 2000; accepted December 8, 2000.
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References |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionAppendix 1References |
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