Stroke incidence and case-fatality among Indigenous and non-indigenous populations in the Northern Territory of Australia,

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1 Stroke incidence and case-fatality among Indigenous and non-indigenous populations in the Northern Territory of Australia, Jiqiong You 1 *, John R. Condon 2, Yuejen Zhao 1, and Steven L. Guthridge 1 Background Stroke is a leading cause of death and disability in Australia. The impact of stroke on the Australia Indigenous people is, however, unclear. Aim This study describes hospital-based stroke incidence and case fatality in the Northern Territory population in Australia. Methods Retrospective study of Northern Territory residents with a first-ever stroke episode and case fatality among Northern Territory residents in Results The rate ratio of age-adjusted stroke incidence between Indigenous and non-indigenous populations was 2 8 for men and 2 7 for women, similar to those reported elsewhere in Australia. The rate ratio increased to 3 8 (95% confidence interval: ) after adjusting for multiple risk factors. There was no change in annual incidence between 1999 and 2011 for either non-indigenous (incidence rate ratio per year 1 01, 95% confidence interval: ) or Indigenous people (incidence rate ratio: 1 00, 95% confidence interval: ), although incidence did increase for non-indigenous people in the year age group (incidence rate ratio:1 09, 95% confidence interval: ) and for Indigenous people in the year age group (incidence rate ratio:1 03, 95% confidence interva ). The case fatality rate decreased from 22% in 1999 to 12% in In-hospital deaths were more common among; older and Indigenous people, for those with other chronic diseases, and from haemorrhagic stroke compared with ischemic stroke. Conclusions In the Northern Territory, as elsewhere in Australia, Indigenous Australians are more likely than other Australians to suffer a stroke. Lack of falling in incidence in the Northern Territory population highlights the importance for ongoing comprehensive primary and acute care in reducing risk factors and managing stroke patients. Key words: acute, case-fatality, incidence, Indigenous Australian, outcome, stroke subtypes Introduction Stroke occurs when brain tissue is damaged by a blocked (ischemic) or ruptured artery (haemorrhagic) (1). Globally, stroke is the third most common cause of death after ischemic heart disease and cancer (2). Stroke was the second leading cause of death among women and the third among men in Australia in the past three decades (3). In 2010, there were 8304 deaths in Australia Correspondence: Jiqiong You*, Northen Territory Government, Department of Health, PO Box 40596, Casuarina, NT 0811, Darwin, NT 0811, Australia. jiqiong.you@nt.gov.au 1 Department of Health, Northen Territory Government, Darwin, NT, Australia 2 Menzies School of Health, Darwin, NT, Australia Received: 28 August 2014; Accepted: 14 November 2014; Published online 15 January 2015 Conflict of interest: None declared. DOI: /ijs with an underlying cause of stroke. These deaths were 6% of all deaths and 18% of all cardiovascular disease deaths ( deaths), making stroke the second most common cause of cardiovascular death after coronary heart disease ( deaths) (4). Stroke mortality has been decreasing in Australia for several decades. Since 1977 the age-standardized death rate for stroke has decreased by an annual average of 4% for both men and women (4). This decrease has been attributed to: reduction in the level of risk factors such as tobacco consumption; improved control of hypertension and blood clots; and improvements in medical treatment for stroke (5). Stroke mortality has also declined in the Northern Territory (NT) over the last two decades, for both non- Indigenous and Indigenous populations (6). There are no national data on the population-based incidence of stroke, but two regional studies provide some information. The northeast Melbourne community-based stroke incidence study was conducted in the mid-1990s (7,8), and the Perth community stroke study was conducted around 1990 and repeated in the late 1990s (9,10). Both studies found evidence of a decline in stroke incidence. Information about stroke incidence among Indigenous (Aboriginal and Torres Strait Islander) Australians is even more limited. There has been one reported study of stroke incidence, from Western Australia (WA), which used linked hospital and death data from 1997 to 2002 to identify incident stroke cases (11). The age-standardized stroke incidence rate was 2 6 [95% confidence interval (CI), ] times higher for Indigenous than non-indigenous men and 3 0 (95% CI, ) times higher for women. There have been no reports of incidence trend or case-fatality for Indigenous Australians. In this study we used hospital inpatient data to identify firstever strokes for the NT population to estimate stroke incidence and time trends (by type of stroke), and case fatality rate (CFR, expressed as the proportion of stroke related in-hospital deaths) for Indigenous and non-indigenous patients. Methods Identification of the first-ever stroke admission The first-ever stroke episodes (the index admission ) among NT residents for treatment of stroke were identified from inpatient data from all five NT public hospitals; data were not available from the one private hospital in the NT. The public hospitals used a single patient information system and a unique client identification number (the Hospital Registration Number). All inpatient episodes for NT residents with either a primary or secondary diagnosis code of stroke were identified between 1991 and Stroke diagnosis codes were International Classification of Diseases, Ninth Revision (ICD9) codes and 436 (to June 1998) and ICD10 code I60 I64 (from July 1998). Type of stroke 716 Vol 10, July 2015, This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

2 J. You et al. was classified as ischemic, haemorrhagic or unspecified, based on diagnosis codes. Transient ischemic attacks (TIAs) were excluded. Inpatient episodes for each individual were collated, and the first episode with a diagnosis of stroke was identified. Patients with a stroke diagnosis in the eight-year period prior to 1 January 1999 were excluded. The eight-year clearance period was applied in order to exclude existing/prevalent cases from subsequent analysis (11). We also excluded non-nt residents and patients aged less than 15 years at the time of their first stroke diagnosis, as recommended by the World Health Organization (12). Data items obtained from the inpatient data set for each firstever stroke were date of birth (to calculate age at onset of stroke), gender, Indigenous status, locality of residence, date of admission, mode of separation (to identify in-hospital deaths), Charlson score (to measure the presence of chronic disease comorbidity) and an indicator for the order of diagnosis code for stroke (primary or secondary). Locality of residence was reclassified as urban (the major towns of Darwin, Palmerston and Alice Springs) or remote. Statistical analysis We calculated the incidence rate of first-ever stroke by age group, gender, Indigenous status, year of diagnosis and remoteness. The denominator was derived from the Australian Bureau of Statistics (ABS) estimated resident population (13). Incidence rates were age-adjusted using direct age-standardization to the ABS 2001 Australian population. To enable comparison of stroke incidence in the NT with previous results from WA (11), we also calculated age-adjusted incidence rates using the world standard population for the period (adjusted for the proportion of the out-of-hospital incidence). We used negative binomial regression for multivariate analysis of stroke incidence. The model included terms for age at onset of stroke, gender, Indigenous status, year of onset, remoteness and an interaction term for Indigenous status by year of onset. The interaction term was included because the relationship between stroke incidence and year of onset was found to be different for Indigenous compared with non-indigenous patients. We calculated CFR directly from mode of hospital separation and used logistic regression to estimates the odds ratio of in-hospital death adjusted for the risk factors mentioned above. Ethics approval The study was approved by the Human Ethics Committee of the NT Department of Health and the Menzies School of Health (HREC ). Results We identified 1962 NT residents with a first-ever stroke admission between 1999 and 2011: 56% were non-indigenous, 57% men and 60% urban residents. First-ever strokes accounted for 58% of all stroke admissions. For 84% of first episodes stroke was the primary diagnosis. For 17% of episodes the patient died in hospital at the index admission. Hospital-based stroke incidence In univariate analysis, the age-adjusted incidence of first-ever stroke was much higher for Indigenous than non-indigenous people (Table 1). For both Indigenous and non-indigenous people, incidence was higher for: men than women and older than younger age groups. For non-indigenous people the incidence of ischemic stroke was approximately 50% higher than that of haemorrhagic or unspecified stroke, but for Indigenous people there was little difference in incidence between types of stroke. There was no evidence for an overall change in stroke incidence over Table 1 Number and age-adjusted incidence rate of first-ever strokes by demographic characteristics, Northern Territory, Non-Indigenous Indigenous n % ASR* n % ASR* Gender Male ( ) ( ) Female (99 124) ( ) Age group (years) (8 13) (42 58) ( ) ( ) ( ) ( ) Remoteness Urban ( ) ( ) Remote ( ) ( ) Study period ( ) ( ) ( ) ( ) Type of stroke Ischemic (53 66) (94 124) Haemorrhagic (32 42) (83 109) Unspecified (35 46) (87 117) Total ( ) ( ) *ASR, age-standardized rate (per population) adjusted to the 2001 Australian population. Vol 10, July 2015,

3 J. You et al. Fig. 1 Incidence 1 of all first-ever strokes combined and by type of stroke, Northern Territory, and Australia, Age-adjusted incidence rate, adjusted to the 2001 Australian standard population. 2 Sourced from Australian Institute of Health and Welfare Table 2 Stroke incidence rates by Indigenous status, Northern Territory and Western Australia, Indigenous Non-Indigenous Rate Rate* 95%CI Rate* 95%CI Ratio Northern Territory (first-ever stroke) Male 336 ( ) 119 ( ) 2 8 Female 263 ( ) 97 (82 113) 2 7 Western Australia (nonfatal stroke) Male 304 ( ) 117 ( ) 2 3 Female 267 ( ) 88 (85 90) 3 0 *Age-adjusted incidence per adjusted to the world standard population. Adjusted for stroke cases not admitted to hospital, using the proportion of non-admitted cases reported in the Western Australia study. Sourced from Katzenellenbogen, Vos, Somerford et al. Stroke. 2011;42 (6): CI, confidence interval. time for either Indigenous or non-indigenous people (Fig. 1). The incidence of first-ever stroke in the NT was similar to the previously reported rates in WA for both non-indigenous and Indigenous populations (Table 2). Multivariate analysis for all types of stroke combined was consistent with the univariate results. When adjusted for other factors, stroke incidence was higher for men and Indigenous people, and increased with age (Table 3). Overall stroke incidence was similar between remote and urban areas. The incidences of haemorrhagic and ischemic stroke were higher for urban residents and unspecified stroke higher for rural residents. There was a 5% increase in incidence for ischemic stroke and 4% decrease for unspecified stroke for Indigenous people, which may reflect the availability of more specific stroke diagnoses in recent years. For non-indigenous people, there was 2% annual increase in incidence of ischemic stroke. Excess stroke incidence in the Indigenous population was much greater in younger than older age groups; the incidence rate ratio was 4 9 in the years age group compared with 1 6 in the 65 years and over age group for all strokes combined (Table 4). 718 Vol 10, July 2015,

4 J. You et al. Table 3 Negative binomial regression analysis with incidence rate ratio of first-ever stroke by type of stroke, Northern Territory, All stroke Haemorrhagic Ischemic Unspecified Age (per year) Non-Indigenous 1 09( ) 1 07 ( ) 1 10 ( ) 1 11 ( ) Indigenous 1 06 ( ) 1 05 ( ) 1 06 ( ) 1 08 ( ) Gender (female vs. male) 0 76 ( ) 0 77 ( ) 0 63 ( ) 0 95 ( ) Indigenous status (Ind vs. non-ind) 3 83 ( ) 4 42 ( ) 3 88 ( ) 2 96 ( ) Residence (remote vs. urban) 1 01 ( ) 0 78 ( ) 0 81 ( ) 1 89 ( ) Year of the first stroke (per year) Non-Indigenous 1 01 ( ) 1 01 ( ) 1 02 ( ) 0 99 ( ) Indigenous 1 00 ( ) 0 99 ( ) 1 05 ( ) 0 96 ( ) Base age 50 and base year Incidence rate ratio with 95% confidence interval in parentheses. Table 4 Negative binomial regression analysis* with incidence rate ratio by type of stroke and age groups, Northern Territory, All stroke Haemorrhagic Ischemic Unspecified years of age Gender (female vs. male) 0 95 ( ) 0 90 ( ) 0 80 ( ) 1 64 ( ) Indigenous status (Ind vs. non-ind) 4 92 ( ) 4 96 ( ) 4 72 ( ) 4 58 ( ) Residence (remote vs. urban) 1 06 ( ) 1 05 ( ) 0 86 ( ) 1 79 ( ) Year of the first stroke (base 2005) Non-Indigenous 1 09 ( ) 1 11 ( ) 1 07 ( ) 1 11 ( ) Indigenous 0 98 ( ) 0 96 ( ) 1 02 ( ) 0 94 ( ) Gender (female vs. male) 0 73 ( ) 0 85 ( ) 0 54 ( ) 0 84 ( ) Indigenous status (Ind vs. non-ind) 4 38 ( ) 5 72 ( ) 4 17 ( ) 3 05 ( ) Residence (remote vs. urban) 1 05 ( ) 0 73 ( ) 0 98 ( ) 2 00 ( ) Year of the first stroke (base 2005) Non-Indigenous 1 01 ( ) 0 98 ( ) 1 04 ( ) 1 02 ( ) Indigenous 1 03 ( ) 1 01 ( ) 1 10 ( ) 0 97 ( ) 65+ Gender (female vs. male) 0 85 ( ) 0 60 ( ) 0 81 ( ) 1 13 ( ) Indigenous status (Ind vs. non-ind) 1 55 ( ) 1 70 ( ) 1 65 ( ) 1 47 ( ) Residence (remote vs. urban) 0 82 ( ) 0 67 ( ) 0 55 ( ) 1 58 ( ) Year of the first stroke (base 2005) Non-Indigenous 1 01 ( ) 1 03 ( ) 1 01 ( ) 0 97 ( ) Indigenous 0 96 ( ) 0 92 ( ) 0 98 ( ) 0 96 ( ) *Base year Incidence rate ratio with 95% confidence interval in parenthesis. There was no evidence for change in stroke incidence, in either Indigenous or non-indigenous populations, over time. Results for individual stroke types were generally similar to those for all types combined, with some exceptions (Table 3). There was some evidence for variation by locality of residence with the incidence of haemorrhagic and ischemic stroke higher for urban residents and unspecified stroke higher for rural residents. There was also some variation in the time trend by stroke type and by Indigenous status. For Indigenous people, incidence increased by 5% per year for ischemic stroke but decreased by 4% per year for unspecified stroke. The annual rate change was different by age group (Table 4). For the years age group, stroke incidence increased by 9% per year for non-indigenous people but there was no evidence for changes among Indigenous people; consequently, the rate ratio between Indigenous and non-indigenous people decreased from 9 times in 1999 to 2 8 times in In the years age group, incidence remained stable for non-indigenous people, while for Indigenous people there was a substantial increase in incidence of both ischemic stroke and all stroke types combined. There were no clear trends in stroke incidence in the 60 years and over age groups. Case fatality rates Figure 2 indicates that the stroke CFR decreased over the 12-year study period from 22% in 1999 to 12% in 2011, with the Indigenous CFRs higher than the non-indigenous rates. In multivariate analysis, CFR for stroke was higher for: people with haemorrhagic than ischemic or unspecified stroke; older than younger people; those with higher Charlson scores; and for stroke patients identified from a secondary diagnosis (Table 5). Gender and remote residence were not associated with risk of in-hospital death. There Vol 10, July 2015,

5 J. You et al. percent Indigenous Non-Indigenous Fig. 2 Case fatality rates by Indigenous status and year, Northern Territory, Table 5 Logistic regression analysis* with odds ratio of case-fatality for first-ever strokes, Northern Territory, All stroke Haemorrhagic Ischemic Unspecified Age (per year) 1 02 ( ) 1 01 ( ) 1 02 ( ) 1 06 ( ) Gender (female vs. male) 1 08 ( ) 1 08 ( ) 1 22 ( ) 0 89 ( ) Indigenous status (Ind vs. non-ind) 1 25 ( ) 1 38 ( ) 0 91 ( ) 1 27 ( ) Residence (remote vs. urban) 1 14 ( ) 1 09 ( ) 1 07 ( ) 1 70 ( ) Year of the first stroke (base 2005) 0 96 ( ) 0 95 ( ) 0 99 ( ) 0 97 ( ) Order of stroke diagnosis (secondary vs. primary) 2 75 ( ) 1 89 ( ) 4 26 ( ) 2 43 ( ) Charlson score 1 11 ( ) 1 16 ( ) 1 04 ( ) 1 13 ( ) Unspecified stroke 1 00 Haemorrhagic stroke 3 55 ( ) Ischemic stroke 1 15 ( ) *Base age 50 and base year % confidence interval in parenthesis. was no evidence of excess in-hospital death for Indigenous people after adjustment for other factors. The CFR from all stroke declined at 4% annually over the study. The decrease was more evident for haemorrhagic than ischemic or unspecified stroke (Table 5). Discussion The incidence of first-ever stroke was much higher for Indigenous than non-indigenous people in the NT between 1999 and 2011, and did not decrease over time for either group. However, CFR decreased considerably for both Indigenous and non-indigenous stroke patients during the study. Incidence of stroke (all types) For the NT non-indigenous population, stroke incidence was similar to that reported elsewhere in Australia. In 2009, the Australian Institute of Health and Welfare reported a national stroke incidence of 140 per (4), similar to NT non-indigenous incidence in this study (138 per ). NT non-indigenous stroke incidence was also similar to that previously reported for the WA non-indigenous population (11), using the same age standard. For the NT Indigenous population, the incidence of first-ever stroke was 4 1 times higher than the non-indigenous population, confirming the previously reported excess stroke incidence for Indigenous people in WA (11). Stroke incidence was similar for the NT and WA Indigenous populations. The incidence rate ratio (Indigenous compared with non-indigenous) in the NT was 2 8 for men and 2 7 for women, similar to the ratio of 2 6 and 3 0 reported in WA for men and women respectively. There were also methodological differences between the NT and WA studies so the incidence rates reported for the two populations are not exactly comparable. Nonfatal incidence in WA study excluded those new cases who died within 28 days from the first diagnosis. In the NT, since the hospital data was not linked to the death data, we were unable to report 28 days nonfatal incidence. Second, the WA study included people suffering a first stroke who died without admission to hospital; we could not include such cases in the NT study; although we did adjust the NT stroke incidence rate for out-of-hospital stroke new cases. No data was available to assess whether the proportion of non-admitted stroke cases in the NT was similar to WA. There was little evidence for a change in the stroke incidence for either NT Indigenous or non-indigenous people, which 720 Vol 10, July 2015,

6 J. You et al. contrasts with the decrease in stroke incidence reported nationally (4). Type of stroke As reported elsewhere (8,14,15), the incidence for ischemic stroke was much higher than haemorrhagic stroke. This was true for both Indigenous and non-indigenous populations in our study. The incidence of haemorrhagic stroke remained stable through the study period, while the incidence of ischemic stroke increased for both Indigenous and non-indigenous populations. The increase may be partly the result of reclassification of stroke of unspecified cause, with the increased availability of advanced diagnostic technology that enabled more specific diagnosis of the type of stroke. Part of the increase in ischemic stroke incidence may also be related to increasing alcohol consumption (16) and alcohol-attributable hospitalization (17). The more accurate diagnosis of type of stroke would be expected to result in an increase in diagnosis of both haemorrhagic and ischemic strokes; and it is possible that the real incidence in haemorrhagic stroke has declined through interventions including improved hypertension management at both primary and acute care settings. Comparison with ischemic heart disease For non-indigenous people, the increased incidence of first-ever stroke for younger people together with the unchanged incidence for older age groups was alarming. This finding was congruent with a previously reported increase in the incidence of ischemic heart disease in the NT non-indigenous population aged under 40 years (increasing 5% annually) (18); these two diseases share many common risk factors (such as smoking, high blood pressure, diabetes and obesity) (19). There have also been recent international reports of a growing number of young people affected by stroke, particularly in low socioeconomic countries (20,21). This increase is associated with increasing prevalence of risk factors such as obesity, diabetes, hypertension, and consumption of alcohol, tobacco and other illicit drugs. By contrast it is unclear why the NT Indigenous population had an increased risk of the incidence of ischemic heart disease while the incidence of stroke has been stable in recent decades (increase at 7% annually) (18). Although stroke incidence has not increased for the Indigenous population, it has remained at very high levels, while it has been falling for the total Australian population, which may reflect lack of progress in reducing the prevalence of risk factors (22), balanced by more active treatment for hypertension, high cholesterol, diabetes and renal disease as evidence by improving survival rates. Rheumatic heart disease also occurs at high rates in the NT Indigenous population (23) and also may be contributing to the incidence of stroke. Case fatality rates In contrast to stroke incidence, there was considerable improvement in CFR for patients presenting with first-ever stroke, among both Indigenous and non-indigenous people. Reduced CFR may indicate earlier diagnosis of stroke or more effective treatment to manage stroke patients or both. The proportion of stroke patients who died in hospital increased with increasing age, and was greater for Indigenous than non-indigenous patients. However, unlike stroke incidence (which was higher for men), the odds ratio of in-hospital death were similar between men and women. Our study included stroke patients identified from both primary (84%) and secondary diagnoses (16%) in the hospital inpatient data set. A previous study showed that using only primary diagnosis to identify strokes (in particular ischemic stroke) in hospital administrative data would exclude patients with higher levels of comorbidity (24). Therefore, studies that identified strokes from only the primary diagnosis may underestimate stroke incidence and CFR. For stroke patients identified from secondary diagnoses in our study, the three most common primary diagnoses recorded in the hospital data were cardiovascular disease, injury and infectious disease. Our finding recognized that strokes identified from both primary and secondary diagnoses had poorer outcome than those identified from only primary diagnosis (24). Limitations There are several limitations to this study. First, national deaths data were unavailable for linkage to the NT hospital inpatient data, so we could not estimate the number of stroke deaths that occurred before the patient reached hospital and therefore the true incidence of stroke in the NT will be underestimated. The WA study reported that 9 12% of stroke patients were not admitted to hospital in (9 11). Second, we included only the first-ever stroke so that subsequent admissions for a new or a different type of stroke were not identified. Third, we were unable to access admission data from the single NT private hospital; however, the hospital did not provide emergency services, and patients suffering from an acute stroke would have been first assessed in the adjacent public hospital. The impact of not including private hospital data was small and negligible. Finally, since this study was a hospital-based study, there was a potential selection bias in comparing CFR between the earlier and later years. As indicated by the Charlson score, the severity of stroke increased over the study period, which suggested that the improvement in CFR might be underestimated. Conclusion We have compared long-term trends in first-ever stroke incidence for Indigenous with non-indigenous populations, using a consistent data source and methodology for a 12-year period. Stroke was much more common in NT Indigenous than in the non- Indigenous population. In contrast to the national trends of decreasing stroke incidence, there is no evidence for falling incidence in either NT population, but increased for the NT younger population. This highlights the importance for ongoing comprehensive primary and acute care in reducing risk factors and managing stroke patients. The decline in case-fatality for both populations is a positive outcome, which is consistent with improvements in acute care services in recent years. References 1 National Stroke Foundation 2012a. What is a stroke? Viewed 26 July World Health Organization. The Atlas of Heart Disease and Stroke. Geneva, World Health Organization, Vol 10, July 2015,

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