Does Socioeconomic Position Affect Knowledge of the Risk Factors and Awareness of the Warning Signs of Stroke in the WHO European Region? A Systematic Literature Review

Background: Cerebrovascular accidents are one of the leading causes of death worldwide. People with a lower socioeconomic position (SEP) (i.e. with regards to education, income and occupation) are at a higher risk of having a stroke and have worse clinical outcomes compared to the general population. Good knowledge levels about stroke risk factors and warning signs are key to prolonging life and reducing health issues caused by stroke. This systematic review examined differences in knowledge of stroke risk factors and awareness of stroke warning signs with regards to SEP in the WHO European region. Methods: MEDLINE, Embase, Web of Science, PsycINFO and CINAHL were systematically searched to find articles looking at knowledge of risk factors and/or awareness of warning signs of stroke, with results broken down by SEP. A title and abstract screen, and, if appropriate, a full text screen, of these results was carried out, as well as screening reference lists of included studies. Only studies in the English language and those based in the WHO European region were included. Results: Screening identified 2,118 records. In the final review, 20 articles were included, with 67,309 study participants between them. Out of 17 studies that looked at stroke risk factors, 11 found increasing knowledge to be associated with higher SEP, four found no difference by SEP, one showed a mixed pattern and one outlier study found increasing knowledge of risk factors to be associated with a lower SEP. Out of 19 studies that looked at stroke warning signs or symptoms, 15 found there to be better awareness of warning signs with a higher SEP, three found there to be no difference, and the same outlier study found increasing knowledge of warning signs with a lower SEP. Studies that seemed to have a higher quality rating found increasing knowledge of stroke with a higher SEP. Conclusions: In the WHO European region, better knowledge of stroke risk factors and awareness of warning signs is associated with a higher SEP. Public health campaigns and educational interventions aiming to increase stroke awareness should be targeted at people with a lower SEP.

incidence of strokes is expected to increase due to the increasing proportion of Europeans living into their 70 s (2). Between the years 2015 to 2035, it has been estimated that there will be a 45% increase in the number of stroke deaths and a 34% increase in the total number of stroke events across countries in the European Union (2).
For individuals who survive a stroke, damage to the brain can lead to functional problems, higher brain dysfunction, post-stroke fatigue and depression (3). As a consequence, strokes lead to not only loss of functional, social and financial independence for patients and their families, but also have a significant economic impact. The total cost of stroke in the European Union in 2015 was estimated as 45 billion euros (2). This estimate included 20 billion euros for direct health care costs, 15.9 billion euros for informal care and 9.4 billion euros in productivity losses due to death and morbidity.
Decreasing both the incidence of stroke and associated long-term disability, therefore, is essential to not only protect patients and their families but also to reduce the economic burden.
Stroke is a preventable condition, however, studies suggest that knowledge about risk factors in the general population, in some countries in Europe, is sub-optimal (2,(4)(5)(6). Modifiable stroke risk factors include hypertension, smoking and physical inactivity (7). Stroke patients who recognise the warning signs of stroke and access treatment early also have better outcomes (8,9). Warning signs of stroke include facial weakness, arm weakness and slurred speech (10). The faster a patient having a stroke can be treated, the more likely they are to survive and minimise the long-term effects (11). Alteplase, a thrombolytic medication used in the treatment of ischaemic strokes (which make up 85% of strokes) (12), must be administered within 4.5 hours of symptom onset (13). It is therefore essential to reduce the time between onset of stroke and treatment. Evidenced-based public health interventions to improve knowledge in the European population about stroke risk factors and warning signs are likely to be key to reducing the burden of strokes to individuals and populations within Europe.
Studies have shown that people with a lower socioeconomic position (SEP) not only have an increased risk of stroke (14), but also have poorer clinical and functional outcomes than those with a higher SEP after having had a stroke (15). It is important, therefore, to examine differences in stroke awareness across groups by SEP, as this could increase understanding of why those with a lower SEP are at a higher risk of having poorer outcomes.
Inequalities in health knowledge by SEP are important to examine, as systematic reviews looking at sociodemographic factors have indicated that social inequalities in stroke awareness by gender (16) and ethnic minorities (17) exist. Women were found to have better knowledge of stroke risk factors and warning signs compared to men (16). This is perhaps not surprising as women visit healthcare services more regularly than men (18), therefore are more likely to acquire information with regards to stroke knowledge whilst there. Ethnic minorities, similar to people with a lower SEP, include a high concentration of at-risk individuals for stroke (17). Mass media campaigns such as 'Act FAST' (facial weakness, arm weakness, speech problems, time to call 999) in the UK (10) were shown to have limited effectiveness in black, minority and ethnic communities (BMEs) (19). A systematic review of health promotion interventions aimed at increasing stroke awareness in ethnic minorities reported that the evidence was limited and inconclusive (17).
The authors of this paper are unaware of any systematic reviews analysing stroke knowledge with regards to SEP in the WHO European region. A systematic review was carried out in 2005 of the existing literature at the time that included looking at the relationship between educational level and stroke knowledge (20). It has been 15 years, however, since that paper was published, and in the interim there has been a significant increase in the literature. There have also been notable public health interventions since 2005, such as the Act FAST campaign (10), which aimed to increase stroke knowledge. The authors believe it is still important to address this important evidence gap, and therefore undertook a systematic review of the literature concerning knowledge of risk factors and awareness of the warning signs of stroke amongst the population of the WHO European region. The study looks specifically at whether this knowledge and awareness varies amongst groups of different SEP.

Methods
The study aimed to provide a synthesis of the available research addressing knowledge of stroke risk factors and awareness of stroke warning signs by SEP in the WHO European region and to assess the quality of the included studies. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist (21) was used as a guide whilst carrying out the review.

Search strategy
A search of the published literature was undertaken on 22/10/2019, using the databases MEDLINE, Embase, Web of Science, PsycINFO and CINAHL (see Additional File 1 for search terms). In addition to this, a hand search of the reference lists of included studies, as well as of the similar systematic reviews on gender (16) and ethnic minorities (17) was carried out in order to identify any further studies.
The PEO(S) framework (Population, Exposure of interest, Outcome, Study designs) (22) was used to explore the research question "Does stroke awareness differ in adults across different SEPs?". In this paper the term 'socioeconomic position' (SEP) is used instead of 'socioeconomic status', as it includes education, income and occupation-based measures, thus is a broader term (23).
The studies had to fulfil the inclusion criteria listed in Table 1. These criteria included adult humans, countries in the WHO European region (Table 2), SEP, knowledge of stroke risk factors, awareness of stroke warning signs, cross-sectional studies, cohort studies and randomised-controlled trials (RCTs).
Exclusion criteria, in terms of population, included studies just involving children, individuals who have had a stroke or transient ischaemic attack (TIA), family members or carers of stroke patients, and countries outside the WHO European region. Further exclusion criteria included studies not analysing at least one aspect of SEP, stroke awareness following an intervention (if no baseline data), studies not broken down by risk factors and/or warning signs, case studies, editorials, qualitative research and systematic reviews. Although in the medical profession, 'signs' and 'symptoms' have different meanings (24), the terms were used interchangeably in the search. There was no limit on the publication years for this project, however the search was limited to studies in the English language only.

Risk of bias
The critical appraisal tool for cross-sectional studies, AXIS (26), was used to assess the quality of the included studies. This tool includes 20 questions that systematically assess research papers, judge the reliability of studies and assess the worth and relevance of studies. The questions address the introduction, methods, results, discussion and other aspects of the studies. This tool received a high level of consensus between medical groups and can be used for systematic reviews (26).
Furthermore, all the studies included in this systematic review were cross-sectional, so it was deemed an appropriate tool to use.
As the measures of SEP, as well as risk factors and warning signs, were too diverse and many studies did not publish data suitable to include in a meta-analysis, a narrative synthesis of the results was carried out, with tables summarising the results of individual studies. The principal summary measures of the results, for the knowledge of risk factors and awareness of warning signs of stroke by SEP, included difference in percentage scores, odds ratios with confidence intervals and p-values.

Study selection
The PRISMA flow diagram (21) was used to record the results of the study selection (Fig. 1 (41), Denmark (42) and Estonia (43).
The overall number of respondents across all 20 studies was 67,309. The number of respondents in the studies ranged from 212 respondents (33) to 28,090 respondents (6). Participant selection was reported to be random for all studies except one which was snowball (i.e. non-random) (36), one which used consecutive patients (31) and one which was unclear (37). The sampling strategy for six (5,32,33,38,39,43) of the random sampling studies was not clearly reported. The majority of the studies only questioned adults. However, four of them (5,34,39,43) included both adults and children. All studies included both genders; with all except one study (40) having a higher proportion of females.
Socioeconomic position type and stroke awareness assessment Table 3 displays the studies' characteristics with regards to the aspect of socioeconomic position that results were given by, type of questioning and stroke knowledge. All studies gave results by educational level as a measure of SEP, except one (29) that gave professional status only. Aside from education, two studies also gave results by income (28,36), one also by both income and professional status (35) and one (41) also by deprivation level. Of the 20 studies, 16 of them (4, 5, 28-33, 35, 37-43) included both knowledge of risk factors and awareness of warning signs of stroke. One study (6) looked only at risk factors and three (27,34,36) looked only at warning signs. Only one study (38), out of those in which it was relevant, described information about non-response bias. In two studies (31,35) this was not applicable as the response rate was high. Results were internally consistent for all except three studies (5,27,29). In all 20 studies (4-6, 27-43), the results for the analyses described in the methods were presented, and the authors' discussions and conclusions were justified by the results. Limitations of studies were discussed in all except two studies (35,41)

Results of individual studies
The most commonly recognised risk factors for stroke across the studies were hypertension, high cholesterol, obesity and smoking (see Additional File 4). Out of eight studies (6,28,29,31,35,36,38,40) that asked open questions with regards to risk factors and gave a percentage of the number of people able to give at least one correct risk factor of stroke, the results ranged from 50.8% (31) to 89.5% (38). This means that in all of these eight studies, over half of participants were able to correctly identify a risk factor of stroke without being prompted.
The most commonly recognised warning signs of stroke across the studies were weakness of one side of body, speech problems and headache. Out of the eight studies (5,28,29,31,35,36,38,40) that asked open questions with regards to stroke warning signs and gave a percentage of the number of people able to give at least one correct warning sign of stroke, the results ranged from 32.6% (29) to 89.1% (36). Five of these studies (5,28,35,36,40) gave results over 50%; meaning that over half of participants in these studies were able to correctly identify a warning sign of stroke without being prompted. The other three studies (29,31,38) gave results of less than 50%. Out of the five studies (30,33,34,37,42) that asked closed questions with regards to stroke warning signs and gave a percentage of the number of people able to correctly identify at least one warning sign from a list, the results ranged from 68.7% (30) to 98% (42). This means that over two-thirds of participants in all of these studies were able to correctly identify at least one stroke warning sign when given a list.

Knowledge of stroke risk factors by SEP
Out of the 17 studies (4-6, 28-33, 35, 37-43) that assessed knowledge of risk factors for stroke, 11 of them (6, 28-31, 33, 35, 39-41, 43) found there to be better knowledge with a higher SEP ( Table 4). All of these studies looked at education except for one article (29), which looked only at professional status, and found that 'home-based occupations' (such as housewives, pensioners, unemployed and disabled people) were linked to a lower knowledge of stroke risk factors in comparison with 'non home-based occupations' (which included all other occupations). Two of the studies (28, 35), which found this positive association between SEP and risk factor knowledge, also looked at income, and one of these (35) also found this association with professional status.
One study (5) had disaggregated their results by different risk factors, and found there to be better knowledge of one risk factor (arrhythmia) with higher SEP, but no difference with regards to SEP for the other five risk factors in the study (hypertension, diabetes, smoking, alcohol, coronary heart disease (CHD)).
Four studies (4,32,38,42) found there to be no difference in knowledge of stroke risk factors by SEP.
For all of these, the measure of SEP was education. Amongst these was one article (32) which found that there was no overall difference, however it found that people with a lower SEP were less likely to name physical inactivity as a risk factor.
Only one study (37) found that there was a higher knowledge of risk factors with a lower SEP; they found that less educated people more frequently recognised stroke risk factors. This was, however, only with regards to vascular risk factors.
Awareness of stroke warning signs by SEP  Table 4). All of these articles looked at education, except one (29) which only looked at professional status and found that, similarly as it did for risk factors, 'home-based occupations' were associated with a lower knowledge of stroke warning signs. Three of these studies (28,35,36) also found this positive association with regards to higher income, and one study (35), found this positive association with regards to professional status. One study (34), which looked at educational level in nine countries, found this positive trend across all countries, however the knowledge level was rather varied between countries. They found that the populations of Austria and Germany were the most knowledgeable, followed by the UK, whilst the populations of Spain and Italy were the least aware of stroke warning signs.
Three studies (38,41,42) found there to be no difference in awareness of warning signs by SEP. One study (37), as it had done for risk factors, found that there was a higher awareness of warning signs with a lower SEP.

Similarities and differences between knowledge of risk factors and warning signs by SEP amongst studies
Out of the 16 studies (4, 5, 28-33, 35, 37-43) that included both knowledge of risk factors and warning signs, 12 of them (28-31, 33, 35, 37-40, 42, 43) had similar associations with regards to knowledge of both these factors and SEP. For example, if they found higher SEP to mean better knowledge, they found this for both risk factors and for warning signs. One study (5), as mentioned earlier, found there to be increasing knowledge of warning signs with a higher SEP, but with regards to risk factors there was no difference in knowledge by SEP, except that people of a higher SEP correctly answered arrhythmia as a risk factor.
Two studies (4,32) found that there was no difference in knowledge of stroke risk factors and level of SEP but that there was a better awareness of stroke warning signs in higher SEP. One study (41), found the opposite, in that people with a higher SEP had more knowledge of stroke risk factors, but there was no difference in awareness of warning signs by SEP.
Most of the studies in Spain (27)(28)(29)34) and Italy (30,31,34) had similar outcomes in that, where risk factors and warning signs were looked at, increasing knowledge was always positively correlated with a higher SEP. The only exception was a Spanish study which found no difference by SEP with regards to risk factors, except for arrhythmia where it was positively correlated with a higher SEP (5).
The two studies undertaken in Croatia (32, 33) did not have the same correlations with regards to risk factors, but did for warning signs. The studies undertaken in Northern Ireland (4, 41) did not share similar correlations with regards to either risk factors or warning signs, however one of these studies (4) also included the Republic of Ireland and did not distinguish between the two countries with regards to stroke knowledge and its association with SEP. Another study (34) included the UK, amongst other countries, but did not break its results down to show Northern Ireland.
Details of the results of individual studies by SEP are displayed in Additional File 5.

Risk of bias in relation to study results
Although the critical appraisal tool AXIS (26) does not provide a numerical scale for assessing study quality, some studies were found to have answered positively to more questions than others (6,30,31,35). These studies all gave the results of better stroke knowledge with increasing SEP.
Four (29,33,36,43) of the five studies (29,33,36,41,43), which had the majority of negative or unclear responses using the AXIS tool, found there to be better stroke knowledge with increasing SEP.
However, one of these studies (41) found no difference in awareness of warning signs by SEP.
The other articles that gave results where higher SEP was not necessarily associated with increasing knowledge of stroke (5,32,37,38,42) had fewer positive responses in the AXIS tool, except for one (4) which had a higher number of positive responses.

Discussion
To the authors' knowledge this is the first systematic review to report on the association between knowledge of stroke risk factors and awareness of stroke warning signs with regards to SEP in the WHO European region. The results indicate that, in general, better stroke knowledge is associated with a higher SEP. Nearly two-thirds of the studies (6, 28-31, 33, 35, 39-41, 43) found that knowledge of stroke risk factors was positively associated with a higher SEP. Only one study (37) found there was a higher knowledge of risk factors with a lower SEP. This study, however, only looked at vascular risk factors. Vascular risk factors are more prevalent amongst people with a lower SEP (44)(45)(46), so they may visit their physician more regularly for check-ups. Healthcare professionals are the best source of information on stroke (47) so therefore it's possible that these patients with a lower SEP could be increasing their knowledge during these visits. Over three quarters of the studies (4, 5, 27-36, 39, 40, 43) found that better awareness of stroke warning signs was positively associated with a higher SEP.
Again, there was only one study that found a higher awareness with a lower SEP; it was the same one that found higher knowledge of risk factors in lower SEP (37).
The results of this systematic review indicate a social gradient with regards to stroke knowledge.
People with a lower SEP had lower levels of both stroke risk factor knowledge and warning sign awareness than those with higher SEPs. Identifying effective interventions to increase stroke knowledge and awareness amongst people with lower SEPs is likely to be a key aspect of any strategy to reduce the incidence of stroke in this group and improve stroke outcomes for them. A German study (6) found that sources of information of stroke risk factors varied according to an individual's socioeconomic profile. It is therefore important to target public health campaigns using platforms and media that people with lower SEPs interact with. Educational interventions have been shown to be effective at increasing stroke warning sign awareness across all educational groups (48). More research is needed, however, to identify the extent to which increased knowledge and awareness results in positive health behaviour change (2).
Reducing inequities in stroke knowledge and awareness amongst people with different SEPs is likely to be important in reducing health inequalities in stroke incidence and outcomes. Whilst this review indicates lower stroke knowledge and awareness amongst lower SEP groups, it is not clear from the review whether knowledge levels across people with higher SEPs was adequate. The studies in the review all used different definitions of good stroke knowledge and different measures to collect data.
In all eight studies (6,28,29,31,35,36,38,40) that asked open questions with regards to risk factor knowledge and gave a percentage of the number of people able to give at least one correct risk factor of stroke, over half of the participants in each study could name at least one. When using open questions, risk factor knowledge was better than knowledge of warning signs. However, it could be argued that it is less important to be able to actually recall warning signs; the importance is recognising a stroke when it is occurring (27,30). The results of warning sign awareness were much higher when individuals were given a list to choose from, i.e. when they were asked closed questions rather than open-ended questions. This is more reflective of real life in terms of recognising a stroke.
All of the five studies (30,33,34,37,42), which asked closed questions with regards to stroke warning signs and gave a percentage of the number of people able to correctly identify at least one warning sign from a list, found that over two-thirds of their participants could correctly identify at least one warning sign.
Whilst it is important to increase knowledge levels amongst those with a lower SEP, if knowledge is low overall then it should be increased for all SEP groups. Reviews of various public health domains (49) indicate that mass media campaigns can increase inequality amongst groups by SEP, particularly when directed at the whole population (50). An example of increasing health inequality through mass media campaigns has been seen amongst ethnic minority groups (19). The Act FAST public health campaign in the UK (10) aimed to increase awareness of the signs of stroke amongst the population.
However, for BMEs, this campaign had a limited effect (19). As ethnicity, like SEP, is a social determinant of health outcomes, this example can be used to underline the importance of carefully targeted campaigns. Whilst there are some ethical, economic and practical reasons that can be put forward for targeting people with the lowest SEP (51), the health inequalities literature and evidence suggests that the most effective way to reduce health inequalities is to tackle the social gradient using interventions applied proportionately according to need (52). As interventions effective in improving outcomes for one socioeconomic group may not be effective for another, tackling the social gradient in stroke knowledge and awareness is likely to require interventions carefully targeted to different SEP groups.
Carefully targeted social marketing, which uses tailored approaches, may be one effective method to improve stroke knowledge of risk factors and awareness of warning signs amongst people with lower SEPs and to narrow the gap between this group and those with higher SEPs, although effects may be small (53). Educational programmes brought into schools, in order to teach children from a young age, about stroke risk factors and warning signs, may also be of value, particularly in those schools with many children from families with a lower SEP. Events held across Europe for World Stroke Day (54) could be rolled out to areas where there is greater social deprivation and located in areas frequented by people with the poorest knowledge levels.
General Practitioners (GPs) and other primary healthcare professionals have key roles to play in educating patients on stroke awareness and prevention. In OECD countries, people with lower SEPs are less likely to access preventive healthcare from a GP than those with higher SEPs for the same level of need, but once they have seen a GP they have at least as many visits (55). This suggests that reducing inequities in access to GPs and other primary care professionals for preventative care, as well as using existing contacts to improve patients' stroke knowledge and to promote interventions to lower patients' stroke risk, are likely to be important to reduce the burden of stroke. Risk factor check-ups in workplaces and pharmacies may also be effective (2).
Currently, death rates from stroke vary widely across Europe with poorer stroke outcomes found amongst people in Eastern Europe (2). In addition to addressing inequalities in stroke risk factor knowledge and warning sign awareness, it is important to address inequalities between European countries. This is likely to require national and WHO regional strategies across Europe.
This systematic review makes an important contribution to the literature on stroke knowledge and awareness. A strength of this review includes the broad search strategy which was used and the comprehensive search of five databases as well as reference list searches of all included articles and of the two similar systematic reviews previously mentioned (16,17). It used a recognised critical appraisal tool for cross-sectional studies, AXIS (26), to assess the quality of the included studies. A limitation of this tool, however, was that it did not provide a numerical scale for assessing study quality. This meant that there was a degree of subjective assessment required. However, all four (6,30,31,35) of the studies which gave more positive responses to the tools' questions identified that an increasing knowledge of stroke was associated with increasing SEP.
The limitations of the study included that a meta-analysis was not possible. This was because the measures of SEP and of knowledge of stroke risk factors and warning signs were too diverse, and many studies did not publish data suitable to include in a meta-analysis. Age ranges of participants were also varied, as well as the use of open-ended or close-ended questions in studies. Only studies in the English language were included, however some studies in other languages may have been relevant, meaning there is potential for publication bias.
Following the study quality appraisal (Additional File 3), it was found that there was a risk of bias amongst some studies, including sampling and selection bias, and concerns about non-response bias.
Furthermore, there were several studies which had not had their instruments or measurements for risk factor and outcome variables previously trialled, piloted or published. Those studies, which are at a higher risk of bias, are of a lower quality.

Implications for future research
As mentioned earlier in the review, there have already been systematic reviews looking at stroke knowledge and its association with gender (16) and ethnic minorities (17). This review has studied stroke knowledge and its association with socioeconomic position. Another demographic factor which has not been systematically reviewed is age; this could therefore be an important area for future research. Elderly patients are at higher risk of a stroke (56) and may be more likely to witness someone close to them having a stroke, so it is important to understand if they are knowledgeable of the risk factors and warning signs of stroke, and if future interventions also need to be directed towards them.
Recognising the warning signs of stroke is important but so is the appropriate response to witnessing them. One study (5) found that extremes of education (i.e. people with no schooling and those with a university degree) would wait longer before acting in the event of a stroke. A review of intent to call an ambulance with regards to SEP would be beneficial. The search also revealed studies that looked at identification of the correct organ affected during a stroke (31,35,37). This could be looked at in another review, as well how people with different SEPs acquire their information. As a similar systematic review found that women had greater stroke awareness than men (16), it may be important to split interventions by gender and SEP; so that they are targeting specifically men with a lower SEP, in order to reduce inequalities. Systematic reviews to assess effectiveness of public health campaigns across Europe are needed (2), as well as a systematic review of interventions for increasing stroke awareness for people with lower SEPs, in order to know which interventions are effective.

Conclusions
The results of this systematic review suggest that individuals living in the WHO European region with a lower socioeconomic position are less knowledgeable of stroke risk factors and less aware of stroke warning signs than those with a higher SEP. As people with a lower SEP are at a higher risk of having a stroke, public health campaigns and educational interventions should be targeted towards them, but in ways that address the social gradient in stroke outcomes and do not further widen inequalities.
This would decrease the incidence of stroke and minimise time between stroke onset and treatment, so that loss of life and serious health issues can be minimised, as well as minimising the economic burden caused by stroke.
Approximately BME Black, minority and ethnic Availability of data and materials The datasets supporting the conclusions of this article are included within the article (and its additional files).
KS and WR devised the research question. KS conducted the database search. KS and WR completed the title and abstract screen and full text screen and discrepancies were discussed. KS and CB independently completed the data extraction and discrepancies were discussed. KS and WR completed the risk of bias assessment and discussed any discrepancies. KS drafted the manuscript.
All authors read and approved the final manuscript.