11
Country Comparisons of Human Stroke Research Since 2001 A Bibliometric Study Kjell Asplund, MD; Marie Eriksson, PhD; Olle Persson, PhD Background and Purpose—This is the first bibliometric comparison between countries of the development of stroke research over time. Methods—Clinical and epidemiological articles on stroke published 2001 to mid-2011 were identified in Science Citation Index Expanded. Article fractions, citation fractions, h-index, and international collaboration were calculated using the BibExcel software and adjusted for population size and gross domestic product. Results—The United States dominated with 28.7% of the sum of article fractions and 36.2% of the sum of citation fractions. The United States, Japan, the United Kingdom, and Germany together accounted for 52.1% of articles and 61.0% of citations. When adjusted for population size or gross domestic product, several small European countries, together with Israel and Taiwan, ranked the highest. Per population, there was a negative association (r0.60) between burden of stroke (disability-adjusted life-years lost) and number of articles per population. In China, South Korea, and Singapore, the annual growth of stroke articles was more than twice the worldwide average. Whereas multinational collaboration was common within Europe and North America, it was relatively uncommon between Asian countries. Conclusions—The Big 4 in scientific literature on stroke, as to both number of articles and citations, are the United States, Japan, the United Kingdom, and Germany. Many small European countries have, in relation to their size, a high scientific production. Several countries with rapidly expanding economies have very fast growth of scientific production on stroke. Our results emphasize the need for stroke research in countries with a high population burden of stroke and they highlight the role of multinational collaboration. (Stroke. 2012;43:830-837.) Key Words: bibliometrics h-index scientific production stroke B ibliometrics is increasingly used to evaluate research by quantity as well as quality. Examples of its use, at least as a supplementary instrument, are ranking of journals, ranking of candidates that apply for academic positions and awards, allocation of resources to research groups, and external reviews of the scientific excellence of institutions or universities. 1 It has been argued that the strength of biblio- metrics is its intrinsic validity in contrast to surrogates such as external grant funding. 2 At the macro level, it may also be used to evaluate scientific performance at a regional, national, or multinational level. Despite its wide application in other research domains, there is very limited literature 3,4 in which bibliometrics has been used for benchmarking of performance in stroke re- search or neurological research at large. A recent editorial in Stroke used bibliometrics to compare the impact of selected neuroscience journals. 5 An extensive validation of bibliomet- ric data on Swedish neurological research showed that a presumed decline in international competitiveness was not attributed to methodological bias. 6 In this benchmarking study, we provide information on countries’ proportions of all articles on human stroke re- search, their impact, and time trends during the years 2001 to 2011. The methodological approach for the present study is similar to that applied in an overview of public health research. 7 Crude data as well as data adjusted by population size and gross domestic product (GDP) are reported. The relation between number of stroke publications and popula- tion burden of stroke is analyzed. In view of the close linkage between clinical and epidemiological research, we have included both. Preclinical experimental research is not covered. Materials and Methods The Science Citation Index Expanded database was used to identify clinical and epidemiological articles on stroke. It includes 8300 major journals across 150 disciplines and was accessed through Web Received August 25, 2011; final revision received November 23, 2011; accepted December 1, 2011. From Riks-Stroke (K.A.), Medicine, Department of Public Health and Clinical Medicine, the Department of Statistics (M.E.) and Inforsk, the Department of Sociology (O.P.), Umeå University, Umeå, Sweden. The online-only Data Supplement is available with this article at http://stroke.ahajournals.org/lookup/suppl/doi:10.1161/STROKEAHA.111.637249/-/DC1. Correspondence to Kjell Asplund, MD, Riks-Stroke, Medicine, Department of Public Health and Clinical Medicine, Umeå University, 90185 Umeå, Sweden. E-mail [email protected] © 2012 American Heart Association, Inc. Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.111.637249 830 by guest on May 11, 2018 http://stroke.ahajournals.org/ Downloaded from by guest on May 11, 2018 http://stroke.ahajournals.org/ Downloaded from by guest on May 11, 2018 http://stroke.ahajournals.org/ Downloaded from by guest on May 11, 2018 http://stroke.ahajournals.org/ Downloaded from by guest on May 11, 2018 http://stroke.ahajournals.org/ Downloaded from

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Page 1: Country Comparisons of Human Stroke Research Since …stroke.ahajournals.org/content/strokeaha/43/3/830.full.pdfUsing BibExcel, we adopted it to estimate the impact of stroke publications

Country Comparisons of Human Stroke ResearchSince 2001

A Bibliometric Study

Kjell Asplund, MD; Marie Eriksson, PhD; Olle Persson, PhD

Background and Purpose—This is the first bibliometric comparison between countries of the development of strokeresearch over time.

Methods—Clinical and epidemiological articles on stroke published 2001 to mid-2011 were identified in Science CitationIndex Expanded. Article fractions, citation fractions, h-index, and international collaboration were calculated using theBibExcel software and adjusted for population size and gross domestic product.

Results—The United States dominated with 28.7% of the sum of article fractions and 36.2% of the sum of citationfractions. The United States, Japan, the United Kingdom, and Germany together accounted for 52.1% of articles and61.0% of citations. When adjusted for population size or gross domestic product, several small European countries,together with Israel and Taiwan, ranked the highest. Per population, there was a negative association (r�0.60) betweenburden of stroke (disability-adjusted life-years lost) and number of articles per population. In China, South Korea, andSingapore, the annual growth of stroke articles was more than twice the worldwide average. Whereas multinationalcollaboration was common within Europe and North America, it was relatively uncommon between Asian countries.

Conclusions—The Big 4 in scientific literature on stroke, as to both number of articles and citations, are the United States,Japan, the United Kingdom, and Germany. Many small European countries have, in relation to their size, a highscientific production. Several countries with rapidly expanding economies have very fast growth of scientific productionon stroke. Our results emphasize the need for stroke research in countries with a high population burden of stroke andthey highlight the role of multinational collaboration. (Stroke. 2012;43:830-837.)

Key Words: bibliometrics � h-index � scientific production � stroke

Bibliometrics is increasingly used to evaluate research byquantity as well as quality. Examples of its use, at least

as a supplementary instrument, are ranking of journals,ranking of candidates that apply for academic positions andawards, allocation of resources to research groups, andexternal reviews of the scientific excellence of institutions oruniversities.1 It has been argued that the strength of biblio-metrics is its intrinsic validity in contrast to surrogates such asexternal grant funding.2 At the macro level, it may also beused to evaluate scientific performance at a regional, national,or multinational level.

Despite its wide application in other research domains,there is very limited literature3,4 in which bibliometrics hasbeen used for benchmarking of performance in stroke re-search or neurological research at large. A recent editorial inStroke used bibliometrics to compare the impact of selectedneuroscience journals.5 An extensive validation of bibliomet-ric data on Swedish neurological research showed that a

presumed decline in international competitiveness was notattributed to methodological bias.6

In this benchmarking study, we provide information oncountries’ proportions of all articles on human stroke re-search, their impact, and time trends during the years 2001 to2011. The methodological approach for the present study issimilar to that applied in an overview of public healthresearch.7 Crude data as well as data adjusted by populationsize and gross domestic product (GDP) are reported. Therelation between number of stroke publications and popula-tion burden of stroke is analyzed. In view of the close linkagebetween clinical and epidemiological research, we haveincluded both. Preclinical experimental research is notcovered.

Materials and MethodsThe Science Citation Index Expanded database was used to identifyclinical and epidemiological articles on stroke. It includes �8300major journals across 150 disciplines and was accessed through Web

Received August 25, 2011; final revision received November 23, 2011; accepted December 1, 2011.From Riks-Stroke (K.A.), Medicine, Department of Public Health and Clinical Medicine, the Department of Statistics (M.E.) and Inforsk, the

Department of Sociology (O.P.), Umeå University, Umeå, Sweden.The online-only Data Supplement is available with this article at http://stroke.ahajournals.org/lookup/suppl/doi:10.1161/STROKEAHA.111.637249/-/DC1.Correspondence to Kjell Asplund, MD, Riks-Stroke, Medicine, Department of Public Health and Clinical Medicine, Umeå University, 90185 Umeå,

Sweden. E-mail [email protected]© 2012 American Heart Association, Inc.

Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.111.637249

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of Science. The study covered a period from January 2001 to August2011. For time trend analyses, we included only full years (2001–2010). Citation analyses were based on articles during the years 2001to 2010 and cited up to August 2011.

Inclusion criteria were (1) clinical and epidemiological articles onstroke, including all subtypes listed in MESH; (2) original articlesand reviews; (3) articles published in English; and (4) time periodfrom January 2001 to August 2011. In time trend analyses, weincluded only countries with �100 articles published during 2001 to2010. Exclusion criteria were (1) nonhuman studies; and (2) articlesother than original studies and reviews; thus, conference proceed-ings, editorials, letters, and book chapters were excluded. Althoughthe main analysis concerned only English language article, articles inother languages were also recorded in a supplementary analysis.

The search strategy is presented in Supplemental Table I(http://stroke.ahajournals.org). In addition to “stroke,” we usedsynonyms to stroke (“cerebrovascular disease[s]” and “apo-plexy”) and all stroke subtypes listed in MESH as search terms.Because the term “stroke” is also included in the cardiology term“stroke volume,” we excluded articles with the latter term. Arandom sample of 455 articles (1% of all articles) was reviewedto validate the search.

The software BibExcel8 was used to analyze the downloadedrecords from the search: editing country addresses, calculation ofarticle fractions, citation fractions, and country coauthorships. Theanalyses are based on sums of article fraction and sums of citationfractions. When an article has authorship from �1 country, eachcountry is assigned a fraction of this article and its citationsdepending on the number of addresses, for example, for an articlewith 2 addresses from 1 country and 1 address from another country,the first country is assigned two thirds of an article when quantity isanalyzed and two thirds of its citations.

As a supplementary analysis, the impact of publications was alsomeasured by the h-index.9 This index is constructed so that itdiscounts the disproportionate weight of highly cited articles orarticles that have not yet been cited. Using BibExcel, we adopted itto estimate the impact of stroke publications at the country level.

The number of articles and citations are reported as percentages ofall articles and citations, both as crude proportions and proportionsadjusted by number of inhabitants and gross national product. Dataon population sizes were derived from UN statistics10 and data ongross national product from The World Bank11 supplemented by dataon Taiwan from the International Monetary Fund database.12 Euro-pean Union countries were combined both as member states in 2001(EU-15) and in 2011 (EU-27). For analyses of number of articles inrelation to population burden of stroke, we used World HealthOrganization country data on disability-adjusted life-years lost bycerebrovascular disease.13

Statistical MethodsPoisson regression was used to model the sum of article fractions.Year was included as a continuous covariate assuming a log-linearrelationship. Separate models were fitted for each country and theregression coefficient�100 was used to estimate the annual relativechange (%). To compare time trends, an additional model includedall countries and the independent variables country, year, andcountry-by-year interaction. Estimates are presented with 95% CIsand the level of significance was 0.05. Approximate 95% CIs forranks were calculated by using a Monte Carlo simulation procedure,similar to that described by Marshall et al,14 based on 10 000iterations. Here, the sums of article and citation fractions for eachcountry were assumed to follow a Poisson distribution. R Version2.14 was used for the simulation. For other statistical analyses, SAS9.2 was used.

ResultsValidationsThe literature search yielded a total of 44 877 clinical andepidemiological articles on stroke published in the English

language from January 2001 to August 2011. In a validationof 445 randomly selected articles (1% of all articles), weidentified 41 articles that did not fulfill the inclusion criteria(13 on neurological conditions other than stroke, 23 on otherdiseases, and 5 nonhuman studies; overall positive predictivevalue 90.8%). The distribution of countries among articlesthat did not fulfill the inclusion criteria (United States 32%;United Kingdom, Japan, and Germany together 24%; othercountries 44%) was similar to that of the entire set of articles(see subsequently). Terms that were added late in the searchprocess, for example, more subclassifications of stroke,resulted in very few additional articles, not identified atprevious steps of the search, indicating high sensitivity.

Articles identified by our search strategy did not alwayshave stroke as a major focus but as 1 of many disorders(including, for instance, stroke as 1 of several manifestationsof cardiovascular disease). If the condition that the term“stroke” should be present in the title, abstract, or authors’key words was added to possibly retrieve more stroke-specific articles, it had very little impact on the ranking ofcountries (data not shown).

When our SCI search was extended to articles published inany language, the great majority of articles retrieved were inEnglish (93.2%). Other relatively frequent languages wereGerman (1.9%), Spanish (1.7%), French (1.1%), and Russian(0.9%). No other language accounted for �0.4%.

Excluding review articles had little impact on the rankingof countries, whether article fractions or citations fractionswere compared, even if citation fractions were, in general,somewhat lower (data not shown).

Country Proportions of All Articles and CitationsFigure 1 shows the top 30 countries by quantity of articles,expressed as sums of article fractions. The United States hada very marked dominance (28.7% of the sum of articlefractions). Next in ranking by quantity were the UnitedKingdom, Japan, and Germany (7%–8%).

The sums of citation fractions for articles published duringthe years 2001 to 2010 are shown in Figure 2 (left panel).Here, the US dominance is even more evident (36.2%).Belgium, Denmark, France, Sweden, and the United King-dom also had a bigger proportion of citations than proportionof articles. For all other countries, the proportion of citationswas equal to or lower than the proportion of articles.

When the h-index was used to further assess the impact ofstroke publications (Figure 2, right panel), most countriesranked about the same as when citation fractions were used.A general pattern was, however, that the Scandinaviancountries (Denmark, Finland, Norway, and Sweden) rankedsomewhat higher when h-index was used, whereas East Asiancountries (China, Japan, South Korea, and Taiwan) rankedlower.

Country Proportions Adjusted for Population Sizeand GDPWhen sums of article fractions were adjusted for populationsize, several small European countries, together with Israel,ranked the highest (Table 1). Among the 4 countries with thelargest production in absolute numbers, the United Kingdom

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ranked considerably higher per million inhabitants than theUnited States, Germany, and Japan. When the EuropeanUnion countries were analyzed together, the article fractionadjusted for population size was somewhat lower than the USfraction but higher than the Japanese fraction (Table 1).

There was a very close relationship between GDP andnumber of publications on stroke (r�0.98 for the top 30countries as to sum of article fractions). When the countrieswere ranked by sum of article fractions adjusted for GDP,Israel had the largest production of scientific articles during2001 to 2011 followed by Taiwan and the same smallEuropean counties that ranked high in the population-adjusted comparisons. Again, the United Kingdom rankedhighest among the 4 countries with most published articles.Countries with big economies such as the United States,China, and Japan, although having a high proportion of articlefractions (Figure 1), tended to rank relatively low afteradjustment for GDP. The European Union countries togetherhad a higher GDP-adjusted article fraction than the UnitedStates and Japan (Table 1).

In citation analyses, Sweden ranked the highest, whetheradjusted by population or economy size (Table 1). Severalother small European countries, plus the United Kingdom,also ranked high. It may be noted that Asian countries with ahigh production of articles (China, Japan, and South Korea)ranked relatively low in citations after adjustment for popu-

lation size or GDP. The citation fraction for articles from theEuropean Union countries combined was similar to that in theUnited States whether adjusted for population size or GDP(Table 1).

Relation to Country Burden of StrokeAmong the 29 countries with the largest number of strokepublications during the years 2001 to 2010 (comparativeWorld Health Organization data on disability-adjusted life-years are not available for Taiwan), there was a strongnegative correlation between the population burden of stroke(measured as age-standardized disability-adjusted life-yearsattributed to cerebrovascular disease per population) and thenumber of publications per population (r�0.60; P�0.001).Several countries with a high burden of stroke had a relativelylow number of stroke articles per population (eg, China,India, Turkey), whereas some countries with a relatively lowburden of stroke had a high number of publications perpopulation (eg, Canada, Israel, and Switzerland).

Time TrendsIn all countries with a quantity of articles that permittedreliable analyses (�100 articles during study period), therewas an increase in the sum of article fractions over the 2001to 2010 period. The overall annual increase was 10.4%(95% CI, 10.1%–10.8%). As emerges from Table 2, leftcolumns, the increasing pattern was similar in most coun-

Figure 1. Country comparisons of sums of articlefractions of clinical and epidemiological studies onstroke published during the Years 2001 to 2011.

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tries, being in the range of 9% to 14% annual increase.However, in 3 countries, China, South Korea, and Singa-pore, the annual rate of increase was more than twice theinternational average. In Israel, Japan, and the UnitedKingdom, the rate of increase was significantly slowerthan the worldwide average (Table 2).

When the article quantity ranking of countries in thebeginning of the study period (2001–2002) was comparedwith that at the end of the period (2010–2011), the top 5countries were identical at the 2 time points. Eight countrieshad advanced �5 positions, 5 of them in Asia (China, India,Iran, South Korea, and Taiwan), 2 in Europe (Greece andPoland), and 1 in South America (Brazil). Three countrieslost �5 positions (Finland, Israel, and Sweden). Due to thelarge number of article fractions, 95% CIs of the rankingswere narrow.

Because recently published articles have fewer citationsthan articles published earlier (articles published in 2002 hadthe highest total number of citations), annual trends incitations by country are not reported here. To illustratechange over time, we instead provide citation ranking data atthe beginning and the end of the study period (Table 2, rightcolumns). Three countries improved their citation fractionranking from 2001 to 2002 to 2009 to 2010 by 5 positions ormore: China, India, and South Korea. Among the top 10countries in 2001 to 2022, Belgium, Japan, and Sweden eachlost �3 ranking positions. Among countries further down the

list, Austria, Finland, Hungary, Norway, Singapore. andTurkey lost �5 positions. It should be noted, however, thatBelgium and Singapore each had 1 very frequently citedarticle in 2001, making their positions at the beginning of thestudy period spuriously high. As for article fractions, the 95%CIs of the rankings were narrow.

Multinational CollaborationIn Figure 3, multinational collaboration, as reflected byarticles with authorship from �1 country, has been mapped.,showing links with at least 50 coauthored articles. The patternwas essentially the same as for sums of article and citationfractions with the United States as the leading country.However, there were a few countries with few strong multi-national authorships in view of their overall production ofstroke articles: China, Japan, and South Korea. Whereas therewas frequent coauthorship between west European countries,there were no strong coauthorships between Asian countries.

DiscussionWorldwide, there has been a �10% annual increase inclinical and epidemiological stroke publications during thelast century. We have documented the US dominance inclinical and epidemiological stroke research and the rapidlyincreasing contribution of Chinese and South Korean re-search to the scientific literature on stroke. When adjusted forpopulation size and GDP, many small European countries

Figure 2. Country comparisons of sums of citation fractions (left) and h-index (an alternative measure of impact, see “Methods”) of arti-cles published 2001 to 2010 (right).

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rank remarkably high in stroke research production, but, overthe years, many of them seem to have lost some of theircompetitiveness.

The addition of relevant new articles was minimal when,by the end of the search procedure, new search terms wereadded. This indicates a high sensitivity of our search strategy.Validation of randomly selected articles indicated a reason-ably good specificity. Articles resulting from the searchstrategy that were found not to be relevant were similarlydistributed between countries as relevant articles. It is highlyunlikely that any bias caused by the limited proportion of

irrelevant articles was systematic enough to significantlyaffect the comparisons between countries.

The fact that our search was not restricted to stroke orneurological journals may be seen both as a strength and aweakness. The search strategy resulted in a broad spectrum ofarticles, that not all had stroke as a major focus. For instance,reports on stroke as 1 of several outcomes or stroke as anadverse effect of therapy were included. Thus, we studiedcountries’ contribution to the collected worldwide knowledgeon stroke rather than success or failure of a country’s policyto promote specific stroke research.

Table 1. Proportion of Stroke Article Fractions and Citation Fractions January 2001 to August 2011 by Country of Origin

Rank

Article Fractions Citation Fractions

Per 10 MillionInhabitants

Per BillionUS $ GDP

Per 10 MillionInhabitants

Per BillionUS $ GDP

Country Index* Country Index* Country Index* Country Index*

1 Sweden 2.11 Israel 5.44 Sweden 2.66 Sweden 5.48

2 Netherlands 2.11 Taiwan 4.52 Netherlands 2.17 UK 5.08

3 Switzerland 1.94 Netherlands 4.46 Iceland 1.99 Iceland 4.76

4 Israel 1.84 Sweden 4.35 Switzerland 1.96 Netherlands 4.60

5 Finland 1.82 Finland 4.07 Finland 1.89 Denmark 4.38

6 Denmark 1.81 UK 3.69 UK 1.88 Finland 4.23

7 Norway 1.42 Denmark 3.19 Luxemburg 1.66 Israel 3.59

8 UK 1.36 Hungary 3.05 Canada 1.65 Canada 3.49

9 Iceland 1.26 Iceland 3.03 Norway 1.53 Belgium 2.87

10 Canada 1.24 New Zealand 3.00 Belgium 1.29 New Zealand 2.84

11 Australia 1.20 Croatia 3.00 Australia 1.24 Switzerland 2.83

12 Austria 1.19 South Korea 2.95 Israel 1.21 Australia 2.75

13 Belgium 0.98 Switzerland 2.80 USA 1.17 USA 2.48

14 Singapore 0.96 Greece 2.69 Austria 1.11 Austria 2.42

15 USA 0.93 Australia 2.66 Germany 0.96 Germany 2.39

16 New Zealand 0.92 Canada 2.63 New Zealand 0.87 Italy 2.10

17 Germany 0.86 Turkey 2.61 Italy 0.69 Hungary 1.99

18 Taiwan 0.85 Austria 2.60 Ireland 0.68 Taiwan 1.90

19 Italy 0.85 Slovenia 2.57 France 0.60 Norway 1.76

20 Greece 0.73 Italy 2.56 Singapore 0.55 Luxemburg 1.66

21 Ireland 0.68 Belgium 2.18 Spain 0.47 France 1.48

22 Japan 0.63 Germany 2.15 Greece 0.39 Estonia 1.45

23 Slovenia 0.61 Estonia 2.09 Japan 0.36 Greece 1.44

24 South Korea 0.61 Poland 1.99 Taiwan 0.36 Ireland 1.30

25 Spain 0.50 USA 1.97 Slovenia 0.30 Spain 1.35

26 France 0.45 Singapore 1.95 Hungary 0.26 Slovenia 1.22

27 Croatia 0.41 Norway 1.63 Denmark 0.26 South Korea 1.15

28 Hungary 0.40 Japan 1.45 South Korea 0.24 Singapore 1.12

29 Luxemburg 0.26 Spain 1.45 Portugal 0.15 Poland 0.92

30 Turkey 0.25 Ireland 1.36 Czech Republic 0.13 Japan 0.84

… EU-15† 0.88 EU-15 2.29 EU-15 1.11 EU-15 2.90

… EU-27‡ 0.69 EU-27 2.33 EU-27 0.87 EU-27 2.93

GDP indicates gross domestic production.*Sum of article fractions and sum of citation fractions divided by population size and GDP, respectively.†European Union member states in Year 2001.‡European Union member states in Year 2011.

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SCI Expanded covers all important medical journals pub-lished in English, but its coverage of non-English literature islimited.15 This may explain why a big country like Russia(with stroke research predominantly published in Russianlanguage journals) does not appear, in any aspect, among thetop 30 producers of stroke research. Correspondingly, re-search published in Spanish, Chinese, and Japanese may beunderrepresented in our analyses of research production.Because non-English articles are infrequently cited in theinternational literature, comparisons of citations are lessprone to be affected by selective language coverage in SCI.

The use of impact factors to evaluate quality of healthcareresearch has often been criticized, perhaps most eloquently by

Seglen as early as 1997.16 Concerns have also been expressedby organizations such as the European Association of ScienceEditors.17 The sum of citation fractions and the h-index, as wehave used, are a more direct measures of the impact strokearticles have had than journal impact factors. The need foradjustment for speciality has also been emphasized.17,18

Because our study was restricted to a relatively uniformresearch area, there was no obvious need for adjustment byspeciality.

The dominance of the United States in both quantitativeand qualitative analyses was impressive, but much less sowhen population size and GDP were taken into account. Itshould be noted that, due to the size of the US economy

Table 2. Time Trends 2001–2010 of Article Fractions and Ranking (95% CIs) Between Countries and Change of Ranking of CitationFractions From 2001–2002 to 2009–2010*

Annual Increase in Sum of Article FractionsSum of Article Fractions, Ranking

(95% CIs)Sum of Citation Fractions, Ranking

(95% CIs)

Country§ Percent Country§ 2001–2002 2009–2010 Country� 2001–2002 2009–2010

PR China 27.2 (25.1–29.4)† USA 1 (1–1) 1 (1–1) USA 1 (1–1) 1 (1–1)

South Korea 24.0 (21.9–26.1)† Japan 2 (2–3) 2 (2–3) UK 2 (2–2) 2 (2–2)

Singapore 22.4 (17.7–27.1)† UK 3 (2–3) 3 (2–4) Germany 3 (3–3) 3 (3–3)

India 19.8 (16.0–23.5)† Germany 4 (4–4) 4 (3–4) Canada 4 (4–4) 4 (4–4)

Poland 19.0 (15.6–22.4)† Italy 5 (5–5) 5 (5–5) Japan 5 (5–5) 8 (8–8)

Taiwan 17.1 (14.6–19.6)† Canada 6 (6–6) 7 (6–8) France 6 (6–6) 5 (5–6)

Brazil 16.8 (13.5–20.0)† Netherlands 7 (7–8) 9 (8–9) Italy 7 (7–7) 7 (6–7)

Greece 16.1 (12.7–19.7)† France 8 (7–8) 10 (10–11) Netherlands 8 (8–8) 6 (5–7)

Australia 14.2 (12.3–16.1)† Sweden 9 (9–11) 15 (13–16) Sweden 9 (9–9) 11 (10–11)

Denmark 14.0 (11.2–16.7)† Australia 10 (9–12) 11 (10–11) Belgium 10 (10–10) 17 (17–20)

Canada 13.0 (11.5–14.4)† Spain 11 (9–14) 13 (12–15) Australia 11 (11–11) 10 (9–11)

Norway 13.8 (10.4–17.2) South Korea 12 (10–16) 8 (7–9) Spain 12 (12–13) 13 (12–13)

Netherlands 13.6 (12.0–15.3)† Turkey 13 (11–17) 14 (12–15) Switzerland 13 (12–13) 14 (14–15)

Spain 13.6 (11.4–15.7)† Israel 14 (11–17) 23 (21–26) Denmark 14 (14–14) 15 (14–15)

Turkey 13.5 (11.0–15.9)† PR China 15 (12–19) 6 (6–7) Finland 15 (15–15) 20 (17–20)

Switzerland 12.9 (10.6–15.3) Taiwan 16 (12–20) 12 (11–13) Austria 16 (16–16) 21 (21–23)

Italy 12.7 (11.3–14.1)† Switzerland 17 (14–21) 16 (15–17) Norway 17 (17–17) 25 (22–26)

France 12.4 (10.6–14.1) Finland 18 (15–21) 24 (21–26) South Korea 18 (18–19) 12 (12–13)

Ireland 12.2 (7.2–17.1) Denmark 19 (15–21) 20 (18–23) Israel 19 (18–20) 19 (17–20)

Belgium 10.9 (8.2–13.7) Austria 20 (16–22) 25 (23–27) PR China 20 (19–20) 9 (9–10)

Hungary 10.8 (6.3–15.4) Belgium 21 (17–22) 21 (18–23) Taiwan 21 (21–21) 16 (16–16)

USA 10.7 (10.1–11.3) Norway 22 (21–26) 26 (23–27) Turkey 22 (22–22) 26 (23–26)

Germany 10.2 (9.0–11.3) Poland 23 (21–26) 17 (17–20) Poland 23 (23–24) 18 (17–20)

New Zealand 9.8 (5.5–14.0) Brazil 24 (21–27) 19 (17–21) Singapore 24 (23–24) 30 (28–30)

Sweden 9.4 (7.4–11.4) India 25 (22–28) 18 (17–20) Greece 25 (25–27) 22 (21–24)

UK 8.4 (7.5–9.4)‡ New Zealand 26 (24–30) 30 (29–34) New Zealand 26 (25–27) 27 (27–29)

Finland 7.7 (4.9–10.6) Greece 27 (24–30) 22 (20–25) Brazil 27 (26–27) 23 (21–26)

Austria 7.5 (4.6–10.4) Hungary 28 (24–30) 29 (28–32) Argentina 28 (28–28) 28 (27–30)

Japan 6.9 (5.8–8.1)‡ Singapore 29 (25–31) 27 (25–29) India 30 (30–32) 24 (22–26)

Israel 4.4 (1.6–7.2)‡ Iran ¶ 28 (26–30) Ireland 33 (33–) 29 (27–30)

*Only countries with at least 100 published articles 2001–2010.†Ninety-five percent CI significantly above the worldwide rate of annual increase (10.1%–10.8%).‡Ninety-five percent CI significantly below the worldwide rate of annual increase.§Only countries with a top 30 position in sum of article fractions 2009–2010.�Only countries with a top 30 position in sum of citation fractions in 2009–2010.¶No publications in 2001–2002.

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(nearly 3 times bigger than that of any other country), the USranking came out as quite low when adjusted for GDP. Theshare of US articles of total number of stroke articles inthe world (sum of article fractions 29%) is approximately thesame or somewhat smaller than reported from other clinicaldisciplines, for example, infectious diseases, cardiopulmo-nary diseases, and public health epidemiology.7,19,20 To-gether, the big 4 (United States, Japan, United Kingdom, andGermany) produce the majority of the world’s stroke litera-ture: 52% of the sum of article fractions and 61% of the sumof citation fractions.

Many small countries in western Europe (most notably theScandinavian countries), together with Israel, rank high in thepopulation and GDP-adjusted comparisons. However, severalof them, for instance all Nordic countries such as Denmark,Finland, Norway, and Sweden, together with Israel, have lostrank positions during the last decade. This may represent aregression-to-the-mean phenomenon in a very competitiveinternational setting, but it may also be an expression ofemerging problems in research organization, innovation cul-ture, and funding in these countries. Exceptions to the trend insmall, previously successful countries to lose positions areThe Netherlands and Switzerland, both keeping their highrankings.

The much cited Clinical Research Roundtable at theInstitute of Medicine has characterized US clinical researchas “increasingly encumbered by high costs, slow results, lackof funding, regulatory burdens, fragmented infrastructure,incompatible databases, and a shortage of qualified investi-gators and willing participants.”21 It is beyond the scope ofthis article to analyze to what extent some countries may havebeen more successful than others to overcome these obsta-cles. However, we note that, first, the United States has,despite these challenges, kept its dominating position instroke research and, second, that common to many of thesuccessful small countries are strong multinational researchnetworks. It is notable that multinational collaboration ismuch less common outside North America and Europe.

There was a very strong negative correlation between thepopulation burden of stroke and stroke research production.

The links are complex with socioeconomic factors seeminglyplaying a major role. Our results highlight the obvious needfor high-quality stroke research in countries with a highburden of the disease.

It seems that countries with rapidly expanding economiesstrengthen their positions. China and South Korea haveemerged as leading countries in stroke research, more so inquantitative terms than in impact. Common to them is verystrong economic growth. Brazil, India, and Taiwan are alsoexamples of countries with an expanding economy that rankconsiderably higher in stroke research now than a decade ago.The rate of increase in number of articles has been less thanthe international average in Japan despite a well-recognizedstroke research history, perhaps related to economic growthbelow the international average during the last decade.

To conclude, we have provided benchmarking data on thequantity of scientific publications and on impact in terms ofcitation rates and h-index in different countries during the lastdecade. We have also mapped multinational collaboration.Irrespective of bibliometric measure, there is a strikingassociation between economic strength (and growth) andvolume and impact of stroke research. Considering theirpopulation size and GDP, several small European countriesrank high both as to publication volume and citation rates.During the decade, there has been a very conspicuousincrease in the Asian contribution to the scientific literatureon stroke.

Source of FundingThis study was supported by Vinnvård, a joint initiative by Vinnova,the Vårdal Foundation, and the Swedish Ministry of Health.

DisclosuresNone.

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Figure 3. Map of international collabora-tion in clinical and epidemiological strokeresearch between countries. The size ofthe symbols represents the number ofcollaborations. Only collaborations with�50 coauthored papers are included inthe analysis.

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Kjell Asplund, Marie Eriksson and Olle PerssonCountry Comparisons of Human Stroke Research Since 2001: A Bibliometric Study

Print ISSN: 0039-2499. Online ISSN: 1524-4628 Copyright © 2012 American Heart Association, Inc. All rights reserved.

is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231Stroke doi: 10.1161/STROKEAHA.111.637249

2012;43:830-837; originally published online January 26, 2012;Stroke. 

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Supplementary table S1. Search strategy in SCI Expanded for the update period January 2001 to August 2011. The search was done on the 6th of August 2011. Set no Records Search # 6 44,877 #5 NOT TS=(animal* OR "stroke volume") AND Language=(English) AND Document Type=(Article OR Review) # 5 48,770 #4 AND TS=(patient* OR human*) AND Language=(English) AND Document Type=(Article OR Review) # 4 77,514 #3 OR #2 OR #1 AND Language=(English) AND Document Type=(Article OR Review) # 3 6,881 TS=("intracranial arteriosclerosis" OR "intracranial embolism" OR "intracranial thrombosis" OR "subarachnoid hemorrhage*" OR "vertebral artery dissection" OR "venous sinus thrombosis") AND Language=(English) AND Document Type=(Article OR Review) # 2 10,781 TS=("carotid thrombosis" OR "carotid stenosis" OR "cerebral hemorrhag*" OR "intracerebralhemorrhag*" OR "cerebral infarct*") AND Language=(English) AND Document Type=(Article OR Review) # 1 68,817 TS=(stroke OR "cerebrovascular dis*" OR apoplexy OR "brain infarct*" OR "brain ischemi*") AND Language=(English) AND Document Type=(Article OR Review)

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39

Abstract 9

Country Comparisons of Human Stroke Research Since 2001A Bibliometric Study

Kjell Asplund, MD; Marie Eriksson, PhD; Olle Persson, PhD

(Stroke. 2012;43:830-837.)

Key Words: bibliometrics h-index scientific production stroke