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A snapshot of pneumonia research activity and collaboration patterns (2001–2015): a global bibliometric analysis

  • José M. Ramos-RincónEmail author
  • Héctor Pinargote-Celorio
  • Isabel Belinchón-Romero
  • Gregorio González-Alcaide
Open Access
Research article
Part of the following topical collections:
  1. Data collection, quality, and reporting

Abstract

Background

This article describes a bibliometric review of the scientific production, geographical distribution, collaboration, impact, and subject area focus of pneumonia research indexed on the Web of Science over a 15-year period.

Methods

We searched the Web of Science database using the Medical Subject Heading (MeSH) of “Pneumonia” from January 1, 2001 to December 31, 2015. The only document types we studied were original articles and reviews, analyzing descriptive indicators by five-year periods and the scientific production by country, adjusting for population, economic, and research-related parameters.

Results

A total of 22,694 references were retrieved. The number of publications increased steadily over time, from 981 publications in 2001 to 1977 in 2015 (R2 = 0.956). The most productive country was the USA (38.49%), followed by the UK (7.18%) and Japan (5.46%). Research production from China increased by more than 1000%. By geographical area, North America (42.08%) and Europe (40.79%) were most dominant. Scientific production in low- and middle-income countries more than tripled, although their overall contribution to the field remained limited (< 15%).

Overall, 18.8% of papers were the result of an international collaboration, although this proportion was much higher in sub-Saharan Africa (46.08%) and South Asia (23.43%). According to the specific MeSH terms used, articles focused mainly on “Pneumonia, Bacterial” (19.99%), followed by “Pneumonia, Pneumococcal” (7.02%) and “Pneumonia, Ventilator-Associated” (6.79%).

Conclusions

Pneumonia research increased steadily over the 15-year study period, with Europe and North America leading scientific production. About a fifth of all papers reflected international collaborations, and these were most evident in papers from sub-Saharan Africa and South Asia.

Keywords

Pneumonia Bibliometrics Scientometrics Scientific production Mapping Publications 

Background

Pneumonia is an important infectious disease worldwide and is associated with high morbidity, mortality and health system expenditure [1, 2]. In 2015, data from the Global Burden of Disease study showed that lower respiratory tract infections, including pneumonia, were the third most common cause of death, exceeded only by ischemic heart disease and cerebrovascular disease [3]. Community-acquired pneumonia (CAP) remains the primary cause of death from infectious disease globally, and its high impact on morbidity and mortality is especially concentrated in children under five and the elderly [1, 4, 5, 6]. The World Health Organization (WHO) predicted that deaths from lower respiratory tract infections would remain among the top four causes of deaths up to at least 2030 [7]. Antibiotic-resistant strains have also been on the rise, although resistance does not appear to be related to mortality. However, pneumonia is associated with high rates of hospitalization and length of hospital stay. Moreover, it has considerable long-term effects on quality of life, and long-term prognosis is worse in patients with pneumococcal pneumonia [1].

Despite the public health importance of the disease, few studies have evaluated research in the area using bibliometric methods. Indeed, only Head et al. (2015) have analyzed publications on pneumonia, and their work was limited in geographical scope to the UK [8, 9]. In this study, by analyzing scientific papers on pneumonia published in the main international scientific journals, we aimed to identify the scientific contribution of different countries to the worldwide research effort, the most cited landmark articles, the degree and nature of scientific collaboration, and the topics addressed.

This bibliometric description can provide relevant information for researchers in the field, particularly new scientists, giving a snapshot of strong research areas in pneumonia and global health as well as possible gaps requiring additional investments [10, 11, 12]. The paper also provides clues for addressing the weaknesses observed, such as the need to promote North-South collaborations and other research initiatives with countries that have relatively little scientific development on the topic [9, 13].

The aim of the present study is to assess the scientific literature on pneumonia that is indexed in the Web of Science (WoS). Specifically, we will analyze: (1) the evolution of scientific production; (2) its distribution by countries and regions; (3) the impact of the research papers; and (4) the degree of international collaboration. Finally, we will present details on the subject area focus of different publications according to the Medical Subject Headings (MeSH).

Methods

Identifying the population of study documents

For the performance of the study, we opted to identify documents about pneumonia by means of the MeSH thesaurus in the MEDLINE database because this is a detailed instrument for controlled terminology. The thesaurus employs both a human team of specialist indexers to analyze each article and assign medical subject headings to it, plus automated processes to improve indexing; the result is a highly consistent system of classification for research topics [14, 15, 16]. The pneumonia descriptor was introduced in 1963 as a disease of the respiratory tract and the lung, and it was defined as “infection of the lung often accompanied by inflammation” [17]. Synonyms of this descriptor (and therefore also included in search results) are “Lung Inflammation” and “Pulmonary Inflammation”. Additional file 1: Table S1 shows the MeSH tree structure for “Pneumonia”.

The next step was to identify the documents assigned with the MEDLINE descriptor of “pneumonia” indexed in the WoS. This body of research constitutes the population of documents for the present study. Conceived by Eugene Garfield but now maintained by Clarivate Analytics, WoS is the top scientific citation search and analytical information platform worldwide, serving both as a multidisciplinary research tool supporting a variety of scientific tasks and as a dataset for large, data-intensive studies [18].

The use of the WoS databases enables the analysis of all institutional affiliations reported in the documents and the calculation of citation indicators. The WoS brings together the most visible literature at a global level. These qualities justify its choice as the database platform used in this study despite some limitations related to covering non-English biomedical journals [18].

Although initially no limitations were imposed on our search, to calculate the bibliometric indicators we considered only two types of documents, articles and reviews, as these are the primary references for researchers. The study period was limited to 2001–2015, as delays associated with assigning MeSH descriptors to documents mean that information on the most recent articles on pneumonia is not updated. The searches took place on the Clarivate Analytics WoS platform, which includes MEDLINE database, on March 20, 2018.

Analyzing bibliographic characteristics and standardizing data

For each of the retrieved documents, data on the following bibliographic characteristics were extracted: year of publication, journal of publication and WoS subject category, document type, authorship, citations, institutional affiliation(s), and MeSH descriptors.

Data were then standardized: institutional affiliations corresponding to England, Northern Ireland, Scotland and Wales were grouped together under “United Kingdom,” while affiliations in Overseas France, British Overseas Territories, and island dependencies were also assigned to their ruling countries (for example, the documents signed by authors from French Polynesia, Guadeloupe, Martinique, New Caledonia, and Reunion were assigned to France), although regional designations correspond to geographical rather than political criteria. Scientific production from Taiwan, which in WoS is considered independently from the Democratic Republic of China (China) but whose status is disputed at an international level, was analyzed separately.

Countries responsible for publications were categorized according to their World Bank classification by income level: low-income (< USD 1025), lower-middle-income (USD 1026 to USD 4035), upper-middle-income (USD 4036 to USD 12,475), and high-income (≥ USD 12,476) countries. Each of the countries identified was assigned to a macro geographical (continental) region according to the groups established by the World Bank based on geopolitical and economic criteria and reflected in the World Bank Country and Lending Groups (see Additional file 1: Tables S2 and S3) [19].

Calculating indicators

Two kinds of indicators were obtained:

Descriptive indicators for the evolution of scientific production

We analyzed the evolution of the number of documents by year of publication and according to three 5-year periods: 2001–2005, 2006–2010, and 2011–2015. Indicators also included the frequency of publication by country, geographical region, journal and MeSH descriptor; the rate of growth in scientific production from the first to the third quinquenniums, calculated as the difference between the number of publications in 2011–2015 and those from 2001 to 2005, divided by the number of publications from 2001 to 2005.

Production by country, adjusted for demographic and economic parameters as well as for human resources dedicated to research activities

We determined standardized indicators for each country’s productivity with respect to:
  • Population: number of publications per million inhabitants (population index).

  • Gross domestic product (GDP): numbers of publications per 1 billion US dollars of GPD (GPD index).

  • Gross national income (GNI) per capita: number of publications per 100 US dollars of GNI per capita (GNI per capita index).

  • Research and development (R&D) expenditure: numbers of publications per % of GDP expenditure in R&D (R&D expenditure index).

  • Researchers in R&D: numbers of publications per researcher per million inhabitants (Researchers in R&D index)

Data were obtained from World Development Indicators in the World Bank online databases [20]. We calculated a mean value for each indicator based on available data from the study period. The analysis was limited to countries participating in the top 30 articles in the field of pneumonia in order to facilitate comparison between countries’ scientific production, demographic indicators, and economic development. Results for the top 15 articles are shown in the main text, while those for the top 30 are provided in Additional file 1.

Citation indicators

We calculated the following citation indicators by journal, country, and geographic region:
  • Citation of the publications. Absolute number of citations received.

  • Citation rate (CR). Number of citations divided by number of publications.

  • Hirsch index (h-index). The H-index is a semiqualitative proxy measure to assess the impact of an author’s or country’s research output on the scientific community [21]. An h-index of 12 indicates that 12 out of 12 published papers have been cited at least 12 times.

In order to assess the differences in the distributions of the publications according to the prestige of the journals, we performed a specific analysis of a sub-sample of publications in journals occupying the top 10% in the impact factor ranking in their respective subject categories in the Journal Citation Reports (2015 edition). We analyzed participation in these “prestigious journals” according to geographical location (regions and countries), collaboration level and number of citations.

Collaboration indicators and network analysis

We calculated the percentage of documents produced in international collaboration and the evolution by quinquennium in order to estimate the scope of cooperative practices at a global level, considering the whole population of documents analyzed (research field) by country and geographic region. To specifically analyze collaboration between countries, collaboration networks were generated for each of the three quinquenniums using Pajek software. To specifically analyze collaboration between countries, collaboration networks were generated for each of the three quinquenniums using Pajek software. The collaboration network is a graphic representation (graph), wherein the nodes represent authors’ countries (as determined from their institutional affiliations) and links between the nodes represent coauthorships between countries, that is, an international collaboration in published research. The more intense the collaboration, the thicker the links between the nodes. The spatial distribution of the nodes responds to the execution of the kamada-kawai algorithm in Pajek, which places the most prominent nodes (those with a greater number of documents and collaboration links) in the center of the map, and the nodes with a smaller number of publications and degree of collaboration towards the periphery.

Analysis of the main topics addressed in research

Based on an analysis of MeSH terms, we identified the main research focus of the studies in the area, generating density maps using the VOSviewer program with a spatial description of the main MeSH terms for each type of pneumonia [22]: (A) “Pneumonia, Aspiration” (B) “Pneumonia, Bacterial,” (C) “Pneumonia, Ventilator-Associated,” (D) “Pneumonia, Viral,” and (E) “Pneumonia, Pneumocystis”). The process of generating and interpreting the maps proceeded as follows:
  • Determination of the co-occurrence of the descriptors assigned to the documents and generation of a matrix of absolute values. The joint assignment of two descriptors in a single document implies a thematic affinity, as both aspects are addressed simultaneously in the same paper. This affinity will be more intense as it is repeated a greater number of times in the collection of documents analyzed.

  • Elimination of generic descriptors. In order to facilitate the analysis, we eliminated some excessively generic descriptors (like “humans” or “animals”), along with geographical descriptors and those related to age groups. These descriptors showed very high-density relationships, complicating the analysis and the interpretation of the results, so we analyzed their frequency more specifically.

  • Visual representation of the network. To establish the main topics that exist for each type of pneumonia and to represent them visually, we used a clustering algorithm in the VOSViewer program, which helps to detect the communities (clusters) within a network, made up of groups of homogeneous items that are strongly related to each other. The different groupings, in the form of “islands” in red tones, represent the main clusters of the thematic networks, while the chromatic gradation illustrates the areas with a lower density of relations between the MeSH in yellow and green tones. The spatial distribution of the MeSH and their proximity to each other responds to the intensity of co-occurrence between them.

All data used to perform the study, including the information downloaded from the database as well as that derived from the treatment of the bibliographic entries, are available in the Dataverse Project, an open access public repository [23] (https://dataverse.harvard.edu/, doi:  https://doi.org/10.7910/DVN/02BUNE).

Ethical aspects

Due to the nature of the study and dataset, it was not necessary to obtain informed consent or approval from an institutional ethics committee.

Results

Evolution of scientific production and distribution by country and geographic region

The search yielded a total of 33,944 documents published between 2001 and 2015 and assigned with the descriptor “Pneumonia” in the MEDLINE database. Of these, 27,017 (79.59%) were indexed in the WoS Core Collection Databases; 20,918 (77.14%) of them were classified as articles and 1776 (6.57%) as reviews. Thus, the population of study documents was a dataset of 22,694 articles and reviews, which we used to calculate the indicators presented below. Letters (N = 2213; 8.19%), editorials (N = 1, 998; 7.39%), news (N = 58; 0.21%), proceedings (N = 17; 0.06%) and other document types (N = 31, 0.11%) were excluded from the analysis.

The number of publications rose from 981 in 2001 to 1977 in 2015.The evolution of scientific production by year was fitted to a linear growth model, showing an R2 value of 0.956. Overall, the study period saw a two-fold increase in scientific production (Additional file 1: Figure S1).

The country with the greatest number of documents was the USA (38.49%), followed at some distance by the UK (7.18%), Japan (6.97%), Germany (6.80%) and France (6.73%). Table 1 shows the number of documents and the evolution of scientific production in the 15 most productive countries by quinquennium (see Additional file 1: Table S4 for results on the top 30 countries).
Table 1

Top 15 countries ranked by total number of publications by quinquenniums 2001–2005, 2006–2010, and 2010–2015

Total

 

2001–2005

2006–2010

2011–2015

Country

N of docs

%

a PPD

Country

N of docs

%

Country

N of docs

%

Country

N of docs

%

USA

8735

38.49

−4.61

USA

2248

41.13

USA

2907

39.14

USA

3580

36.52

UK

1629

7.18

0.81

France

417

7.63

Germany

521

7.01

China

827

8.44

Japan

1581

6.97

0.03

UK

403

7.37

Japan

518

6.97

Japan

725

7.40

Germany

1544

6.80

0.18

Germany

388

7.10

UK

512

6.89

UK

714

7.28

France

1527

6.73

0.30

Japan

338

6.18

France

498

6.71

Germany

635

6.48

Spain

1251

5.51

0.81

Spain

297

5.43

Spain

423

5.70

France

612

6.24

China

1126

4.96

0.11

Canada

290

5.31

Canada

361

4.86

Spain

531

5.42

Canada

1091

4.81

0.74

Netherlands

205

3.75

Italy

298

4.01

Canada

440

4.49

Netherlands

911

4.01

1.43

Italy

160

2.93

Netherlands

279

3.76

Netherlands

427

4.36

Italy

859

3.79

1.35

Australia

150

2.74

China

237

3.19

Italy

401

4.09

Australia

734

3.23

1.32

Switzerland

128

2.34

Australia

225

3.03

Australia

359

3.66

Brazil

600

2.64

1.62

Belgium

87

1.59

Brazil

213

2.87

South Korea

315

3.21

Switzerland

541

2.38

1.65

Sweden

84

1.54

Switzerland

190

2.56

Brazil

313

3.19

South Korea

534

2.35

1.5

Denmark

83

1.52

Taiwan

149

2.01

Taiwan

296

3.02

Taiwan

509

2.24

0.76

Turkey

83

1.52

South Korea

148

1.99

Switzerland

223

2.28

N of docs = numbers of documents

a PPD = Percentage point difference from 2001 to 2005 to 2011–2015

Although the USA ranks first in all periods, its relative contributions have declined, from 41.13% of all documents in 2001–2005 to 36.52% in 2011–2015. On the other hand, China’s emergence is highly notable, with a 1.13% share of total scientific production in the first period (rank = 22), compared to a 8.44% share in the third (rank = 2). South Korea has also seen considerable growth, contributing just 1.30% to total research production in 2001–2005 (rank = 19) but 3.21% in 2011–2015 (rank = 12). Likewise, Taiwan and Brazil have increased their production from 1.17 and 1.35%, respectively, to 3.02 and 3.19%.

Scientific production in different countries and geographic regions, and its evolution by quinquennium, is concentrated in North America and Europe & Central Asia; together these regions are responsible for 82.87% of the papers included in the population of documents. Research in the two regions has decreased the proportion of documents from 2001 to 2005 to 2011–2015 (− 5.46 and − 4.56%). Countries from East Asia & the Pacific and from Latin America & the Caribbean contributed with 20.90 and 4.84% of the documents, respectively. Growth was pronounced in these regions, at 13.18 and 2.52%. Table 2) (see Additional file 1: Figure S2 for a visual representation of density equalizing mapping projections).
Table 2

Geographical regions and income brackets by total number of publications and quinquennium 2001–2005, 2006–2010, and 2010–2015

 

Total

 

2001–2005

2006–2010

2011–2015

N of docs

%

a PPD

N of docs

%

N of docs

%

N of docs

%

Geographic area

 North America

9549

42.08

−5,46

2469

45.18

3187

42.91

3893

39.72

 Europe & Central Asia

9256

40.79

−4,54

2359

43.17

3110

41.87

3787

38.63

 East Asia & Pacific

4742

20.90

13,18

743

13.60

1374

18.50

2625

26.78

 Latin America & Caribbean

1099

4.84

2,52

174

3.18

366

4.93

559

5.70

 Middle East & North Africa

590

2.60

0,93

115

2.10

178

2.40

297

3.03

 Sub-Saharan Africa

523

2.30

0,35

121

2.21

151

2.03

251

2.56

 South Asia

461

2.03

1,48

56

1.02

160

2.15

245

2.50

Income bracket

0

      

 HI

20,102

88.58

−7,76

5092

93.17

6638

89.38

8372

85.41

 UMI

3094

13.63

10

434

7.94

902

12.14

1758

17.94

 LMI

803

3.54

2,43

109

1.99

261

3.51

433

4.42

 LI

222

0.98

0,74

32

0.59

60

0.81

130

1.33

N of docs = numbers of documents

a PPD = Percentage point difference from 2001 to 2005 to 2011–2015

HI high-income, UMI upper-middle-income, LMI = lower-middle-income, LI = low-income

Number of publications by country relative to population and economic parameters

Table 3 ranks the production of the top 15 countries, adjusted for demographic and economic indicators (see Additional file 1: Table S5 for results on the top 30 countries). When normalized by population, the most productive countries were Switzerland, the Netherlands, Iceland, and Denmark. Adjusted for the GDP index, the most productive LMICs were the Gambia, Malawi, Uganda, and Guinea Bissau. If we calculate the ratio of pneumonia publications to GNI per capita index, the USA, China, India, Malawi y Brazil were the most productive. Adjusting by R&D expenditure index, the USA ranked first, followed by Spain, the UK, China, and Italy. In relation to the researchers in R&D index, the USA also leads the ranking, followed by India, Uganda, and China. (see Additional file 1: Figure S3 and Figure S4 for a visual representation of density equalizing mapping projections of the number of documents and world development indicators, by GNI per capita index, GDP index and population index plus R&D expenditure index).
Table 3

Top 15 countries and world regions ranked according to population index, GDP index, GNI per capita index, R&D expenditure index and Researchers in R&D Indexb,a

Countrya

Population Indexb

Country

GPD Indexc

Country

GNI per capita Indexd

Country

R&D expenditure Indexe

Country

Researchers in R&D Indexf

Switzerland

70.32

Gambia

30.83

USA

18.31

USA

3276.91

USA

2.25

Netherlands

55.23

Malawi

9.27

China

14.08

Spain

1056.90

India

1.84

Iceland

51.70

Uganda

3.42

India

8.25

UK

993.78

Uganda

1.39

Denmark

50.54

Guinea Bissau

2.62

Malawi

5.19

China

735.50

China

1.22

Finland

40.77

Andorra

1.94

Brazil

4.83

Italy

731.10

Malawi

1.16

Belgium

37.29

Kenya

1.88

UK

4.67

France

712.03

Brazil

1.06

Sweden

35.94

Vanuatu

1.78

Japan

4.54

Germany

589.28

Tanzania

0.78

Israel

35.05

Cambodia

1.60

France

4.40

Canada

579.61

Cambodia

0.67

Australia

34.24

Nepal

1.55

Spain

4.20

Brazil

557.01

South Africa

0.62

Canada

32.71

Grenada

1.35

Germany

4.06

Turkey

532.13

Italy

0.54

USA

28.78

Israel

1.26

Uganda

4.04

Netherlands

500.78

Philippines

0.53

Spain

27.90

Papua N Guinea

1.26

Bangladesh

3.07

Japan

493.90

Colombia

0.52

Greece

26.84

Mozambique

1.25

Canada

2.89

Greece

448.47

Mozambique

0.52

UK

26.32

Netherlands

1.22

Kenya

2.86

Thailand

445.07

Turkey

0.51

New Zealand

25.65

Tunisia

1.19

Italy

2.59

Gambia

423.33

Ghana

0.50

a Monaco has a population index of 112.42 and Andorra, 75.86; these countries were excluded due to their especially small size and population b Number of publications per million inhabitants

c Number of publications per 1 billon US dollars of gross domestic product (GPD)

dNumber of publications per 100 USD dollars of gross national income (GNI) per capita

e Numbers of publications per % of GDP expenditure in Research and Development (R&D)

f Numbers of publications per researcher per million inhabitants

Impact of publications

The citation analysis by geographical regions reflects the balance in the absolute number of citations received by researchers in North America and Europe, with the rest of the regions trailing considerably. In contrast, North America presents a somewhat higher citation rate (CR) than Europe (35.76 versus 29.20); among the other regions, Africa showed the best performance on this indicator (CR 31.41), with the rest presenting values of 20.07 to 24.00. In consonance with these data, at a country level the HICs (which are mostly in Europe and North America) showed higher CRs than countries in the rest of the income categories. By individual country, articles with author affiliations from the USA were the most cited (N = 316,942), followed by articles from the UK (N = 62,612), France (N = 48,019), Spain (N = 43,459) and Germany (N = 43,434). Regarding the country-specific CR, Vietnam dominated (CR 50.79), followed by the Switzerland (CR 42.94), South Africa (CR 42.85), New Zealand (CR 40.49), Saudi Arabia (CR 38.62) and the UK (CR 38.44). The USA and the UK were the top-ranked countries with an h-Index of 197 (USA) and 106 (UK), followed by France (96), Spain (94) and Germany (94) (Table 4) (see Additional file 1: Table S6 for the 30 most productive countries).
Table 4

Citation indicators for pneumonia research: rankings by 15 top-producing countries, geographic region and income (2001–2015)

 

Citations

 

Citation Rate

 

H-index

Country

 USA

316,942

Vietnam

50.79

USA

197

 UK

62,612

Switzerland

42.94

UK

106

 France

48,019

South Africa

42.85

France

96

 Spain

43,459

New Zealand

40.49

Spain

96

 Germany

43,436

Saudi Arabia

38.62

Germany

94

 Canada

40,090

UK

38.44

Canada

88

 Netherlands

34,798

Netherlands

38.20

Netherlands

88

 Japan

30,978

Ireland

36.85

Japan

74

 Italy

25,600

Canada

36.75

Switzerland

74

 Switzerland

23,228

Sweden

36.65

Australia

71

 Australia

22,440

Denmark

36.53

Italy

70

 China

18,370

USA

36.28

Belgium

62

 Belgium

13,919

Spain

34.74

Sweden

56

 Sweden

12,203

Belgium

34.71

Denmark

55

 Brazil

11,136

Finland

34.17

China

54

Geographic area

 North America

341,438

North America

35.76

North America

202

 Europe & Central Asia

270,237

Europe & Central Asia

29.20

Europe & Central Asia

172

 East Asia & Pacific

96,628

Sub-Saharan Africa

31.41

East Asia & Pacific

103

 Latin America & Caribbean

22,740

Middle East & North Africa

24.00

Latin America & Caribbean

61

 Sub-Saharan Africa

16,426

Latin America & Caribbean

20.69

Sub-Saharan Africa

54

 Middle East & North Africa

14,159

East Asia & Pacific

20.38

Middle East & North Africa

53

 South Asia

9254

South Asia

20.07

South Asia

46

Countries by income

 HIC

593,632

HIC

29.53

HIC

222

 UMIC

58,785

LMIC

21.82

UMIC

89

 LMIC

17,523

LIC

21.46

LMIC

60

 LIC

4765

UMIC

19.00

LIC

34

HIC high-income countries, UMIC upper-middle-income countries, LMIC lower-middle-income countries, LIC low-income countries

Analysis of international collaboration

Overall, 18.80% of the articles published in the study period were written in international collaboration, although the rates increased from 14.35% in the 2001–2005 quinquennium to 21.64% in 2011–2015. Among the top 15 most productive countries, international collaboration was much more intense in the European countries, Brazil, Canada, and Australia (34 to 62%) compared to the USA (26.33%) and the most productive countries of East Asia & Pacific (China, South Korea, and Taiwan: 16 to 28%) (Table 5). The very high levels of international collaboration are even more pronounced in some Latin American, South Asia and particularly African countries. Indeed, the analysis of collaboration by geographical regions shows that globally, sub-Saharan Africa collaborated on 46.08% of the papers produced. The results for Latin America and the Caribbean (22.66%) are heavily weighted by research from Brazil, but the rates of international collaboration were 63.01% in Colombia, 60.94% in Argentina, and 52.21% in Mexico, while in East Asia & Pacific and South Asia (and looking beyond the most productive countries like China), countries like Bangladesh showed levels of international collaboration of 73.61%; Thailand, 60.29%; and Pakistan, 58.82%.
Table 5

Rates of international collaboration (%) in the top 15 most productive countries and by world region, pneumonia research output (2001–2015)

 

Total

2001–2005

2006–2010

2011–2015

N docs

N docs Int col

%

N docs

N docs Int col

%

N docs

N docs Int col

%

N docs

N docs Int col

%

Country

 USA

8735

2300

26.33

2248

427

18.99

2907

761

26.18

3580

1112

31.06

 UK

1629

811

49.82

403

156

38.71

512

241

47.07

714

414

57.98

 Japan

1581

285

18.03

338

58

17.16

518

94

18.15

725

133

18.34

 Germany

1544

626

40.54

388

113

29.12

521

186

35.70

635

327

51.50

 France

1527

513

33.59

417

98

23.50

497

155

31.19

613

260

42.41

 Spain

1251

422

33.73

297

61

20.54

423

124

29.31

531

237

44.63

 Peoples R. China

1126

320

28.42

62

21

33.87

237

91

38.40

827

208

25.15

 Canada

1091

503

46.10

290

112

38.62

361

145

40.17

440

246

55.91

 Netherlands

911

414

45.44

205

69

33.66

279

127

45.52

427

218

51.05

 Italy

859

345

40.16

160

43

26.88

298

115

38.59

401

187

46.63

 Australia

734

355

48.37

150

65

43.33

225

111

49.33

359

179

49.86

 Brazil

600

216

36

74

30

40.54

213

75

35.21

313

111

35.46

 Switzerland

541

337

62.29

128

62

48.44

190

123

64.74

223

152

68.16

 South Korea

534

105

19.66

71

19

26.76

148

32

21.62

315

54

17.14

 Taiwan

509

83

16.31

64

11

17.19

149

23

15.44

296

49

16.55

Total international collaboration

22,593

4248

18.80

5442

781

14.35

7373

1351

18.32

9778

2116

21.64

Geographic area

 North America

9549

1276

13.36

2469

216

8.75

3187

407

12.77

3893

653

16.77

 Europe & Central Asia

9256

1033

11.16

2359

167

7.08

3110

341

10.96

3787

525

13.86

 East Asia & Pacific

4742

610

12.86

743

100

13.46

1374

209

15.21

2625

301

11.47

 Latin America & Caribbean

1099

249

22.66

174

45

25.86

366

68

18.58

559

136

24.33

 Middle East & North Africa

590

110

18.64

115

14

12.17

178

28

15.73

297

68

22.90

Sub-Saharan Africa

523

241

46.08

121

43

35.54

151

67

44.37

251

131

52.19

 South Asia

461

108

23.43

56

10

17.86

160

33

20.63

245

65

26.53

Total world region collaboration

22,593

3109

13.76

5442

536

9.85

7373

1007

13.66

9778

1566

16.02

Figure 1 shows the collaboration networks between different countries by quinquennium. The most prominent countries in all time periods, occupying central positions in the networks with multiple cooperative links, are the USA, Canada, the UK, Germany, France, and the Netherlands. The presence of South American and African countries is scarce in all periods. Only South Africa has a notable presence in the third quinquennium (Fig. 1a). A few other countries also “emerge” with a high degree of collaborative links in the second period, like Spain, Greece, Italy, Australia, China, and Japan, although the latter two countries are not fully integrated in global networks, showing collaborative ties only with the USA (Fig. 1b). Finally, other European countries, while present throughout all three periods, stand out to a greater degree in the third period. This is the case of Sweden, Switzerland, Belgium, and Austria. At the same time, China and Japan seem more implicated in the network in this third period, while India and South Korea also gain relevance (Fig. 1c).
Fig. 1

Networks generated from international collaborations, by quinquennium: (a) 2001–2005, (b) 2006–2010, and (c) 2011–2015

The intensity of collaboration is reflected through the thickness of the links. The most prominent nodes (those with a greater number of documents and collaboration links) are in the center of the map, while the nodes with a smaller number of publications and lower degree of collaboration are located on the periphery

Journals of publication

The documents we analyzed were published in 2115 scientific journals. Twelve journals accounted for 16.63% of the pneumonia literature Table 6
Table 6

Top 15 most productive journals and their citation indicatiors, pneumonia research 2001–2015)

Top 15 journals

N. of docs

%

CR

Impact factor 2015

Journal category (ranking)

PLOS ONE

494

2.18

15.12

3.057

Multidisciplinary Sciences (11 of 63)

Clinical Infectious Diseases

412

1.81

63.96

8.736

Immunology (9 of 151)

Infectious Diseases (2 of 83)

Microbiology (10 of 123)

Chest

397

1.75

55.95

6.136

Respiratory System (6 of 58)

Critical Care Medicine (5 of 33)

Journal of Immunology

354

1.56

49.10

4.985

Immunology (32 of 151)

American Journal of Physiology-Lung Cellular and Molecular Physiology

323

1.42

34.96

4.721

Physiology (8 of 83)

Respiratory System (8 of 58)

Critical Care Medicine

291

1.28

55.15

7.422

Critical Care Medicine (4 of 33)

European Respiratory Journal

283

1.25

42.49

8.332

Respiratory System (3 of 58)

Infection and Immunity

256

1.13

37.77

3.603

Immunology (56 of 151)

Infectious Diseases (20 of 83)

American Journal of Respiratory And Critical Care Medicine

256

1.13

88.46

13.118

Critical Care Medicine (2 of 33)

Respiratory System (2 of 58)

American Journal of Respiratory Cell and Molecular Biology

251

1.11

32.77

4.082

Biochemistry & Molecular Biology (74 of 289)

Cell Biology (64 of 187)

Respiratory System (10 of 58)

Antimicrobial Agents and Chemotherapy

213

0.94

27.84

4.415

Microbiology (22 of 123)

Pharmacology & Pharmacy (34 of 255)

Intensive Care Medicine

212

0.93

42.65

10.125

Critical Care Medicine (3 of 33)

Journal of Clinical Microbiology

209

0.92

29.54

3.631

Microbiology (36 of 123)

Pediatric Infectious Disease Journal

196

0.86

28.09

2.587

Immunology (84 of 151)

Infectious Diseases (38 of 83)

Pediatrics (22 of 120)

Vaccine

190

0.84

22.98

3.413

Immunology (60 of 151)

Medicine. Research & Experimental (36 of 124)

CR citation rate

. shows a list of the 15 top journals with the highest number of papers published from 2001 to 2015, as well as their impact factors for the year 2015, subject category according to the Journal Citation Reports classification, and CR (Additional file 1: Table S7 for results on the top 30 journals). The journals publishing the most articles on pneumonia were PLOS ONE (N = 494), Clinical Infectious Diseases (N = 412), and Chest (N = 397), whereas the journals with the most citations were Clinical Infectious Diseases, (N = 26,351), American Journal of Respiratory and Critical Care (N = 22,647), and Chest (N = 22,212); all of these were also among the 15 most productive journals. The journals with the highest CRs were the New England Journal of Medicine (75 documents, CR 278.13), The Lancet (54 documents, CR 210.17) and JAMA (49 documents, CR = 199.71) (see Additional file 1: Table S8 for results on the top 30 journals with highest absolute and relative citations).

The comparative analysis of the scientific production and CRs of different journals is noteworthy in that some journals (such as the American Journal of Respiratory and Critical Care, Critical Care Medicine, and Intensive Care Medicine) present a very high CR in relation to their total scientific production (Additional file 1: Figure S5 for the top 15 journals producing the most research on pneumonia, plus citation rates).

With regard to the subject categories to which the journals are assigned, the most prominent are “Infectious Diseases” (17.57% of the documents), “Respiratory System” (15.77%), “Immunology” (14.08%), “Microbiology” (11.85%), and “Critical Care Medicine” (9.26%) Table 7.
Table 7

Top 15 Web of Science Categories in pneumonia research (2001–2015)

 

2001–2015

2001–2005

2006–2010

2011–2015

WoS Category

N

%

N

%

N

%

N

%

Infectious Diseases

3987

17.57

957

17.51

1374

18.50

1656

16.89

Respiratory System

3579

15.77

989

18.10

1192

16.05

1398

14.26

Immunology

3195

14.08

799

14.62

1143

15.39

1253

12.78

Microbiology

2690

11.85

725

13.27

899

12.10

1066

10.88

Critical Care Medicine

2101

9.26

584

10.69

742

9.99

775

7.91

Medicine, General & Internal

2038

8.98

569

10.41

622

8.37

847

8.64

Pharmacology & Pharmacy

1664

7.33

382

6.99

526

7.08

756

7.71

Pediatrics

1574

6.94

437

8.00

565

7.61

572

5.84

Surgery

1091

4.81

270

4.94

387

5.21

434

4.43

Public, Environmental & Occupational Health

962

4.24

187

3.42

330

4.44

445

4.54

Veterinary Sciences

879

3.87

273

5.00

268

3.61

338

3.45

Medicine, Research & Experimental

714

3.15

149

2.73

223

3.00

342

3.49

Biochemistry & Molecular Biology

661

2.91

143

2.62

194

2.61

324

3.31

Cell Biology

602

2.65

150

2.74

170

2.29

282

2.88

Multidisciplinary Sciences

576

2.54

7

0.13

65

0.88

504

5.14

Many of the most productive journals in pneumonia also fall into these subject categories. Moreover, over the course of the three study periods, nearly all of the subject categories saw a moderate decrease in their relative contribution, as research articles became more dispersed and made headway into different disciplines producing less research on pneumonia Table 7.
Table 8

Distribution of participation by countries in the most prestigious 10% of journals

Country

N of docs

%

Rank

N docs International collaboration

%

N cites

Citation Rate

Rank

USA

1954

47.66

1

627

32.09

139,247

71.26

1

UK

473

11.54

2

263

55.6

34,471

72.88

2

Japan

132

3.22

11

55

41.67

6782

51.38

11

Germany

285

6.95

5

177

62.1

16,636

58.37

7

France

401

9.78

3

152

37.9

26,174

65.27

3

Spain

373

9.1

4

173

46.38

25,387

68.06

4

China

105

2.56

12

51

48.57

4926

46.91

14

Canada

271

6.61

6

141

52.03

19,291

71.18

5

Netherlands

256

6.24

7

118

46.09

16,820

65.7

6

Italy

174

4.24

8

111

63.79

11,626

66.82

9

Australia

161

3.93

9

89

55.28

9688

60.17

10

Brazil

78

1.9

14

49

62.82

2629

33.7

22

Switzerland

154

3.76

10

113

73.38

13,206

85.75

8

South Korea

50

1.22

19

19

38

2226

44.52

23

Taiwan

41

1

22

15

36.58

1568

38.24

30

Analysis of collaboration and citation in a top 10% de las prestigious journals

The analysis of the 4100 documents published in the top 10% of prestigious journals shows a higher participation from the USA (27.66%, compared to 38.49% in the overall body of documents) and from some other European countries like the UK or Spain. In contrast, the weight of Asian countries, particularly Japan and China, is much lower (Table 8). Overall, international collaboration in these journals (N = 1065, 25.98%) was sensibly higher than in the overall body of documents (18.8%), and the greater degree of collaboration was much more pronounced for countries like Brazil, Japan, China, and even European countries like Italy and Germany (Table 8).

The high degree of collaboration was also confirmed between regions in the publications appearing in these journals (Table 9). With regard to the degree of citation, we observed notable increases in the citation rate of the USA and the European countries; these were even more significant for countries in the Middle East & North Africa, and for sub-Saharan Africa when they participated in these journals (Table 9).
Table 9

Distribution of participation by countries in the most prestigious 10% of journals

Geographic area

N of docs

%

N docs world region collaboration

%

Citation

Citation Rate

North America

2138

52.15

630

29.47

149,290

69.83

Europe & Central Asia

1978

48.24

600

30.33

125,727

63.56

East Asia & Pacific

543

13.24

241

44.38

28,248

52.02

Latin America & Caribbean

152

3.71

109

71.71

8246

54.25

Middle East & North Africa

75

1.83

45

60

6383

85.11

Sub-Saharan Africa

105

2.56

93

88.57

8568

81.6

South Asia

70

1.71

51

72.86

3855

55.07

Analysis of subject areas; frequency and distribution of MeSH terms

With regard to types of pneumonia studied, the MeSH terms to appear most frequently were “Pneumonia, Bacterial” (19.99%), followed by “Pneumonia, Pneumococcal” (7.02%), and “Pneumonia, Ventilator-Associated” (6.79%). Table 10 shows the number of documents assigned to each term describing the different types of pneumonia (Additional file 1: Table S10 for the 30 top general MeSH).
Table 10

Number of documents assigned to MeSH terms describing different types of pneumonia

MeSH Term

N of docs

%

Pneumonia MeSH

 Pneumonia, Bacterial

4536

19.99

 Pneumonia, Pneumococcal

1593

7.02

 Pneumonia, Ventilator-Associated

1542

6.79

 Pneumonia, Pneumocystis

1323

5.83

 Pneumonia, Viral

1212

5.34

 Pneumonia, Aspiration

1109

4.89

 Pneumonia, Mycoplasma

887

3.91

 Pneumonia, Staphylococcal

423

1.86

 Bronchopneumonia

310

1.37

 Pneumonia of Swine, Mycoplasmal

226

1.00

 Pleuropneumonia

129

0,57

 Pneumonia, Lipid

70

0.31

 Pneumonia of Calves, Enzootic

38

0.17

 Chlamydial Pneumonia

24

0.11

 Pneumonia, Rickettsial

2

0.01

 Pneumonia, Necrotizing

0

0.00

N of docs numbers of documents

Table 11 ranks the top 15 countries in crude numbers of retrieved articles, stratified by types of pneumonia (Additional file 1: Table S11 for information on the 30 most productive countries). For “Pneumonia, Aspiration”, the main countries were the USA, Japan, and Germany; for “Pneumonia, Bacterial”, the USA, France, and Spain; for “Pneumonia, Pneumocystis”, the USA, France, and the UK; for “Pneumonia, Ventilator-Associated”, the USA, France, and Spain; and for “Pneumonia, Viral”, the USA, China, and Japan.
Table 11

Distribution of research articles on different pneumonia types amont 15 most productive countries

Pneumonia, Aspiration

Pneumonia, Bacterial

Pneumonia, Pneumocystis

Pneumonia, Ventilator-Associated

Pneumonia, Viral

Country

N of docs

Country

N of docs

Country

N of docs

Country

N of docs

Country

N of docs

USA

394

USA

1709

USA

525

USA

650

USA

383

Japan

169

France

379

France

149

France

170

China

98

Germany

78

Spain

378

UK

106

Spain

139

Japan

95

UK

74

Germany

329

Japan

104

Greece

72

UK

83

Australia

45

Japan

297

Spain

64

Canada

69

Germany

81

Canada

44

UK

252

Germany

58

UK

68

Spain

71

France

40

Canada

209

Italy

46

Germany

67

France

66

Spain

39

Italy

176

Switzerland

38

China

63

Italy

59

Turkey

31

Netherlands

173

China

38

Brazil

63

Canada

48

China

25

China

171

South Africa

35

Italy

63

Netherlands

47

Italy

24

Australia

123

Denmark

28

Turkey

58

South Korea

41

South Korea

22

Taiwan

104

Canada

27

Netherlands

53

Finland

39

Switzerland

21

Switzerland

103

Taiwan

27

Australia

49

Australia

29

Netherlands

21

Brazil

100

Netherlands

25

Belgium

45

Brazil

26

Taiwan

21

South Korea

92

Australia

23

India

39

Thailand

21

N of docs numbers of documents

Table 12 shows the relationship between MeSH terms referring to age groups with those corresponding to different types of pneumonia. The closest associations for “Aged, 80 and over” and “Aged” were with “Pneumonia, Aspiration” (22.58 and 40.56%, respectively), while “Pneumonia, Viral” was the most frequent topic for studies in pre-adults (“Infant”, “Child”, “Child, preschool” and “Adolescent”). The one exception to this was “Infant, newborn”, where the highest proportion of articles was about “Pneumonia, Pneumocystis.” In “Adult” and “Middle aged” people, studies most frequently focused on “Pneumonia, Bacterial” and “Pneumonia, Ventilator-Associated.”
Table 12

Distribution of MeSH terms referring to age groups, by main types of pneumonia studied in those groups

MeSH age

Pneumonia, Aspiration

Pneumonia, Bacterial

Pneumonia, Ventilator-Associated

Pneumonia, Pneumocystis

Pneumonia, Viral

N of docs

rank

%

N of docs

rank

%

N of docs

rank

%

N of docs

rank

%

N of docs

rank

%

Infant, newborn

51

9

4.61

143

10

3.15

80

10

5.20

112

10

9.24

35

10

2.65

Infant

98

8

8.85

140

5

10.58

89

8

5.79

278

4

22.94

278

4

22.94

Child, preschool

100

7

9.03

91

8

6.88

85

9

5.53

268

5

22.11

268

5

22.11

Child

117

5

10.57

124

6

9.37

100

7

6.50

222

7

18.32

222

7

18.32

Adolescent

107

6

9.67

148

4

11.19

145

5

9.43

250

6

20.63

250

6

20.63

Adult

280

3

25.29

548

1

41.42

493

3

32.05

397

1

32.76

397

1

32.76

Young adult

44

10

3.97

266

9

5.86

133

6

8.65

126

9

10.40

95

7

7.18

Middle aged

366

2

33.06

502

2

37.94

680

1

44.21

348

2

28.71

348

2

28.71

Aged

449

1

40.56

288

3

21.77

496

2

32.25

281

3

23.18

281

3

23.18

Aged, 80 and over

250

4

22.58

88

9

6.65

188

4

12.22

134

8

11.06

134

8

11.06

N of docs numbers of documents

Figure 2 shows the subject area maps with the main MeSH terms in the documents on (a) “Pneumonia, Aspiration”; (b) “Pneumonia, Bacterial”; (c) “Pneumonia, Ventilator-Associated”; (d) “Pneumonia, Viral”; and (e) “Pneumonia, Pneumocystis.” The principal MeSH term related to “Pneumonia, Aspiration” is “Deglutition Disorder”, but research is linked to a broad array of topics, including epidemiological aspects (“Incidence”, “Risk Factor”, “Retrospective Studies”), treatment approaches in intensive care, and surgical techniques procedures facilitating breathing, swallowing, and feeding (Fig. 2a).
Fig. 2

Subject area maps with the main MeSH terms associated with different types of pneumonia-(a) “Pneumonia, Aspiration” (b) “Pneumonia, Bacterial, ” (c) “Pneumonia, Ventilator-Associated, ” (d) “Pneumonia, Viral, ” and (e) “Pneumonia, Pneumocystis”

Groupings in the form of “islands” in red tones represent the main clusters of the thematic networks, while the chromatic gradation in yellow and green tones illustrates the areas with a lower density of relations between the MeSH. The spatial distribution of the MeSH and their proximity to each other responds to the intensity of co-occurrence between them

The two main MeSH terms that appear most frequently with “Pneumonia, Bacterial” are “Community-acquired Infections” and “Anti-bacterial Agents”, reflecting the central focus that research has taken to identify risk factors and test different therapeutic approaches. MeSH terms related to specific bacteria and infections, such as Streptococcus, Chlamydia, Acinetobacter, and Haemophilus influenzae, are also prominent (Fig. 2b).

For its part, research on “Pneumonia, Ventilator-associated” seems more disperse, although three areas of interest can clearly be differentiated: (a) epidemiological studies, clinical protocols, and treatment in intensive care units (the term “Intensive Care Unit” is the most prominent in this area); (b) treatment outcomes (“Treatment outcome” and “Anti-Bacterial Agents”); and (c) cross infections (“Cross infection”) (Fig. 2c).

Research on “Pneumonia, Viral” also shows a disperse nature, with different areas of interest. Epidemiological aspects are covered under terms such as “Community-acquired Infections” and “Hospitalization”, while at a researcher level, interests reside in the virus “Influenza, Human” and “Orthomyxoviridae Infections” (Fig. 2d). With regard to “Pneumonia, Pneumocystis”, one prominent subject focus is on “AIDS-Related Opportunistic Infections” and another is on “Pneumocystis jirovecii” (Fig. 2e).

Discussion

Our analysis shows that the number of publications on pneumonia increased notably over the study period, with annual research outputs doubling from 2001 to 2015. Different factors may have contributed to this. The first of these is the growing research relevance of pneumonia as a clinical entity, as this disease is one of the community-acquired infections with the highest incidence and is an important cause of hospital admissions. It is also associated with a high global burden of morbidity and mortality in both children and adults [1, 2, 3, 24]. The second potential factor relates to advances in basic immunological and microbiological research along with deepening knowledge on the pathogenesis of the disease with regard to aspects like microbiological resistance and preventive interventions (e.g. vaccines) [25]. Thirdly, increased funding has been directed toward research and particularly “proactive investments for emerging infectious threats” [8, 9], and finally, the increase in scientific production could be related to scientific development and international dissemination of scientific research in the WoS databases. This is particularly the case of China and other emerging economies like Brazil, where the rates of growth were highest relative to their respective regions [26, 27, 28].

We observed a substantial increase in research worldwide, but particularly in some geographical regions and countries of South Asia, East Asia & the Pacific, Latin America & and the Caribbean, and sub-Saharan Africa. To a great extent, this increase is simply a reflection of the limited contribution to global research that these countries made in the first period analyzed (2001–2005). The bulk of scientific production continues to come from countries with more economic and scientific development in Europe and North America (together, these countries participated in 77% of all publications).

Despite the striking increase in scientific production across LMICs, the relative contribution to pneumonia research remains very modest, and the fact that some countries rank highest in demographic and economic indicators may not be a positive feature, but rather a reflection of the scant development in their scientific systems. Furthermore, the increase in international collaboration could have played a role in these indicators, multiplying the assignment of articles to different countries and possibly inflating some values, masking the real contribution of countries with less scientific development in research activities [29].

The USA is undoubtedly the main reference for pneumonia researchers in quantitative terms, as it produces by far the largest volume of publications—four times that of the next most productive country in the last period. Other European countries with important scientific systems (e.g. the UK, Germany, France, and Spain), along with other countries like Japan, Canada, China, India, and Brazil, also stand out in relation to some of the indicators of scientific production and economic development (GNI per capita index, and R&D expenditure Index). The other significant aspect in the analysis of how scientific production evolved over the study period is the emergence of China, which in the last period of study (2011–2015) trailed only the USA in research output. This growth has come about in large part from the investments and scientific policies to foster openness that have been implemented over the past several decades to promote internationalization [30, 31].

The level of international scientific collaboration that we have observed in the field of pneumonia (19%) is below that seen in other areas of knowledge [11, 29, 30, 32, 33, 34, 35]. Thus, even though the trend is toward increased international cooperation, rising from 14 to 22% over the study period, implementing new strategies that favor collaboration is still necessary [11].

Initiatives promoting research could include those launched by international organizations, such as the World Health Organization (WHO) and the Bill & Melinda Gates Foundation, which have both invested considerable resources to investigate the etiology of childhood pneumonia in low-income countries [36, 37, 38]. However, these initiatives carry risks too, as major actors in LMIC research, including the Bill & Melinda Gates Foundation, have been shown to be biased toward research done by researchers from HIC (doing research in LMIC) [39].

The European and Developing Countries Clinical Trials Partnership and the Global Fund [40] are also collaborating in different projects related to HIV, tuberculosis, and malaria, and these organizations are largely responsible for the important degree of collaboration between European and sub-Saharan African countries [41]. Research for operational health services is necessary to improve the distribution and accessibility of pneumonia treatments, including antibiotics in primary healthcare centers and oxygen in hospitals. Likewise, new vaccines still need to be developed for strains of pneumococcus that current multivalent conjugate vaccines do not protect against [8].

In addition to programs focused on financing and implementing collaborative North-South and South-South projects, other efforts could be directed toward reducing obstacles associated with publication processes that limit the dissemination of LMICs through the main international scientific journals. The literature has described obstacles related to linguistic skills and methodological deficiencies, which highlights the need to improve these areas in particular [42, 43]. Other authors have pointed to the costs associated with publishing in open access journals, so it is worth assessing whether the programs to support open access publishing implemented at an institutional level and by publishers such as PLOS, Biomed Central, or The Lancet Journals, are sufficient [44, 45, 46].

With regard to the impact of research, although Europe and North America are balanced in terms of the absolute number of citations, North America holds an advantage in terms of the citation rate. Research from sub-Saharan Africa also has a very high citation rate, which almost reaches that achieved in Europe. The fact that these African countries present a high degree of collaboration with researchers in the USA and Europe, who represent the “mainstream” international research interests, could help explain the high citation rates seen in this region. On the other hand, Latin America & Caribbean, South Asia, and East Asia & Pacific are all regions with generally lower citation rates, although this difference is not so pronounced in the case of papers produced in collaboration, as reported elsewhere [47].

By country, the hegemony of the USA and several European countries in terms of the number of citations received was evident, as was the lower ranking of some Asian countries, such as Japan and China, in relation to their scientific production. The positioning of China as a reference for scientific production and participation in international research networks does not correspond to its ranking with regard to citation indicators, despite their improved standing over the past several years [30]. On these indicators, China still lags behind the USA as well as the leading European countries, Canada, Australia and even nearby countries such as Japan. For now at least, the countries that have traditionally occupied the “mainstream” of scientific research still maintain their hegemony [48].

As with the relative indicators of scientific production adjusted for economic and demographic parameters, some countries surpass the major scientific systems with regard to the citation rate, which links the degree of citation with the volume of scientific production [33]. These countries may have participated in certain highly relevant contributions, or they may be small countries with highly developed scientific systems, such as Vietnam, Switzerland, South Africa, New Zealand, and Saudi Arabia. These countries also stand out for their high levels of international collaboration, which is a factor associated with more citations.

The high mean citations received by publications produced in sub-Saharan Africa, and the participation of different emerging countries like Vietnam and South Africa in some of the highest cited papers we identified, underlines the capacity of these countries to contribute to high-impact and excellent-quality scientific studies. This result is consistent with previous studies that have also demonstrated these countries’ capacity to participate in emerging research topics [49]. These specialists therefore represent an excellent asset, strengthening the human capital from high-income countries and enabling the advancement of research [50, 51].

In general, the most prestigious journals show a greater concentration of research from the USA and Europe, with greater collaboration and impact when countries from other geographical regions also participate [52].

Bacterial pneumonia is the main branch for the multidisciplinary and multipathological MeSH of “Pneumonia”, with the main areas of interest (“Community-acquired Infections”, “Anti-bacterial Agents” and “Treatment Outcome”) reflecting the focus of research on identifying risk factors and assessing different treatments and their outcomes. In publications pertaining to the MeSH “Pneumonia, Ventilator-Associated,” the main axes of the subject content according to the MeSH terms were the group of epidemiological studies and clinical and treatment protocols in intensive care. “Pneumonia Pneumocystis,” is closely related to infection due to HIV and immunodepression. The main areas of research interest for “Pneumonia, Viral,” were the epidemiological aspects related to the setting for the infection (“Community-acquired Infections” and “Hospitalization”) along with the viruses responsible (“Influenza, Human” and “Orthomyxoviridae Infections”). Finally, for the MESH “Pneumonia, Aspiration” the main research focus is “Deglutition Disorder”.

The main limitation of this present study is its analysis of only the documents included in the WoS databases and MEDLINE (80% of the documents). Thus, a number of papers were excluded from the study, particularly those written in languages other than English, as well as the proceedings included in WoS, as our searches were based on the journals included in MEDLINE. On the other hand, our approach also allowed us to precisely characterize collaboration in the area, as only recently has MEDLINE begun to include all the institutional affiliations of the authors. We were also able to analyze the citations of the publications, with a focus on the journals with the highest impact and dissemination at an international level [28].

In conclusion, pneumonia research increased steadily over the 15-year study period, with Europe and North America leading scientific production. About a fifth of all papers reflected international collaborations, and these were most evident in papers from sub-Saharan Africa and South Asia.

Notes

Acknowledgements

We gratefully acknowledge the assistance of Meggan Harris in translating our manuscript from Spanish.

Authors’ contributions

JMRR: study conception, study, design, data analysis, manuscript writing and final manuscript approval; HPC: data collection, data analysis, manuscript writing and final manuscript approval; IBR: study conception, manuscript writing and final manuscript approval; GGA: study conception, study design, data collection, data analysis, manuscript writing and final manuscript approval

Funding

No funding was received for this work.

Ethics approval and consent to participate

Due to the nature of the study and dataset, it was not necessary to obtain informed consent or approval from an institutional ethics committee.

Consent for publication

The authors give consent to publish the manuscript.

Competing interests

The authors declare that they have no competing interests.

Supplementary material

12874_2019_819_MOESM1_ESM.docx (7 mb)
Additional file 1: Table S1. Descriptors included under the MeSH “Pneumonia” in PubMed. Table S2. Countries by regions according to World Bank Country and Lending Groups. Table S3. Countries by incomes according to World Bank Country and Lending Groups. Table S4. Top 30 countries ranked by total number of publications by quinquennium 2001–2005, 2006–2010 and 2011–2015. Table S5. Top 30 countries and world regions ranked according to according to population index, GDP index, GNI per capita index, R&D expenditure index and Researchers in R&D Index. Table S6. Top 30 countries ranked according to citations, citation rate and h-Index in the period 2001–2015. Table S7. Top 30 journals with the highest number of pneumonia articles published in 2001–2015, citations, citation rate (CR), impact factors for the year 2015, journal category with ranking from the Journal Citation Report and language of publication. Table S8. Top 30 journals with citations and citations rate (CR). Table S9. Top 30 citations rate (CR) journal *. Table S10. The 30 top general Medical Subject Headings (MeSH). Table S11. Top 30 countries in crude numbers of retrieved articles in “Pneumonia, Aspiration”, “Pneumonia, Bacterial”, “Pneumonia Pneumocystis”, “Pneumonia, Ventilator-Associated”, and “Pneumonia, Viral” MeSH. Figure S1. Evolution of scientific production on pneumonia (2001–2015). Figure S2. Density equalizing mapping projections. Number of documents per quinquennium for scientific production on pneumonia, (A) 2001–2005; (B) 2006–2010, and (C) 2011–2015. Figure S3. Density equalising mapping projections: number of documents and world development indicators, (A) GNI per capita index; (B) GDP index. Figure S4. Density equalising mapping projections: number of documents and world development indicators (A) population index; (B) R&D expenditure index. Figure S5. Top 15 journals producing the most research on pneumonia, plus citation rates. (DOCX 7194 kb)

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Authors and Affiliations

  1. 1.Department of Internal MedicineGeneral University Hospital of AlicanteAlicanteSpain
  2. 2.Department of Clinical MedicineMiguel Hernandez University of Elche de ElcheAlicanteSpain
  3. 3.Service of DermatologyGeneral University Hospital of AlicanteAlicanteSpain
  4. 4.Department of History of Science and DocumentationUniversity of ValenciaValenciaSpain

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