Environ Sci Pollut Res DOI 10.1007/s11356-014-3925-1

RESEARCH ARTICLE

Temporal trend, geographic distribution, and publication quality in asbestos research Donatella Ugolini & Stefano Bonassi & Alfonso Cristaudo & Giacomo Leoncini & Giovanni Battista Ratto & Monica Neri

Received: 23 July 2014 / Accepted: 27 November 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Asbestos is a well-known cause of cancer and respiratory diseases. The aim of the current study was to investigate the scientific production in asbestos research evaluating temporal trend, geographic distribution, impact factor (IF) of published literature, and taking into account socioeconomic variables. The PubMed database was searched starting from 1970. Publication numbers and IF were evaluated as absolute values and after standardization by population and gross domestic product (GDP). Six thousand nine hundred seven articles related to asbestos were retrieved. Publications grew steeply in the 1970s, leveled off in the 1980s, decreased in the 1990s, and then increased again. Mesothelioma, lung neoplasms, and occupational diseases are the most commonly used keywords. In the period of 1988–2011, 4220 citations were retrieved, 3187 of whom had an impact factor. The US, Italy, and the UK were the most productive countries. European countries published about 20 % more asbestos-related Responsible editor: Philippe Garrigues D. Ugolini (*) Department of Internal Medicine, University of Genoa, Genoa, Italy e-mail: [email protected] D. Ugolini Unit of Clinical Epidemiology, IRCCS AOU San Martino-IST-Istituto Nazionale per la Ricerca sul Cancro, Genoa, Italy S. Bonassi : M. Neri Unit of Clinical and Molecular Epidemiology, IRCCS San Raffaele Pisana, Rome, Italy A. Cristaudo Unit of Occupational Preventive Medicine, Azienda Ospedaliera Universitaria Pisana, Pisa, Italy G. Leoncini : G. B. Ratto Unit of Thoracic Surgery, IRCCS AOU San Martino-IST-Istituto Nazionale per la Ricerca sul Cancro, Genoa, Italy

articles than the US, although the latter reached a higher mean IF, ranking second after Australia. When the national scientific production (sum of IF) was compared taking into account socioeconomic variables, Australia and Scandinavian countries performed very well, opposite to all main asbestos producers like Russia, China, and Brazil (except for Canada). The American Journal of Industrial Medicine and the Italian La Medicina del Lavoro published the highest numbers of articles. This study provides the first bibliometric analysis of scientific production in asbestos research. Interest appears to be higher in selected countries, with strong national features, and is growing again in the new millennium. Keywords Asbestos . Occupational exposure . Environmental pollution . Respiratory diseases . Publications . Bibliometrics

Introduction Asbestos is the generic commercial designation for a group of naturally occurring mineral silicate fibers of the serpentine and amphibole series. These include the serpentine mineral, chrysotile (white asbestos), and the five amphibole minerals, crocidolite (blue asbestos), amosite (brown asbestos), anthophyllite, tremolite, and actinolite (International Agency for Research on Cancer 2012). Asbestos was largely used in the second half of the last century because of its resistance to fire and heat. The demand for asbestos peaked around 1977, when some 25 countries produced a combined total of 4.8 million metric tons per year, manufactured in 85 countries (Virta 2006). The global use of asbestos has decreased since then, but remained fairly stable at 2 million metric tons per year during 2011– 2012 (US Geological Survey 2013). The majority of this volume was consumed by industrializing countries, notably Asian countries and Commonwealth of Independent States

Environ Sci Pollut Res

(CIS) (Le et al. 2011; Park et al. 2011; US Geological Survey 2013). World Health Organization (WHO) (2006) asserts that “asbestos is one of the most important occupational carcinogens causing about half of the deaths from occupational cancer”. The risks associated with the use of asbestos are well documented, in particular for crocidolite (blue asbestos) and amosite (brown asbestos), as reported in 1972 by the International Labor Organization (ILO) and the International Agency for Research on Cancer (IARC). The risk of chrysotile (white asbestos) was evaluated by the IARC in the 1980s, and an asbestos convention was upheld by the ILO in 1986. Based upon this evidence, the IARC concluded that asbestos was carcinogenic to humans and classified this agent as a group 1 carcinogen (International Agency for Research on Cancer 1973; International Agency for Research on Cancer 1977; International Agency for Research on Cancer 1987; International Labor Organization 2013). Asbestos-related diseases comprise lung cancer, malignant mesothelioma, asbestosis (fibrosis of the lungs), pleural plaques, thickening, and effusions. In addition, IARC concluded in the 2009 that several non-pulmonary forms of cancer can be caused by exposure to asbestos, such as cancers of the larynx and ovary with sufficient evidence and colorectum, pharynx, and stomach cancer with limited evidence (Straif et al. 2009). Asbestos exposure may also be associated with risks of systemic autoimmune disease, and a possible link between asbestos exposure and cardiovascular disease was recently reported (Harding et al. 2012). Asbestos-linked cancers have a typically long latency period, i.e., at least 10–20 years for lung cancer and up to 50 years for pleural mesothelioma (Carbone et al. 2002; Merler et al. 1997; Niklinski et al. 2004), presumably the longest lag among occupational cancers. The oncogenic effect of exposure to high levels of asbestos fibers was reported first in the 1930s in Great Britain, while in the mid-60s, it became clear to the scientific community that even low exposures could cause cancer (Alleman and Mossman 1997). When in the 1980s asbestos carcinogenicity became incontrovertible, many industrialized countries banned its use (Kazan-Allen 2005; Kazan-Allen 2013; Peto et al. 1995). As a result of these restriction and assuming a minimum latency period of 20 years, a peak of mesothelioma incidence related to asbestos use should be observed from 2000 to 2005 for the US and in the 2011 through 2027 for Australia, Japan, Italy, and the UK (Robinson 2012). Bibliometrics is a quantitative method to evaluate academic literature. The basic bibliometric measures are number of papers and impact factor (IF), indexes of quantity, and quality of scientific production, respectively. The IF is based on citation analysis, i.e., the number of times an article is cited

as a reference in other articles, and is based on the general assumption that the number of citations reflects an article’s influence and notoriety and, hence, its quality (Garfield 1970; Smith 2007; Li et al. 2009). Bibliometric analyses collect information from international databases, such as the one made available by the Institute for Scientific Information-ISI (now known as Thomson Reuters), which evaluates papers published in more than 12,000 journals and publishes a yearly index (Journal Citation Reports—JCR). Several studies show that the analysis of published literature may provide critical information about research production and quality. Bibliometrics plays a crucial role in the decision-making process related to science. It is widely used not only to rank applications for academic positions (Franco 2013) but also to evaluate the performance of journals, universities, and countries and is considered as a possible auxiliary tool to allocate research funding (Fernandes et al. 2012; Fu et al. 2013; Glynn et al. 2010; Tuitt et al. 2011; Ugolini et al. 2012). On this premise, and aware of the utility of science evaluation in order to stimulate scientific research, we performed an analysis on the distribution of publications related to asbestos. Articles on this topic published from 1970 to 2011 were collected using PubMed and analyzed for geographic and temporal distribution. An analysis of IF by country was performed for the most recent years (1988–2011). In order to take into account discrepancies among countries by economic wealth and population size, the two indicators of scientific production estimated for each country were corrected for gross domestic product (GDP) and resident population.

Methods Bibliographic search The search was performed on Maj 2013 in the PubMed database (National Library of Medicine, National Institutes of Health, Bethesda, MD, USA—http://www.ncbi.nlm.nih. gov/PubMed) and referred to the period from 1970 to 2011. PubMed was chosen among available databases to allow a comparison with previously published bibliometric analyses in other areas of biomedical research. The keyword “asbestos” in the MeSH field [mesh] was used for the search. Asbestos [mesh] was first introduced in 1970 in the PubMed database. The mesh term “minerals” was used before, but it included several different substances. The generic search “asbestos” [All Fields] AND 1956:1969 [dp] found 293 citations. The search was refined excluding some types of documents that do not represent research publications, as identified in the “publication type” field [pt]. The search strategy was the following: asbestos [mesh] NOT (congresses [pt] OR letter

Environ Sci Pollut Res

[pt] OR editorial [pt] OR news [pt] OR comment [pt] OR lectures [pt] OR addresses [pt] OR bibliography [pt] OR biography [pt] OR dictionary [pt] OR directory [pt] OR festschrift [pt] OR government publications [pt] OR historical article [pt] OR interview [pt] OR legal cases [pt] OR legislation [pt] OR newspaper article [pt] OR overall [pt]) AND 1970:2011 [dp] NOT 2012:2013 [dp]. Specific analyses were conducted in the most recent citations (1988:2011 [dp]), because PubMed includes author’s affiliation only starting from 1988. The years 2012 and following were excluded as database entries for this period would not have been complete at the time of the search. Keywords PubMed indexers assign keywords (called MeSH—Medical Subject Headings—terms), generally 5 to 15, to each paper (National Library of Medicine 2012). All keywords used for indexing selected articles were identified and their frequency calculated using Excel software. To produce a list of the most used terms, keywords with similar meaning were joined, e.g., carcinogens and carcinogens environmental, pulmonary diseases and lung diseases, smoke and smoking, etc.

national GDP (GDP expressed in current hundred billion US dollars) and by the population size (expressed in millions of inhabitants). GDP and population for each year were obtained from the World Databank Group (The World Bank 2013). Database building Data extraction was performed through dedicated “Application Specific Software (ASS)”, developed in Microsoft Visual C# 2010 Express: this allowed ISSN (International Standard Serial Number) based cross-link between PubMed and JCR databases. Microsoft Excel 2010 was used to handle the data set. Intensive usage of the “Filters” tool was pursued, thus allowing an “operator-friendly” analysis of a large amount of data. Cross-check formulas were extensively implemented in order to virtually reduce to zero input and data handled errors.

Results Total number of published items

Countries

The number of publications and the mean IF (mIF) (i.e., .the sum of the IF of each paper to the total number of publications) was calculated for periods of 3 years for each country. The 2011 Journal Citation Reports (JCR, Thomson Reuters) edition was used to attribute the IF of each publication. Because journal’s abbreviation slightly differs in PubMed and in JCR, the International Standard Serial Number (ISSN), which unambiguously identifies a journal, was used. Journals not listed in Journal Citation Reports received the score “zero” as IF.

The query returned 6907 articles which were downloaded from the PubMed database published in the period 1970 to 2011 in 65 different countries (7 of which only on journals without IF). Figure 1 shows the distribution of articles published worldwide on asbestos, increasing from 149 in the biennium 1970– 1971 up to 377 in the biennium 2010–2011. Numbers steeply increased in the 1970s, leveled off in the 1980s, decreased in the 1990s and then, starting in 2002–2003, a new increase of the scientific interest on asbestos resulted in a higher number of papers in the new millennium. The most productive biennium was 1990–1991 with 426 articles. Publication trend of asbestos papers was compared with the publication trend of mesothelioma papers (same search strategy, replacing the MeSH “asbestos” with “mesothelioma”). Literature on mesothelioma shows a slower but more regular growth, with a stronger increase in the last years (150.5 % from 2002–2003 to 2010–2011 versus 26.9 % for asbestos research). Articles were published in 24 different languages. English accounted for 5712 articles (82.7 %). Among the other languages, 253 papers (3.7 %) were published in Italian followed by German (210, 3 %), Russian (192, 2.8 %), French (134, 1.9 %), and Japanese (122, 1.8 %).

Demographic and economic data

Research topics—keyword analysis

To take into account discrepancy among countries the sum of IF of all published papers for each country were divided by the

PubMed indexers used 2384 keywords (MeSH terms) to classify 6907 articles. Out of them, 894 keywords (37.5 %)

Each publication was assigned to a country according to the first author’s affiliation. For many articles the country has been manually identified by consulting various bibliographic sources. Finally, 98.9 % of the articles were geographically classified. Publications from England, Wales, Scotland, and Northern Ireland were assigned to the UK. Data from countries with 12 or more indexed entries during 1988–2011 were reported in more detail (n=28). The remaining countries accounted for a total of 81 articles. Impact factor

Environ Sci Pollut Res Fig. 1 Temporal trend of publications on asbestos and on mesothelioma in 1970–2011. White triangles indicate asbestos literature, black squares indicate mesothelioma literature

were used only once, 474 (19.9 %) twice, and 277 (11.6 %) keywords were used three times. Keywords were arbitrarily assembled in 5 groups using higher-order keywords in the MeSH tree structure, i.e., Chemicals, Diseases, Neoplasms by sites, Public Health, Neoplastic and Genetics Processes. Table 1 shows the top ten terms for each homogeneous groups of keywords (MeSH terms). The most frequently used keywords were from the group of Chemicals, with asbestos obviously ranking first (3794 times), and from the group of Neoplasms by site, with mesothelioma (2742 times) and lung neoplasms (1745 times) at the top. Other commonly used keywords were pleural neoplasms (1527), occupational diseases (1413), lung diseases (1392), asbestosis (1332), and occupational exposure (959). Unexpectedly, smoke was quite often cited (416). Papers number and quality The analysis on papers number, IF, and sociodemographic variables were focused on 4220 publications issued in the period of 1988–2011, as the quality and completeness of more recent data available in the PubMed was not stable enough. Country was assigned to 4172 articles (98.9 %), and 3187 (75.6 %) had an impact factor. In the 28 countries with 12 or more indexed entries, the highest number of papers on asbestos (586) was published in 1991–1993, as shown in Table 2. The number of published articles fell to 413 in 2000–2002 and rose again thereafter, reaching 526 in the last two triennia. A similar numbers of

articles were published on non-impacted or impacted journals in 1988–1990, but this proportion dropped to one in five since mid 1990s. The numbers of papers without IF were particularly high in non-English speaking countries with a strong scientific production in their own language, like Russia, Japan, and China. The US contributed the greatest output, producing 1119 articles with IF, that is more than one in three published papers on asbestos (35.1 %). Other highly productive countries were Italy (415, 13 %), the UK (198, 6.2 %), and Japan (197, 6.2 %). Taken together, European countries accounted for 1348 articles. The mean IF of the top 28 most productive countries was 2.13 on average, with only minor fluctuations in time, and ranged from 0.54 for Poland to 4.53 for Australia. All countries ranking in the first five positions were English mother tongue speakers, except for Finland (namely, they were Australia, the US, the UK, and Canada). From 1988 to 2011, almost all countries with the highest production decreased the number of not impacted papers. The US scientific production was rather stable as regards the number of papers with IF, but the mean IF decreased and so did the number of papers without IF. Italy tripled the number of articles with IF and doubled both the mean IF and the number of other papers, in the same period. On the contrary, Canada showed a constant loss in all indexes. Scandinavian countries confirmed their well-known strength in occupational health, with a high number of publications and higher than average.

Environ Sci Pollut Res Table 1

Keywords [MeSH terms] most frequently assigned by PubMed indexers to papers in the field of asbestos research

Chemicals

Citations Diseases

Citations Neoplasms by sites

Citations Public health

Citations Neoplastic and genetics processes

Citations

Asbestos

3794

Lung diseases

1392

Mesothelioma

2742

1413

369

1332

Lung neoplasms 1745 Pleural 1527 neoplasms Peritoneal 415 neoplasms Adenocarcinoma 133

Asbestos, serpentine Carcinogens/ mutagens Smoke

608

Asbestosis

539

Pleural diseases

785

416

401

Asbestos, amphibole Air pollutants Dust

251

Pulmonary fibrosis Pneumoconiosis

58

185

Respiratory tract diseases Pleural effusion

175

Pneumonia

45

158

Pulmonary atelectasis Silicosis

44

Asbestos, amosite Silicon dioxide Minerals

220

106

100

56

44

Carcinoma, squamous cell Laryngeal neoplasms Carcinoma, small cell Carcinoma, non small cell Stomach neoplasms

Socioeconomic analysis The ratio between IF sum in 1988–2011 to the resident population was calculated and showed Finland (36.5), Australia (10.4), Norway (9.1), Sweden (8.1), and the US (7.1) in the top five positions (Fig. 2). To provide an evaluation of the research quality for each country adjusted by the economic resources available in each country, we calculated the ratio between IF sum and GDP. This index was particularly high for Finland (13.2), Croatia (6.6), Australia (3.8), Canada (3.2), and Sweden (2.8) (ss. 2). Journals Out of the 4172 papers with assigned country published in the period 1988–2011, 985 (23.6 %) were not indexed in the JCR. Most of these articles were from the US (214 articles), Russia (125), Japan (101), Italy (87) and China (66). The indexed papers (3187; 76.4 %) were published in 491 journals, and 23 of them published at least 32 articles (1 %) during the period considered, as reported in Table 3. Most of these were from USA, followed by the UK (4 journals), Italy (2), and other 5 European journals (1 each), while one was from Japan. The large majority of journals were in English, two in Italian, one in French, and one was a Polish journal. The first 119 journals (24.2 %) in the list published 80 % of the articles. A wide range of journals hosts scientific literature on asbestos, including some of the most important journals in the following JCR categories: Public, Environmental and Occupational Health (12 journals), Respiratory System (5),

46

Occupational diseases Occupational exposure Environmental exposure Air pollutants, occupational Environmental monitoring Air pollution indoor Inhalation exposure Environmental pollutants Risk assessment

44

Air pollution

96 63 53

959

Cell trasformation neoplastic DNA

251

314

RNA

143

313

Gene expression

128

132

Reactive oxygen species Tumor necrosis factors Protooncogene proteins Tumor markers biological Transforming growth factors Tumor suppressor proteins

94

106 75 55 37 37

87 76 63 46 46

Toxicology (1), Oncology (2), Biotechnology and Applied Microbiology (1), Multidisciplinary Sciences (1), and Medicine, Legal (1).

Discussion The present study represents the first effort to explore the geographical distribution, temporal trends, and quality of asbestos research. This topic has drawn global research interest, as documented by articles from 65 countries. Most articles came from countries with traditionally high research output, like North America, Europe, and Japan, but also countries like Australia, India, Turkey, China, South Africa, Brasil, South Korea, Russia, and Israel showed an intense research activity in this area. Not surprisingly, Australia, the UK, and Italy, which showed the highest rates of asbestos-related death in the world (Australian Institute of Health and Welfare AIHW 2008; Ugolini et al. 2010), reported accordingly a remarkable scientific productivity on this topic. To confirm the link between resources invested in research and societal interest in asbestos, also countries that have banned asbestos, but have a controlled use of chrysotile such as Canada, Croatia, and Greece (a strategy which may reflect the political and economic influence of the asbestos mining and manufacturing industry) ranked high among the list of most productive countries. The number of indexed publications grew faster in the first period of observation, reaching the maximum in the early

41

34

36

26

23

22

19

27

138 125

15

18

Croatia

Switzerland

Greece

Brazil

South Korea

Denmark

Russia

Hungary

Israel

122

4172 985

Others

Tot

2

8

3

1

4

5

8

6 7

3187

81

3106 2.13

12 0.65 26

13 0.89 22

13 1.06 20

15 0.75 24

17 0.86 23

20 0.60 27

22 1.65 18

22 2.14 14

23 0.66 25

24 1.01 21

27 2.36 13

27 2.72

28 2.82

29 1.63 19

29 1.76 17

42 1.90 16

45 2.54 12

51 0.54 28

52 2.60 11

110 4.53

114 3.81

125 3.76

145 2.69

172 2.66 10

197 2.69

198 4.03

415 2.06 15

1119 4.21

279

1

0

18

4

0

2

0

0

1

1

5

3

6

4

3

2

3

14

8

9

2

17

21

16

28

25

9

77

289

1 0.54

0 0.00

1 0.54

4 1.82

0 0.00

0 0.00

1 0.75

3 1.12

3 0.54

1 0.26

7 2.38

3 3.98

2 1.97

4 0.45

4 2.07

0 0.00

2 0.66

4 0.58

8 1.75

8 3.05

7 2.22

25 4.84

12 2.80

5 2.64

12 2.74

25 4.52

23 1.65

181

2

0

23

3

0

0

1

1

5

0

2

2

0

12

1

0

2

7

5

5

3

7

14

2

24

9

7

44 3

3

0

0

0

0

1

1

1

0

1

0

7

0

1

1

5

1

1

0

0

4

4

405

1 0.54

0 0.00

84

2

1

3 1.38 11

0 0.00

0 0.00

0 0.00

4 1.73

2 1.86

3 1.16

1 0.46

2 3.44

3 3.32

3 1.99

2 1.58

6 2.01

3 3.08

6 1.81

15 0.30

8 4.21

8 4.29

17 3.26

21 2.92

12 2.32

16 3.49

23 2.79 15

32 3.21

37 1.35

0

0

1

2

0

2

1

2

4

2

5

5

7

1

1

0

0

0

1

1

1

0

1

414

1 0.11

3 0.94

74

0

0

2 1.74 12

8 1.99

0 0.00

0 0.00

2 1.89

0 0.00

4 1.81

0 0.00

2 1.50

3 2.30

4 3.32

2 0.99 12

1 0.68

3 0.56

7 2.51

8 0.42

15 2.77

11 3.11

29 3.99

25 4.11

21 3.17

21 2.93

19 3.09

28 6.04

34 1.42

0

0

1

1

0

1

1

2

2

2

5

6

7

0

0

0

0

0

2

1

1

0

0

379

4 0.56

2 2.83

81

1

0

1 1.41 19

2 1.57

3 2.50

1 0.30

0 0.00

0 0.00

0 0.00

2 2.01

3 1.30

4 2.26

6 3.89

3 1.30 10

5 2.81

4 2.47

4 4.22

5 0.57

12 4.16

6 6.26

12 3.61

16 6.57

28 2.92

35 2.02

21 2.13

24 3.71

40 1.25

0

3

1

1

1

2

0

0

2

2

2

1

0

0

0

0

2

1

2

2

0

0

332

1 0.69

3 1.08

78

0

0

3 0.55 13

1 0.35

1 1.77

2 0.28

1 1.75

0 0.00

4 1.28

6 2.86

1 1.14

3 4.32

5 3.85

4 1.19 10

2 1.66

12 3.00

6 8.25

9 0.41

2 2.75

6 4.13

12 3.55

9 3.14

38 2.63

20 3.28

20 2.32

27 4.08

34 2.10 21 0

0

0

0

0

0

1

1

1

0

0

7

0

1

0

2

2

3

0

0

1

2

402

1 0.63

2 1.06

84

0

1

1 2.12 14

0 0.00

4 1.73

8 0.93

3 1.26

7 2.14

1 0.60

10 1.59

4 3.02

6 3.23

3 2.53

3 3.92

5 2.73

6 3.14

13 1.95

4 1.32

3 2.43

24 7.74

7 7.69

4 0.79

14 2.56

23 2.58

18 2.12 13

23 2.54

80 2.27 23

4

1

0

0

0

1

3

2

1

1

4

0

0

0

1

0

1

0

0

6

2

9

6

442

1 0.81

3 1.27

83

0

0

0 0.00 15

0 0.00

1 0.35

6 1.88

4 3.10

5 8.75

0 0.00

2 0.93

2 2.79

3 1.80

2 0.39

6 1.71

1 0.81

10 1.42

5 2.07

3 0.20

4 3.15

19 3.48

18 3.96

12 3.19

9 1.48

19 2.24

32 3.17

21 4.39

87 2.40 10

mIF

443

2 1.43

0 0.00

2 0.62

0 0.00

8 1.40

3 1.57

7 2.79

5 3.49

8 0.35

2 0.32

6 3.72

2 0.84

3 2.10

5 2.24

5 1.38

4 1.85

2 0.47

3 1.71

0 0.00

28 3.26

12 3.95

13 2.22

11 2.88

33 2.68

52 2.77

18 3.53

80 2.59

129 3.96

mIF NoIF IF

2009–2011

167 3.76 16

mIF NoIF IF

2006–2008

125 3.98 12

mIF NoIF IF

2003–2005

100 3.20 12

mIF NoIF IF

2000–2002

136 5.13 19

mIF NoIF IF

1997–1999

161 4.46 13

mIF NoIF IF

1994–1996

177 3.55 21

mIF NoIF IF

124 5.76

mIF IFrank NoIF IF

1991–1993

Tot total, NoIF articles without Impact Factor, IF articles with Impact Factor, mIF mean Impact Factor

41

4050 944

Tot

6

2

12

2

2

1

4

13

10

14

7

8

66

Spain

95

China

4

the Netherlands

33

South Africa

7

9

36

49

Turkey

34

54

India

33

17

Norway

84

24

7

28

54

32

55

Belgium

69

Poland

153

Canada

Sweden

199

Germany

121

204

France

134

298 101

Japan

Australia

253

the UK

Finland

502

Italy

87

1333 214

the US

NoIF IF

Tot

1988–1990

Numbers of published papers on asbestos and mean impact factor (mIF) by country, from 1988 to 2011

Countries

Total

Table 2

Environ Sci Pollut Res

Environ Sci Pollut Res Fig. 2 Scientific production on asbestos in the most productive countries, standardized by population (Pop) and economic parameters (GDP) from 1988 to 2011. White bars indicate media sIF/GDP, black bars indicate media sIF/POP

nineties, decreased for the next decade and grew again thereafter. It appears that asbestos research has reached a bottleneck or found some kind of limiting factor in the years when asbestos began to be banned on a global scale. The novel increase in the last decade may be linked to a renewed interest for genetic or translational studies. Asbestos raised scientific interest at a local level, as demonstrated by the number of papers published in not impacted journals and in the native language. The most striking cases are Russia, that published 13 impacted articles versus 125

(91 %) papers on journals without IF, similarly to China (66 papers in English versus the 147 (69 %) in Chinese). The journal that published most papers on asbestos was the American Journal of Industrial Medicine, followed by La Medicina del Lavoro, in Italian. Another Italian journal (Epidemiologia e Prevenzione) is included in the list, together with Medycyna Pracy, published in Poland (in Polish). The two first journals have an interesting story that may partly explain why they have published the lion’s share of asbestos-related articles. The American Journal of Industrial

Environ Sci Pollut Res Table 3

List of 23 journals with impact factor, publishing at least 32 articles on asbestos from 1988 to 2011

Journals

No. of articles

% of articles

Impact factor

Journal country

Language

American Journal of Industrial Medicine La Medicina del Lavoro Occupational and Environmental Medicine Environmental Health Perspectives The Annals of Occupational Hygiene Annals of the New York Academy of Sciences American Journal of Respiratory Cell and Molecular Biology International Journal of Occupational and Environmental Health Cancer Research Industrial Health Inhalation Toxicology Regulatory Toxicology and Pharmacology: RTP Chest Environmental Research Epidemiologia e Prevenzione Scandinavian Journal of Work, Environment and Health International Archives of Occupational and Environmental Health

212 119 116 115 111 71 63 55 53 51 50 49 48 48 47 46 41

6.7 3.7 3.6 3.6 3.5 2.2 2.0 1.7 1.7 1.6 1.6 1.5 1.5 1.5 1.5 1.4 1.3

% % % % % % % % % % % % % % % % %

1.625 0.321 3.02 7.036 1.949 3.155 5.125 1.035 7856 0.94 1.919 2.427 5.25 3.398 0.651 3.122 1.889

USA Italy England USA England USA USA USA USA Japan USA USA USA USA Italy Finland Germany

English Italian English English English English English English English English English English English English Italian English English

Carcinogenesis Medycyna Pracy Mutation Research The European Respiratory Journal Revue des Maladies Respiratoires American Journal of Respiratory and Critical Care Medicine

41 40 40 37 33 32

1.3 1.3 1.3 1.2 1.0 1.0

% % % % % %

5.702 0.303 3.035 5.895 0.587 11.08

England Poland Netherlands England France USA

English Polish English English French English

Medicine (AJIM), founded in 1980, published pivotal articles in occupational medicine. Irving J. Selikoff, editor-in-Chief of the journal since 1980, was the clinician and researcher who in the 1960s established the link between the inhalation of asbestos particles and lung-related diseases. His work is largely responsible for the regulation of asbestos today. The Italian La Medicina del Lavoro was issued in December 1901 and is the oldest journal of occupational health in the world still publishing. His founder was Luigi Devoto, a Professor at the Medical School of Pavia who was the first to offer a university course on occupational diseases (Smith 2009; Smith and Beh 2011; Riva et al. 2012). Generally speaking, however, the number of articles without IF, after a steep decline in the period 1991–1996, remained almost steady later on, showing an internationalization of research in the following years. Most articles were published in journals of the JCR Category Public, Environmental and Occupational Health, although a wide variety of journals published on asbestos. Analysis of indexed articles published between 1988 and 2011 clearly identified that the two world leader were the European countries and the US, which, taken together, published nearly four-fifths (77.4 %) of journal articles. Although European countries published about 20 % more asbestos-

related articles than the US (1348 versus 1119), the latter reached a higher mean IF (4.214 versus 2.086), preceded only by Australia (4.531). A similar pattern has been shown in other fields of research, e.g., malignant mesothelioma (Ugolini et al. 2010). Although the field of occupational health is often hampered by the relatively short citation-counting period used for calculating journals IF (Smith 2007), papers on asbestos showed a good citation performance. Actually, in comparison with other bibliometric analyses carried out with the same methodology, the mean IF in asbestos research (2.1) is higher than in some other fields (mesothelioma research 1.7—ophthalmology 1.15—otolaryngology 0.9), but lower than in others (oncology 3.3—molecular epidemiology 2.4—cancer rehabilitation 2.2) (Ugolini et al. 2010; Ugolini et al. 2001; Cimmino et al. 2005; Ugolini and Mela 2003; Ugolini et al. 2007; Ugolini et al. 2012). A characteristic feature of asbestos research, rather uncommon in the field of occupational medicine (Gehanno et al. 2007, Smith et al. 2008), is a relatively high number of citation classics (i.e., papers with more than 100 citations). Some of them received even more than 500 citations, such as Mossman et al. (1990), published on Science, or Peto et al. (1999), published on the British Journal of Cancer. This may be due

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to the great interest of the scientific community for papers that have brought new insights concerning the toxic effects of asbestos and, in addition, to the intrinsic strength of journals where this highly cited papers have been published. When national scientific production (sum of IF) was compared within the 28 most productive countries according to socioeconomic variables, Australia and some European small countries (Scandinavian countries and Croatia) performed very well. Bibliometric studies often show that small developed countries are particularly efficient: possible explanations include destination to research of a higher proportion of GDP and a better use of available resources, besides the well-known Scandinavian attention to occupational and environmental health issues. On the other hand, all the main asbestos producers (Russia, China, Kazakhstan, Brazil, Zimbabwe, and Colombia) with the exception of Canada gave a limited contribution to research on asbestos, as recorded in the PubMed database. Big asbestos producers seem not to be interested in asbestos research and fund allocation of in this field: this may shed a light on their political choices. This is not true for Canada, where research may find support from several sources, including non-government agencies and private foundations that may be less affected by a protective attitude of governments toward best home business. Furthermore, the much extensive exposure of scientists in Canada to international exchanges may have played a role. The analysis of keywords may provide useful hints about research trends and may help to monitor the development of science with the final scope of interpreting new perspectives in the field (Su and Lee 2010). Our analysis of keywords revealed a high fragmentation in the use of terms, a problem which affects many biomedical disciplines (Cimmino et al. 2005; Falagas et al. 2005; Mela and Cimmino 1998; Rahman et al. 2005; Ugolini et al. 2001; Ugolini et al. 2007). Indeed, the most commonly used keywords reflected very closely asbestos-related diseases and confirmed that the research mainly concerns the occupational and environmental exposure area. Biochemical studies seemed to increase in the new millennium, when studies on biomarkers and on asbestosassociated diseases (including the role of genetic susceptibility, the possible interaction of asbestos with other causative agents and new therapeutic strategies) have probably fuelled again the interest of scientists. Worldwide, about 60 countries have banned the use of asbestos, totally or in part, and this will lead to a decline in asbestos-associated diseases in the future. However, so far, there is still a great lack of basic knowledge on asbestos, e.g., its toxic effects and carcinogenic mechanisms have not been fully understood, and studies on biomarkers for prevention and monitoring are also needed. The effects of asbestos exposure will remain for decades and therefore more research is necessary, especially considering that most of the world population still live in countries where asbestos and asbestos-

containing products are still used. Research projects generate important knowledge that may boost decision making. Political action also derives from research pressure. Eighty-five percent of the world production of asbestos is used today to manufacture products in Asia and Eastern Europe, the rest being mainly utilized in Latin America and Africa. In 2012, 2 million tons of asbestos were mined worldwide. Russian Federation was the largest producer with about 50 % world share followed by China, Brazil, Kazakhstan, and Canada. China is by far the largest consumer of asbestos in the world today, followed by India, Russia, Kazakhstan, Brazil, Indonesia, Thailand, Uzbekistan, and Ukraine. Nonoccupational exposure to asbestos from construction materials is also a serious international problem often neglected. In western countries, large amounts of asbestos are still present in thousand of buildings (schools, homes, hospitals, commercial, or industrial buildings), while in developing countries, many people continue to be asbestos-contaminated by the use of this fiber in construction. Regarding asbestos associated diseases, lung diseases were predominant among non-neoplastic diseases, whereas among neoplastic diseases, the greatest number of studies concerned the pleura. This dichotomy is explained in part by the greater focus of researchers on malignant mesothelioma of the pleura, given the direct link to asbestos exposure, and to a general underestimation of lung cancer risk associated to asbestos exposure. The study has a number of limitations. The bibliometric evaluation may be limited by the use of PubMed as the only data source. Although PubMed is among the largest global biomedical databases, some publications cannot be retrieved and other international databases such as Web of Sciences or Scopus could have been used. However, PubMed allows for a comparison with other bibliometric analyses published in diverse fields. Finally, a bibliometric study has different needs compared to a systematic review that relies instead upon extensive literature searching using multiple databases to ensure that all relevant studies are retrieved (Wright et al. 2014). Even if an underreporting is possible, it can be hypothesized that the research trends pointed out in the present study express a reliable estimate of ongoing research in the field. The first author’s address has been used to attribute a nationality to each paper. The methodology may have not adequately reflected international cooperation. However, we were dealing with large numbers, and an internationally authored work usually entails a rotation of referent/ corresponding writers (Ugolini et al. 2002). Our aim was to offer a reasonable review of the publication trends in a specific field, recognizing and comparing the contribution of each country. This analysis employed the IF as a proxy measure of research quality. The IF is calculated by dividing the number of current year citations to the source items published in that

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journal during the previous two. Although widely used, as a quantitative tool for ranking, evaluating, categorizing, and comparing journals, the IF is the object of debate within research evaluators, funding agencies, and the scientific community, due to its intrinsic inaccuracy. The IF represents a mean score of the journal, not the value of each article, and may vary as scientific priorities change. Ideally, an exhaustive survey should take account of more than one bibliometric indicator, e.g., number of cites, 5-year impact factor, immediacy index, cited half-life, Eigenfactor. IF 2011 edition was applied in the current analysis, irrespective of the actual publication year of each article. Possible misinterpretation of results may arise from this choice; however, it is reasonable to assume that if an under/overestimation of national impact factor may have occurred, the same bias affected all the considered countries, assuring validity to the country comparison. Finally, the PubMed database is biased in favor of journals published in English; therefore, English speaking countries such as the US, Canada, and the UK have an advantage when compared to countries traditionally publishing in other languages, e.g., China, Japan, and Russia. English is the international language of communication in academic fields, and high-quality articles and journals are mainly published in English; however, as much as 1198 (17.3 %) articles related to asbestos were published in non-English languages since 1970, according to the PubMed database, as previously discussed. This is the first comprehensive bibliometric analysis of scientific activities in the field of asbestos research. The use of results from bibliometric studies to extrapolate general concepts such as scientific progress and research performance have been questioned, based on the application of the Matthew effect in environmental sciences (Grandjean et al. 2011). However, a more detailed discussion about this scenario and its sociologic features is out of the scope of this paper and is left to interested readers. Bibliometric studies, in spite of their methodological limitations, are useful tools for assessing the social and scientific relevance of a particular discipline or subject, since they permit analysis of the growth, size, and distribution of scientific literature on the topic of interest. Comparative bibliometric assessment of the research output of different countries is a critical tool to evaluate the interest of a specific topic, provides policy makers and funding agencies a useful measure of national performance, and can help scientists within individual countries to carry out more effective research. In conclusion, interest in asbestos research is growing again in the new millennium, after a slowdown in the nineties. It appears to be higher in the countries were asbestos has been banned, and it remains particularly deep-rooted at a local level.

Acknowledgments This study was supported by grants funded by INAIL, Fondazione Buzzi-Unicem per la Ricerca sul Mesotelioma, University of Genoa, Ministero della Salute, Fondazione Veronesi, and Associazione Italiana per la Ricerca sul Cancro (AIRC) Conflict of interest The authors declare they have no actual or potential competing financial interests.

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