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Mapping the history and current situation of research on John Cunningham virus – a bibliometric analysis

BMC Infectious Diseases20099:28

DOI: 10.1186/1471-2334-9-28

Received: 01 July 2008

Accepted: 11 March 2009

Published: 11 March 2009

Abstract

Background

John Cunningham virus (JCV) constitutes a family of polyoma viruses, which plays important roles in the progressive multifocal leukoencephalopathy (PML) and tumorigenesis. However, no bibliometric investigation has been reported to guide the researchers and potential readers.

Methods

Papers were collected from database Sci-expanded and Pubmed until May 22, 2008. The highly-productive authors, institutes and countries, highly-cited authors and journals were ranked. The highly-cited articles were subjected to co-citation and chronological analysis with highly-frequent MeSH words for co-occurrence analysis.

Results

Until now, 1785 articles about JCV were indexed in Sci-expanded and 1506 in Pubmed. The main document type was original article. USA, Japan and Italy were the largest three producers about JCV. Temple University published 128 papers and ranked the top, followed by University of Tokyo. Khalili K and Yogo Y became the core authors due to more than 20 documents produced. Journal of Neurovirology published more than 15 papers and ranked the top. Padgett BL and Berger JR were the first two highly-cited authors. Journal of Virology and Journal of Neurovirology respectively ranked to the first two highly-cited journals. These top highly-cited articles were divided into 5 aspects: (1) The correlation between JC virus and tumors; (2) Causal correlation of JCV with PML; (3) Polyoma virus infection and its related diseases in renal-allograft recipients; (4) Detection of JCV antibody, oncogene and its encoding protein; (5) Genetics and molecular biology of JCV. The MeSH/subheadings were classified into five groups: (1) JCV and virus infectious diseases; (2) JCV pathogenicity and pathological appearance of PML; (3) JCV isolation and detection; (4) Immunology of JCV and PML; (5) JCV genetics and tumors.

Conclusion

JCV investigation mainly focused on its isolation and detection, as well as its correlation with PML and tumors. Establishment of transgenic animal model using JCV T antigen would be a hopeful and useful project in the further study.

Background

John Cunningham virus (JCV) constitutes a family of polyoma viruses, which contain small, circular and double-stranded DNA genomes. The early region is alternatively spliced to produce large T antigen and small t antigen [1]. T antigen, a large nuclear phosphoprotein for viral DNA replication, binds to viral replication region to promote the unwinding of double helix and recruitment of cell proteins that are required for DNA synthesis. The late region encodes the capsid structural protein VP1, VP2 and VP3 due to alternative splicing and the small regulatory protein known as agnoprotein [1, 2]. VP proteins are essential to assemble with viral DNA to form virons. Serological studies have indicated an asymptomatic JCV infection in about 90% of the adult population, but it may be activated under immunosuppressive conditions, leading to the lethal demyelinating disease, progressive multifocal leukoencephalopathy (PML) [15]. Evidences from transgenic and infectious animal models indicated that JCV could transform cells and cause various malignancies [69]. In recent years, links have been suggested between JCV and various types of human cancers, including colorectal, prostate and esophageal cancers, brain tumors, bronchopulmonary carcinoma and B cell lymphoma [19], pointing out its roles as oncovirus. However, no bibliometric investigation has been reported to guide the researchers and potential readers.

Investigators in some fields commonly predict that decision making for the following experiments, clinical practice and paper's submission should be based on the findings of scientific studies published in journals. Although scientific papers have provided useful and helpful information to the readers, it is a little difficult to learn about the history, status and future trend of some study field. The bibliometric method employs empiric data and quantitative analysis to trace the core production or citation, the content or quality of publications, and motivations of the researchers in the form of published literature so that it proves to be a valid and reliable way to map external and internal features of a scientific field [10]. A key assumption underpinning this method to catch insight into the flow of knowledge is that investigation papers represent knowledge produced by scientific research. Generally, academic productivity of individuals or groups is measured by counting the number of publications. The number of times that one work is cited is viewed as a measure of research impact. That is, the more frequently a paper is cited, the higher its impact or quality [10, 11]. Examination of bibliometric information shows the communication patterns of the investigation within the field and the patterns of influence among different work. Authors who publish earlier and experience frequent citations tend to accrue the number of citations over time as Matthew effect describes. For example, co-citation analysis (in which two papers are cited together in a paper) can indicate a strong conceptual relationship between the studies. On the other hand, PubMed indexes journal articles using MeSH terms, which constitute a thesaurus that embodies all the concepts appearing in the medical literature and are arranged in a hierarchical, tree-like structure by subject categories. Associated with MeSH is a list of corresponding subheadings to enhance the focus of MeSH searches. The combination of MeSH terms and subheadings can not only facilitate the sensitivity and specificity of search, but also indicate the research contents and the relationship between papers [1214]. If the further co-occurrence cluster analysis of MeSH is applied in some field, the close link between subtrees of the field will be well established.

In the present study, production and citation of JCV research have been analyzed using such bibliometric methods as chronological, co-citation and co-occurrence analysis to explore the whole history, current status and frontier about JCV study.

Methods

Data collection

The bibliographic data were collected in the database of the Institute for Scientific Information available on the web (http://www.isiknowledge.com, Sci-expanded) and National Library of Medicine on the web (http://www.ncbi.nlm.nih.gov/sites/entrez, Pubmed) until May 22, 2008. The tile, author, address, source, references or the US list of the papers were downloaded according to the retrieval strategy of "JC virus OR John Cunningham virus OR JCV OR JC polyomavirus OR JC polyoma virus" for Sci-expanded or Pubmed.

Highly-produced and -cited analysis

Using Foxpro 5.0, Microsoft Excel, Bibliographic Item Co-occurrence Mining System (BIOCOMS) provided by Cui Lei and Sci-expanded statistical system, we applied Sci-expanded data to determine the document types, core authors, highly-produced institutes and countries. The references were analyzed to clarify the distribution of highly-cited papers, authors and journals. The top MeSH/subheading words were collected from Pubmed and subjected to statistical analysis for highly-frequent ones.

Cluster analysis

After their identification, the top 34 most-cited articles were subjected to co-citation cluster analysis according to their co-citation times in one paper. The 48 highly-frequent MeSH/subheadings of all articles from Pubmed were studied using co-occurrence cluster analysis in term of their co-existence times in one paper. In any cluster analysis, the matrixes were built up according to co-citation or -occurrence times between the selected articles or words. Then, the related matrixes were developed using Ochiai index as previously described [1518]. Finally, we employed the SPSS 10.0 software to perform the cluster analysis of these related matrixes.

Results

Core countries, institutes, authors and journals

Until May 22, 2008, 1785 articles about JCV were indexed in Sci-expanded with 62508 references and 1506(225 reviews) in Pubmed with 6435 major MeSH/subheading words. The literature about JCV was gradually rising from 3 articles in 1976 until 179 in 2006 as indicated in Figure 1. The average annual growth rate was 5.7 pieces in the period. According to document type, there were 1307 original articles (73.2%), 123 reviews (6.9%) and 209 meeting abstracts (11.7%) in all collected literature (Table 1). In overall 21 countries listed, USA, Japan, Italy and Germany were in order the largest four producers about JCV despite 62 countries included (Table 2). The overall 1245 institutes were mentioned to investigate JCV, among which Temple University of USA published 128 papers and ranked the top, followed by University of Tokyo, and National Institute of Neurological Disorder and Stroke subsequently. Fourteen of 21 (66.7%) core institutes come from USA with three core institutes in Italy (Table 3). Such 33 authors as Khalili K, Yogo Y and etc produced more than 20 documents in spite of all 4856 authors involved. There were 9 highly-produced scientists from Temple University and 6 from University of Tokyo, Japan, and 4 from National Institute of Neurological Disorder and Stroke, USA respectively (Table 4). As shown in Table 5, Journal of Neurovirology, Journal of Virology, Virology, Journal of Medical Virology, Journal of General Virology and so forth published more than 15 papers and were considered as the core journals although there existed JCV papers in 395 journals. These source journals mainly include the field of Virology, Neurosciences, Clinical Neurology, Immunology, Pathology, Oncology and so on (Table 6).
https://static-content.springer.com/image/art%3A10.1186%2F1471-2334-9-28/MediaObjects/12879_2008_Article_793_Fig1_HTML.jpg
Figure 1

Temporal distribution of production about JCV investigation.

Table 1

Document types of the scientific papers about JCV

Num

Document type

Record count

Percentage(%)

1

Original article

1307

73.2

2

Meeting abstract

209

11.7

3

Review

123

6.9

4

Note

63

3.5

5

Letter

40

2.2

6

Editorial material

31

1.7

7

Correction

4

0.20

8

Book review

3

0.17

9

Discussion

2

0.11

Table 2

The territory distribution of the scientific papers about JCV

Num

Country

Record count

Percentage(%)

1

USA

968

54.2

2

Japan

190

10.6

3

Italy

173

9.7

4

Germany

158

8.8

5

UK

88

5.0

6

France

72

4.0

7

Spain

48

2.7

8

Switzerland

44

2.5

9

Canada

37

2.1

10

Sweden

36

2.0

11

Taiwan

24

1.3

12

Norway

22

1.2

13

China

15

0.8

14

Australia

14

0.8

15

Poland

13

0.7

16

Belgium

12

0.7

17

Brazil

12

0.7

18

South Korea

12

0.7

19

Lithuania

11

0.6

20

Finland

10

0.6

21

Netherlands

10

0.6

Table 3

The core institutes to investigate the JCV

Num

Institution name

Country

Record count

Percentage(%)

1

Temple University

USA

128

7.2

2

University of Tokyo

Japan

86

4.8

3

National Institute of Neurological and Communication Disorders and Stroke

USA

79

4.4

4

Harvard University

USA

61

3.4

5

Hokkaido University

Japan

59

3.3

6

National Institute of Neurological Disorder and Stroke

USA

56

3.1

7

Pennsylvania State University

USA

56

3.1

8

Thomas Jefferson University

USA

47

2.6

9

University of Milan

Italy

40

2.2

10

University of Wisconsin

USA

39

2.2

11

Brown University

USA

38

2.1

12

Johns Hopkins University

USA

36

2.0

13

National Cancer Institute

USA

32

1.8

14

University of California san Diego

USA

31

1.7

15

University of Wurzburg

Germany

29

1.6

16

University of Pittsburgh

USA

28

1.6

17

IRCCS

Italy

25

1.4

18

Baylor College of Medicine

USA

24

1.3

19

University of Hamburg

Germany

24

1.3

20

National Institute of Health

USA

23

1.3

21

University of Ferrara

Italy

20

1.1

Table 4

The core authors for JCV investigation

Num

Core author

Institutes

Record count

Percentage(%)

1

Khalili K

Temple University, USA

174

9.8

2

Yogo Y

University of Tokyo, Japan

75

4.2

3

Major EO

National Institute of Neurological Disorders and Stroke, USA

74

4.2

4

Stoner GL

National Institute of Neurological Disorders and Stroke, USA

70

3.9

5

Del Valle L

Temple University, USA

62

3.5

6

Kitamura T

University of Tokyo, Japan

59

3.3

7

Nagashima K

Hokkaido University, Japan

57

3.2

8

Frisque RJ

Pennsylvania State University, USA

48

2.7

9

Ryschkewitsch CF

National Institute of Neurological Disorders and Stroke, USA

45

2.5

10

Koralnik IJ

Harvard Medical School, USA

43

2.4

11

Gordon J

Temple University, USA

42

2.4

12

Sugimoto C

University of Tokyo, Japan

41

2.3

13

Atwood WJ

Brown University, USA

40

2.2

14

Walker DL

University of Wisconsin Medical School, USA

39

2.2

15

Zheng HY

University of Tokyo, Japan

37

2.1

16

Ferrante P

University of Milan, Italy

33

1.9

17

Sawa H

Hokkaido University, Japan

32

1.8

18

Agostini HT

National Institute of Neurological Disorders and Stroke, USA

28

1.6

19

Boland CR

Baylor University Medical Center, USA

27

1.5

20

Takasaka T

University of Tokyo, Japan

26

1.5

21

White MK

Temple University, USA

26

1.5

22

Croul S

Temple University, USA

25

1.4

23

Safak M

Temple University, USA

25

1.4

24

Wegner M

Universität Hamburg, Germany

25

1.4

25

Amini S

Temple University, USA

24

1.3

26

Padgett BL

University of Wisconsin Medical School, USA

23

1.3

27

Reiss K

Temple University, USA

22

1.2

28

Tanaka S

Hokkaido University, Japan

22

1.2

29

Berger JR

Temple University, USA

21

1.2

30

Butel JS

Baylor University Medical Center, USA

21

1.2

31

Dorries K

Universität Würzburg, Germany

21

1.2

32

Shah KV

Johns Hopkins Bloomberg School of Public Health, USA

21

1.2

33

Ikegaya H

University of Tokyo, Japan

20

1.1

Table 5

Core journals of JCV investigation

Num

Source title

Record count

Percentage(%)

1

Journal of Neurovirology

167

9.4

2

Journal of Virology

128

7.2

3

Virology

69

3.9

4

Journal of Medical Virology

51

2.9

5

Journal of General Virology

44

2.5

6

Annals of Neurology

36

2.0

7

Journal of Infectious Diseases

35

2.0

8

Journal of Clinical Micrology

31

1.7

9

Journal of Neuropathology and Experimental Neurology

31

1.7

10

AIDS

29

1.6

11

Journal of Biological Chemistry

29

1.6

12

Neurology

29

1.6

13

Oncogene

25

1.4

14

Proceedings of The National Academy of Sciences of The United States of America

25

1.4

15

Journal of Virological Methods

24

1.3

16

Transplantation

23

1.3

17

Gastroenterology

21

1.2

18

Anthropological Science

20

1.1

19

International Journal of Cancer

20

1.1

20

Polyomaviruses and Human Diseases

19

1.1

21

Archives of Virology

17

1.0

22

Clinical Infectious Diseases

16

0.9

23

American Journal of Transplantation

15

0.8

24

New England Journal of Medicine

15

0.8

Table 6

Subject categories for JCV investigation

Num

Subject category

Record count

Percentage (%)

1

Virology

601

33.7

2

Neurosciences

329

18.4

3

Clinical Neurology

238

13.3

4

Immunology

154

8.6

5

Pathology

154

8.6

6

Oncology

144

8.1

7

Biochemistry & Molecular Biology

142

8.0

8

Infectious Diseases

128

7.2

9

Biotechnology & Applied Microbiology

103

5.8

10

Cell Biology

85

4.8

11

Microbiology

80

4.5

12

Transplantation

80

4.5

13

Surgery

73

4.1

14

Genetics & Heredity

61

3.4

15

Medicine, Research & Experimental

60

3.4

16

Medicine, General & Internal

58

3.3

17

Evolutionary Biology

40

2.2

18

Hematology

35

2.0

19

Urology & Nephrology

34

1.9

20

Pediatrics

33

1.9

21

Biochemical Research Methods

32

1.8

22

Gastroenterology & Hepatology

31

1.7

23

Multidisciplinary Sciences

31

1.7

Highly-cited authors, journals and papers

The papers of 10 highly-cited authors (totally 1577 producers) like Padgett BL and Berger JR were cited for more than 400 times, among whom 8 persons come from USA (Table 7). The 10 highly-cited journals (totally 3584 journals) were selected due to more than 1179 citation times, including 3 for Virology and 4 for comprehensive journals (Table 8). Journal of Virology and Journal of Neurovirology respectively ranked to the first two among 404 cited journals (Table 9). The highly-cited papers were chronologically analyzed and grouped into two stages: (1) 1971–1984: discovery and isolation of JCV in PML disease and (2) 1985-present: clarification of JCV genomic DNA sequence and its correlation with diseases (Table 9).
Table 7

The highly-cited authors for JCV papers

Num

Authors

Institute

CT

CP(%)

1

Padgett BL

University of Wisconsin Medical School, USA

958

1.53

2

Berger JR

University of Kentucky, USA

761

2.75

3

Agostini HT

National Institute of Neurological Disorders and Stroke, USA

649

3.79

4

Frisque RJ

Pennsylvania State University, USA

630

4.80

5

Major EO

National Institute of Neurological Disorders and Stroke, USA

604

5.77

6

Walker DL

Tulane University, USA

495

6.56

7

Arthur RR

Johns Hopkins University, USA

430

7.25

8

Dorries K

University of Wurzburg, Germany

419

7.92

9

Yogo Y

University of Tokyo, Japan

415

8.58

10

Shah KV

Johns Hopkins University, USA

400

9.23

CT, cited time; CP, cumulative percentage

Table 8

The highly-cited journals for JCV papers

Num

Journal

CT

CP(%)

1

Journal of Virology

5871

9.43

2

Virology

2498

13.44

3

Proceedings of The National Academy of Sciences of The United States of America

2313

17.16

4

Journal of Infectious Diseases

2230

20.74

5

New England Journal of Medicine

1655

23.40

6

Journal of Neurovirology

1274

25.45

7

Science

1230

27.42

8

Cell

1227

29.39

9

Journal of Clinical Microbiology

1201

31.32

10

Annals of Neurology

1179

33.22

CT, cited time; CP, cumulative percentage

Table 9

The highly-cited articles for the JCV investigation

N

Authors

Year

Title

Source

V

P

CT

CP

1

Padgett BL

1971

Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy.

Lancet

1

1257

366

0.59

2

Frisque RJ

1984

Human polyomavirus JC virus genome.

J Virol

51

458

360

1.16

3

Major EO

1992

Pathogenesis and molecular biology of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain

Clin Microbiol Rev

5

49

285

1.62

4

Padgett BL

1973

Prevalence of antibodies in human sera against JC virus, an isolate from a case of progressive multifocal leukoencephalopathy

J Infect Dis

127

467

219

1.97

5

Chesters PM

1983

Persistence of DNA sequences of BK virus and JC virus in normal human tissues and in diseased tissues.

J Infect Dis

147

676

215

2.31

6

Berger JR

1987

Progressive multifocal leukoencephalopathy associated with human immunodeficiency virus infection. A review of the literature with a report of sixteen cases.

Ann Intern Med

107

78

197

2.63

7

Astrom KE

1958

Progressive multifocal leuko-encephalopathy; a hitherto unrecognized complication of chronic lymphatic leukaemia and Hodgkin's disease

Brain

81

93

179

2.91

8

Yogo Y

1990

Isolation of a possible archetypal JC virus DNA sequence from nonimmunocompromised individuals.

J Virol

64

3139

172

3.19

9

Gardner SD

1971

New human papovavirus (B.K.) isolated from urine after renal transplantation

Lancet

1

1253

165

3.45

10

Tornatore C

1992

Detection of JC virus DNA in peripheral lymphocytes from patients with and without progressive multifocal leukoencephalopathy

Ann Neurol

31

454

146

3.69

11

Kitamura T

1990

High incidence of urinary JC virus excretion in nonimmunosuppressed older patients.

J Infect Dis

161

1128

136

3.90

12

Houff SA

1988

Involvement of JC virus-infected mononuclear cells from the bone marrow and spleen in the pathogenesis of progressive multifocal leukoencephalopathy.

New Engl J Med

318

301

135

4.12

13

Berger JR

1995

Progressive multifocal leukoencephalopathy: the evolution of a disease once considered rare

J Neurovirol

1

5

134

4.33

14

Arthur RR

1989

Detection of BK virus and JC virus in urine and brain tissue by the polymerase chain reaction.

J Clin Microbiol

27

1174

132

4.55

15

Walker DL

1973

Human papovavirus (JC): induction of brain tumors in hamsters

Science

181

674

128

4.75

16

Loeber G

1988

DNA rearrangements in organ-specific variants of polyomavirus JC strain GS

J Virol

62

1730

126

4.95

17

White FA

1992

JC virus DNA is present in many human brain samples from patients without progressive multifocal leukoencephalopathy

J Virol

66

5726

117

5.14

18

Agostini HT

1996

Genotype profile of human polyomavirus JC excreted in urine of immunocompetent individuals.

J Clin Microbiol

34

159

114

5.32

19

Bergsagel DJ

1992

DNA sequences similar to those of simian virus 40 in ependymomas and choroid plexus tumors of childhood

New Engl J Med

326

988

108

5.49

20

Brooks BR

1984

Progressive multifocal leukoencephalopathy

Neurol Clin

2

299

108

5.67

21

Markowitz RB

1993

Incidence of BK virus and JC virus viruria in human immunodeficiency virus-infected and -uninfected subjects.

J Infect Dis

167

13

108

5.84

22

Kenney S

1984

Prospective study of the human polyomaviruses BK and JC and cytomegalovirus in renal transplant recipients.

Science

226

1337

107

6.01

23

London WT

1978

Brain tumors in owl monkeys inoculated with a human polyomavirus (JC virus).

Science

201

1246

106

6.18

24

Coleman DV

1980

A prospective study of human polyomavirus infection in pregnancy

J Infect Dis

142

1

105

6.35

25

Dorries K

1994

Infection of human polyomaviruses JC and BK in peripheral blood leukocytes from immunocompetent individuals.

Virology

198

59

105

6.52

26

Gardner SD

1984

Prospective study of polyomavirus type BK replication and nephropathy in renal-transplant recipients

J Clin Pathol

37

578

104

6.68

27

Flaegstad T

1991

Amplification and sequencing of the control regions of BK and JC virus from human urine by polymerase chain reaction

Virology

180

553

102

6.85

28

Hogan TF

1980

Human polyomavirus infections with JC virus and BK virus in renal transplant patients

Ann Intern Med

92

373

101

7.01

29

Martin JD

1985

Differences in regulatory sequences of naturally occurring JC virus variants

J Virol

53

306

97

7.16

30

Monaco MCG

1996

JC virus infection of hematopoietic progenitor cells, primary B lymphocytes, and tonsillar stromal cells: implications for viral latency.

J Virol

70

7004

96

7.32

31

Richardson EP

1961

Progressive multifocal leukoencephalopathy

New Engl J Med

265

815

95

7.47

32

Randhawa PS

1999

Human polyoma virus-associated interstitial nephritis in the allograft kidney.

Transplantation

67

103

92

7.62

33

Frisque RJ

1992

The molecular biology of JC virus, causative agent of progressive multifocal leukoenchephalpathy

Mol Neurovirology

 

25

92

7.76

34

Padgett BL

1977

JC virus, a human polyomavirus associated with progressive multifocal leukoencephalopathy: additional biological characteristics and antigenic relationships

Infect Immun

15

656

90

7.91

V, volume; P, page; CT, cited times; CP, cumulative percentage

Co-citation analysis of highly-cited articles

In the overall references about JCV, most highly-cited articles were published before 1999 with more than 90 citation times and came from major journals, such as Journal of Infectious Disease, Journal of Virology, Science, New England Journal of Medicine and so forth. As shown in Figure 2, these top highly-cited articles were divided into 5 aspects by co-citation analysis: (1) The correlation between JC virus and tumors; (2) Causal correlation of JCV with PML: pathogenesis and molecular biology; (3) Polyoma virus infection and its related diseases in renal-allograft recipients; (4) Detection of JCV antibody, gene and encoding protein; (5) Genetics and molecular biology of JCV.
https://static-content.springer.com/image/art%3A10.1186%2F1471-2334-9-28/MediaObjects/12879_2008_Article_793_Fig2_HTML.jpg
Figure 2

Co-citation cluster analysis of highly-cited references.

Co-occurrence analysis of highly-frequent MeSH/subheading words

The 48 highly-frequent MeSH/subheading words generally existed for more than 25 times in the papers about JCV (Table 10). Among them, 17 words (35.4%) belonged to the C02 subcategory of MeSH (Viral Disease) and 15 (31.3%) to B04 subcategory (Viruses). These MeSH/subheadings were classified into five groups: (1) JCV and virus infectious diseases; (2) JCV pathogenicity and pathological appearance of PML; (3) JCV isolation and detection; (4) Immunology of JCV and PML; (5) JCV genetics and tumors(Figure 3).
https://static-content.springer.com/image/art%3A10.1186%2F1471-2334-9-28/MediaObjects/12879_2008_Article_793_Fig3_HTML.jpg
Figure 3

Co-occurrence cluster analysis of the highly-frequent MeSH/subheading words.

Table 10

The highly-frequent MeSH/subheading words

Num

MeSH/subheading words

Subcategory number

Times

CP

1

JC Virus/Genetics

B04.280.640.615.400

289

4.49

2

JC Virus/Isolation and Purification

B04.280.640.615.400

216

7.84

3

Leukoencephalopathy, Progressive Multifocal/Virology

C02.182.500.300.500

115

9.63

4

Leukoencephalopathy, Progressive Multifocal/Diagnosis

C02.182.500.300.500

86

10.96

5

JC Virus/Physiology

B04.280.640.615.400

84

12.27

6

JC Virus/Immunology

B04.280.640.615.400

73

13.40

7

Polyomavirus/Genetics

B04.280.640.615

69

14.47

8

Leukoencephalopathy, Progressive Multifocal/Pathology

C02.182.500.300.500

68

15.53

9

BK Virus/Isolation and Purification

B04.280.640.615.100

68

16.58

10

DNA, Viral/Analysis

D13.444.308.568

64

17.57

11

Leukoencephalopathy, Progressive Multifocal/Drug Therapy

C02.182.500.300.500

58

18.48

12

JC Virus/Pathogenicity

B04.280.640.615.400

56

19.34

13

Tumor Virus Infections/Virology

C02.928

54

20.18

14

Polyomavirus Infections/Virology

C02.256.721

51

20.98

15

Leukoencephalopathy, Progressive Multifocal/Etiology

C02.182.500.300.500

50

21.75

16

BK Virus/Genetics

B04.280.640.615.100

50

22.53

17

Leukoencephalopathy, Progressive Multifocal/Microbiology

C02.182.500.300.500

47

23.26

18

Leukoencephalopathy, Progressive Multifocal/Complications

C02.182.500.300.500

45

23.96

19

JC Virus

B04.280.640.615.400

45

24.65

20

Polyomavirus/Isolation and Purification

B04.280.640.615

42

25.31

21

Acquired Immunodeficiency Syndrome/Complications

C02.782.815.616.400.040

39

25.91

22

Polyomaviridae

B04.280.640

38

26.50

23

DNA, Viral/Genetics

D13.444.308.568

37

27.08

24

HIV Infections/Complications

C02.782.815.616.400

36

27.64

25

Gene Expression Regulation, Viral

G05.315.385

35

28.18

26

Polymerase Chain Reaction/Methods

E05.393.620.500

34

28.71

27

Polyomavirus/Immunology

B04.280.640.615

34

29.23

28

Leukoencephalopathy, Progressive Multifocal/Immunology

C02.182.500.300.500

34

29.76

29

Tumor Virus Infections/Diagnosis

C02.928

33

30.27

30

Tumor Virus Infections/Complications

C02.928

33

30.79

31

Brain/Virology

A08.186.211

33

31.30

32

Capsid Proteins

D12.776.964.970.600.550

33

31.81

33

Brain/Pathology

A08.186.211

31

32.29

34

Promoter Regions (Genetics)

G06.184.603.080.689.675

31

32.77

35

Genes, Viral

G14.330.605

30

33.24

36

JC Virus/Metabolism

B04.280.640.615.400

30

33.71

37

Virus Replication

G04.185.515.880.941

29

34.16

38

Polyomavirus Infections/Complications

C02.256.721

28

34.59

39

DNA, Viral/Cerebrospinal Fluid

D13.444.308.568

28

35.03

40

Neuroglia/Virology

A08.637

28

35.46

41

Brain Neoplasms/Virology

C04.588.614.250.195

27

35.88

42

AIDS-Related Opportunistic Infections/Drug Therapy

C01.539.597.050

27

36.30

43

Tumor Virus Infections/Microbiology

C02.928

27

36.72

44

Simian virus 40/Isolation and Purification

B04.280.640.615.700

27

37.14

45

Brain/Microbiology

A08.186.211

25

37.53

46

Kidney Transplantation

E02.870.500

25

37.91

47

Polyomavirus Infections/Diagnosis

C02.256.721

25

38.30

48

BK Virus/Immunology

B04.280.640.615.100

25

38.69

CP, cumulative percentage

Discussion

A systematic view of JCV papers to discern the distinct set of core researchers, institutional affiliations and corresponding countries helps us to gain a deeper understanding of approaches to JCV. As shown in our bibliometric analysis, the document type of JCV was original articles (1307/1785) and many data (209/1785) had been communicated in meeting activities. The review part occupies 6.9% (123/1785). The results indicated that JCV research was very active and interesting many investigators, and some scientists had begun to summary the achievement of JCV. Among 33 core authors, 19 persons come from Temple University, University of Tokyo, and National Institute of Neurological Disorder and Stroke, which ranked the top in the highly-produced institutes. Additionally, 14 (66.7%) core institutes of USA also focused on the investigation of JCV and USA was the first top producer of JCV papers until now. JVC was discovered in 1971 by American Padgett and named after the two initials of a patient with progressive multifocal leukoencephalopathy (PML). It was suggested that the JCV investigation originated from USA, which consequently became the top source information for JCV. It is rational and helpful for the scientists to tack the core authors and institutes to grasp the frontier of this field, open new projects and submit their distinguished work.

The list of top-cited articles about JCV identified the authors, articles and topics that reflected history and development of this specialty. Among highly-cited authors, Padgett is the discoverer for JCV in PML and published the first article in Lancet. The paper has been cited for 366 times and ranks the top in the highly-cited ones. His outstanding was also due to another article in Journal of Infectious disease, which described the detection of the antibody against JCV in PML. Therefore, it is explanatory for Padgett BL to be the most highly cited. These top-cited articles produced valuable information for readers, but also tell us some historical achievement in some field. According to these highly-cited papers, the research about JCV was chronologically separated into beginning and developing stages including discovery and isolation of JCV in PML disease, and clarification of JCV genomic DNA sequence and its relationship with diseases by polymerase chain reaction (PCR) respectively.

Most of highly-cited journals almost come from Virology, Neurology, and comprehensive journals, indicating JCV paper mainly absorbs frontier knowledge from these fields. Oncogene, Journal of Biological Chemistry, and International Journal of Cancer also become the highly-cited journal (data not shown), indicating the attempts of JCV study to combine with Molecular Biology and Oncology. This data also demonstrate the close link of JCV with these specialties. In the overall references of JCV papers, most highly-cited articles were published in Proceeding of National Academy and Science, USA and New England Journal of Medicine, indicating that these famous-brand journals highlight the investigation of JCV and emphasized the scientific achievement of JCV. Therefore, investigators of JCV not only read the journals of Virology, but also emphasized the novel findings of JCV published in other journals with high impact factor.

Methodologically, the cluster techniques include text segmentation, summary extraction, feature selection, term association, cluster generation, topic identification, and information mapping [19]. Clustering algorithms prominently used in co-citation analysis has proved very useful in revealing research streams in some discipline [2023]. Here, we carried out empirical co-citation analysis to map the network of highly-cited papers about JCV. Our data indicated that these top highly-cited articles were grouped into such 4 aspects as the correlation between JC virus and tumors, causal correlation of JCV with PML, polyoma virus infection and its related diseases in renal-allograft recipients, detection of JCV antibody, oncogene and its encoding protein, and genetics and molecular biology of JCV. These findings might not only enrich the knowledge of students and specialists about the development's history of JCV research, but also open new bursts of scientific investigation.

Co-occurrence has been considered as carriers of meaning across different domains in studies of science. Based on this principle, we performed co-occurrence cluster analysis using Pubmed MeSH/subheading words to construct a new tie between two words depending on the co-existing frequencies [24]. Consequently, most of the top highly-frequent MeSH/subheading words are mainly classified into C02 subcategory of MeSH (Viral Disease) and B04 subcategory (Viruses). The analytic data showed that the contents of published papers about JCV included JCV isolation and detection, as well as JCV and virus infectious diseases like PML or tumors. It was suggested that JCV investigation centered on its isolation, its pathogenicity of PML and its genetics at early time. Recently, the causal relationship between JCV and tumors has been emphasized by the scientists. It was demonstrated that JCV investigation like isolation and detection mainly aimed to clarify the molecular mechanism of its relevant diseases including PML and tumors.

As well known, JCV infection experiences two outcomes as other viruses. In un-permissive condition, JCV infection initiates binding to the JCV-sensitive cell surface and JCV capsids undergo endocytosis and are transported to the nucleus where the viral DNA is uncoated and the early and late region begins to be transcripted. Subsequently, JCV genomic DNA is assembled with caspid protein to undergo the lytic viral release, finally to cause demyelinating disease, PML. Under permissive infection, viral DNA can replicate, resulting in lytic infection with viral amplification and non-permissive cells don't allow the viral replication, leading to an abortive infection or cell transformation [69]. The evidence provided enough reasons for the following data: (1) The core and highly-cited journals mainly contained the field of virology, neurology and oncology; (2) The highly-cited articles and highly-frequent MeSH/subheading also mentioned the research contents of JCV, PML and tumors.

Recently, the further clarification of JCV genetics promoted the scientists to detect its genomic existence in tumors or make the transgenic mice to study the oncogenic role of JCV. Our group had examined the JCV targeting T antigen using nested-PCR, real-time PCR, in situ PCR, in situ hybridization, and immunohistochemistry [69]. It was found that positive rate and copies of JCV were higher in gastric, lung and tongue carcinomas than corresponding normal tissues, indicating its oncogenic role in epithelial carcinogenesis. Furthermore, JCV T antigen can serve as helicase, and polymerase, orchestrate the assembly and function of cellular proteins, disrupt the signal pathways of p53, Rb and Wnt signaling pathway, and should be considered as a viral oncogene [24]. Therefore, we are establishing a transgenic model of gastric neoplasia induced by JCV T antigen, which will help to verify the oncogenic role of JCV in gastric carcinoma and provide a novel tool to investigate gastric carcinomas. It was hypothesized that application of JCV T antigen in tumor transgenic animal model would be a novel and hot project in the future.

Conclusion

In this study, we successfully performed the scientometric analysis of JCV literature. Our data indicated that JCV mainly centered on PML and tumors. The bibliometric study assists researchers to know the history and frontier of JCV investigation, guide them to open new projects and submit the distinguished work. These cluster methods employed in this investigation can clarify the history, status and development in the field of JCV.

Declarations

Acknowledgements

This study was supported by Natural Scientific Foundation of China (No.70473101; No. 30600286), Shenyang Outstanding Talent Foundation of China, Liaoning BaiQianWan Talents Program, Grant-in aid for Scientific Research from the Ministry of Education, Culture, Sports and Technology of Japan (20659109) and Smoking Research Foundation.

Authors’ Affiliations

(1)
Department of Biochemistry and Molecular Biology, College of Basic Medicine, China Medical University
(2)
Department of Medical Informatics and Information System, China Medical University
(3)
Department of Diagnostic Pathology, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama

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Copyright

© Zheng et al; licensee BioMed Central Ltd. 2009

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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