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Neurological Sciences

, Volume 39, Issue 9, pp 1537–1545 | Cite as

The 100 most-cited articles in Parkinson’s disease

  • Jin-hua Xue
  • Zhi-ping Hu
  • Ping Lai
  • De-qing Cai
  • Er-sheng Wen
Original Article

Abstract

Background

Parkinson’s disease (PD), the second most common neurodegenerative disease, has serious clinical effects. Research on PD is increasing, but the quantity and quality of this research have not been reported.

Methods

To analyze the most-cited articles on PD and provide information about developments in this field, we searched for articles in the Web of Science for the keyword “Parkinson*” in the title. We selected the 100 most-cited articles and evaluated information including citation number, publication time, journal, impact factor, authors, original country, institution of corresponding author, and study type.

Results

Citation numbers for the 100 most-cited articles ranged from 669 to 6902, with a median of 944. The 100 articles were published from 1967 to 2009, with most appearing between 1996 and 2000 (n = 24) and 2001 to 2005 (n = 27). The publications appeared in a total of 31 journals, led by Science with 15 and the New England Journal of Medicine (NEJM) with 13. The majority (84%) of the 100 most-cited articles had ≥ 3 authors. The articles originated from 14 countries, led by the USA (n = 44) and England (n = 17). Among the 100 most-cited articles, 24 were clinical studies, 54 were laboratory studies, 20 were reviews, and 2 were clinical guidelines. None of these articles originated from South America, Oceania, or Africa.

Conclusions

The present study provides historical perspectives on the progress of PD research and highlights trends and academic achievements in this field.

Keywords

Most-cited Parkinson’s disease Neurodegenerative diseases 

Introduction

Parkinson’s disease (PD) is the second-most prevalent neurodegenerative disease which characterized by the progressive loss of dopaminergic neurons in the substantia nigra pars compacta [1, 2]. It is a major contributor to worsened medical outcomes, poor quality of life, disability, and nursing home placement [3, 4]. Medical researchers have increasingly explored the mechanisms, early recognition, and prevention of PD. However, the PD research literature has not been analyzed to assess the quality of scientific insights in this area.

Citation analysis is an important method for determining the influence of an article on scientific progress as well as evaluating the impact factor (IF) of a scientific journal [5]. The study of citation analysis may help to identify articles, research topics, and authors of influence.[6]. Attempts have been made to identify the most cited articles in many fields, including neurosurgery,[7], traumatic brain injury [8], orthopedics [9], radiology [10], and surgery [11]. However, no citation analysis of PD has been published. Therefore, we analyzed and characterized the 100 most-cited articles on PD, to obtain an indication of the most impactful advances, developments, and discoveries in this field during the past century.

Methods

In September 2017, we performed a citation search on the bibliometric database ISI Web of Science (Philadelphia, PA, USA) from 1900 to 2017 for articles pertaining to PD. The search used the key term “Parkinson*” in the title (*as a wild card character used in search string). Articles on the list were reviewed by two independent reviewers by reading the abstracts. The full texts were acquired from PubMed, EMBASE, or ScienceDirect when necessary. Only studies focused on PD as the main topic and published in English were included. Articles were excluded if they were not pertinent.

We identified and selected the 100 most-cited articles related to PD, which were then manually reviewed by two independent investigators using the modified approach of the methods by Azer [12] and Lim et al. [13]. We compiled the information on the journal name, citation number, IF, title, number of authors, authorship (first, second, and corresponding authors), publication year, and country of origin of each article. If the authors were from multiple countries, the country of origin was deemed to be that of the corresponding author.

Statistical analysis

Data were described by the median or interquartile range. The Wilcoxon rank sum test and Spearman test were used to evaluate different indicators. All data were analyzed with SPSS V.17 software (SPSS, Chicago, IL, USA). All probability values were two-tailed, and statistical significance was defined as p < 0.05.

Results

Citation count and publication year

A total of 75,913 articles on PD were identified in the Web of Science core database after the initial search in the period from 1900 to present. We selected the 100 most frequently cited articles and ranked them according to the number of citations listed in Table 1. Citation numbers ranged from 669 to 6902, with a median number of 944. Among them, one article was cited more than 5000 times and 44 articles were cited more than 1000 times. The citation index (median 58, range 22–250) was correlated with number of the citations per article (r = 0.690, p = 0.000).
Table 1

The top 100 cited articles on Parkinson’s disease

Rank

Author (first)

Title

Journals

Years

Times cited

Citation index

PMID

1

Hoehn, MM

Parkinsonism-onset progression and mortality

Neurology

1967

6902

138.04

6,067,254

2

Hughes, AJ

Accuracy of clinical-diagnosis of idiopathic Parkinson’s disease—a clinicopathological study of 100 cases

Journal of Neurology Neurosurgery and Psychiatry

1992

4873

194.92

1,564,476

3

Polymeropoulos, MH

Mutation in the alpha-synuclein gene identified in families with Parkinson’s disease

Science

1997

4483

224.15

9,197,268

4

Braak, H

Staging of brain pathology related to sporadic Parkinson’s disease

Neurobiology of Aging

2003

3510

250.71

12,498,954

5

Langston, JW

Chronic parkinsonism in humans due to a product of meperidine-analog synthesis

Science

1983

3283

96.56

6,823,561

6

Kitada, T

Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism

Nature

1998

2870

151.05

9,560,156

7

Kruger, R

Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson’s disease

Nature Genetics

1998

2455

129.21

9,462,735

8

Dauer, W

Parkinson’s disease: mechanisms and models

Neuron

2003

2266

161.86

12,971,891

9

Singleton, AB

Alpha-synuclein locus triplication causes Parkinson’s disease

Science

2003

2234

159.57

14,593,171

10

Betarbet, R

Chronic systemic pesticide exposure reproduces features of Parkinson’s disease

Nature Neuroscience

2000

2012

118.35

11,100,151

11

Burns, RS

A primate model of parkinsonism-selective destruction of dopaminergic-neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine

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

1983

1985

58.38

6,192,438

12

Gibb, WRG

The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease

Journal of Neurology Neurosurgery and Psychiatry

1988

1925

66.38

2,841,426

13

Bernheimer, H

Brain dopamine and syndromes of Parkinson and Huntington clinical, morphological and neurochemical correlations

Journal of The Neurological Sciences

1973

1890

42.95

4,272,516

14

Fearnley, JM

Aging and Parkinson’s disease substantia nigra regional selectivity

Brain

1991

1656

63.69

1,933,245

15

Valente, EM

Hereditary early-onset Parkinson’s disease caused by mutations in PINK1

Science

2004

1591

122.38

15,087,508

16

Gelb, DJ

Diagnostic criteria for Parkinson disease

Archives of Neurology

1999

1495

83.06

9,923,759

17

Spillantini, MG

Alpha-synuclein in filamentous inclusions of Lewy bodies from Parkinson’s disease and dementia with Lewy bodies

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

1998

1469

77.32

9,600,990

18

Mcgeer, PL

Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson’s and Alzheimer’s disease brains

Neurology

1988

1458

50.28

3,399,080

19

Bonifati, V

Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism

Science

2003

1431

102.21

12,446,870

20

Zarranz, JJ

The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia

Annals of Neurology

2004

1428

109.85

14,755,719

21

Zimprich, A

Mutations in LRRK2 cause autosomal-dominant Parkinsonism with pleomorphic pathology

Neuron

2004

1409

108.38

15,541,309

22

Freed, CR

Transplantation of embryonic dopamine neurons for severe Parkinson’s disease

New England Journal of Medicine

2001

1407

87.94

11,236,774

23

Shimura, H

Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase

Nature Genetics

2000

1307

76.88

10,888,878

24

Kish, SJ

Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson’s disease-pathophysiologic and clinical implications

New England Journal of Medicine

1988

1270

43.79

3,352,672

25

Feany, MB

A Drosophila model of Parkinson’s disease

Nature

2000

1256

73.88

10,746,727

26

Paisan-Ruiz, C

Cloning of the gene containing mutations that cause PARK8-linked Parkinson’s disease

Neuron

2004

1248

96

15,541,308

27

Lang, AE

Parkinson’s disease—first of two parts

New England Journal of Medicine

1998

1248

65.68

9,761,807

28

Schapira, AHV

Mitochondrial complex I deficiency in Parkinson’s disease

Journal of Neurochemistry

1990

1244

46.07

2,154,550

29

Bergman, H

Reversal of experimental parkinsonism by lesions of the subthalamic nucleus

Science

1990

1237

45.81

2,402,638

30

Jankovic, J

Parkinson’s disease: clinical features and diagnosis

Journal of Neurology Neurosurgery and Psychiatry

2008

1210

134.44

18,344,392

31

Krack, P

Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease

New England Journal of Medicine

2003

1151

82.21

14,614,167

32

Limousin, P

Electrical stimulation of the subthalamic nucleus in advanced Parkinson’s disease

New England Journal of Medicine

1998

1137

59.84

9,770,557

33

de Lau, LML

Epidemiology of Parkinson’s disease

Lancet Neurology

2006

1125

102.27

16,713,924

34

Cotzias, GC

Aromatic amino acids and modification of parkinsonism

New England Journal of Medicine

1967

1106

22.12

5,334,614

35

Javitch, JA

Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-uptake of the metabolite N-methyl-4-phenylpyridine by dopamine neurons explains selective toxicity

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

1985

1102

34.44

3,872,460

36

Leroy, E

The ubiquitin pathway in Parkinson’s disease

Nature

1998

1087

57.21

9,774,100

37

Cotzias, GC

Modification of parkinsonism-chronic treatment with l-dopa

New England Journal of Medicine

1969

1060

22.08

4,178,641

38

Dawson, TM

Molecular pathways of neurodegeneration in Parkinson’s disease

Science

2003

1057

75.5

14,593,166

39

Braak, H

Stages in the development of Parkinson’s disease-related pathology

Cell and Tissue Research

2004

1056

81.23

15,338,272

40

Kim, JH

Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson’s disease

Nature

2002

1055

70.33

12,077,607

41

Davis, GC

Chronic parkinsonism secondary to intravenous-injection of meperidine analogs

Psychiatry Research

1979

1047

27.55

298,352

42

Dexter, DT

Basal lipid-peroxidation in substantia nigra is increased in Parkinson’s disease

Journal of Neurochemistry

1989

1038

37.07

2,911,023

43

Deuschl, G

A randomized trial of deep-brain stimulation for Parkinson’s disease

New England Journal of Medicine

2006

1032

93.82

16,943,402

44

Riederer, P

Transition-metals, ferritin, glutathione, and ascorbic-acid in parkinsonian brains

Journal of Neurochemistry

1989

1023

36.54

2,911,028

45

Conway, KA

Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson’s disease: implications for pathogenesis and therapy

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

2000

991

58.29

10,639,120

46

Tomlinson, CL

Systematic review of levodopa dose equivalency reporting in Parkinson’s disease

Movement Disorders

2010

983

140.43

21,069,833

47

Chartier-Harlin, MC

Alpha-synuclein locus duplication as a cause of familial Parkinson’s disease

Lancet

2004

964

74.15

15,451,224

48

Rascol, O

A five-year study of the incidence of dyskinesia in patients with early Parkinson’s disease who were treated with ropinirole or levodopa

New England Journal of Medicine

2000

964

56.71

10,816,186

49

Baba, M

Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson’s disease and dementia with Lewy bodies

American Journal of Pathology

1998

961

50.58

9,546,347

50

Emre, M

Clinical diagnostic criteria for dementia associated with Parkinson’s disease

Movement Disorders

2007

959

95.9

17,542,011

51

Conway, KA

Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease

Nature Medicine

1998

929

48.89

9,809,558

52

Carlsson, M

Interactions between glutamatergic and monoaminergic systems within the basal ganglia—implications for schizophrenia and Parkinson’s disease

Trends in Neurosciences

1990

923

34.19

1,695,402

53

Forno, LS

Neuropathology of Parkinson’s disease

Journal of Neuropathology and Experimental Neurology

1996

921

43.86

8,786,384

54

Chaudhuri, KR

Non-motor symptoms of Parkinson’s disease: diagnosis and management

Lancet Neurology

2006

912

82.91

16,488,379

55

Olanow, CW

Etiology and pathogenesis of Parkinson’s disease

Annual Review of Neuroscience

1999

902

50.11

10,202,534

56

Limousin, P

Effect on parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation

Lancet

1995

889

40.41

7,815,888

57

Goetz, CG

Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): Scale Presentation and Clinimetric Testing Results

Movement Disorders

2008

870

96.67

19,025,984

58

Lucking, CB

Association between early-onset Parkinson’s disease and mutations in the parkin gene

New England Journal of Medicine

2000

868

51.06

10,824,074

59

Simon-Sanchez, J

Genome-wide association study reveals genetic risk underlying Parkinson’s disease

Nature Genetics

2009

866

108.25

19,915,575

60

Jenner, P

Oxidative stress in Parkinson’s disease

Annals of Neurology

2003

864

61.71

12,666,096

61

Bergman, H

The primate subthalamic nucleus. 2. Neuronal-activity in the MPTP model of parkinsonism

Journal of Neurophysiology

1994

859

37.35

7,983,515

62

Kordower, JH

Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson’s disease

Science

2000

856

50.35

11,052,933

63

Lees, AJ

Parkinson’s disease

Lancet

2009

844

105.5

19,524,782

64

Schapira, AHV

Mitochondrial complex I deficiency in Parkinson’s disease

Lancet

1989

840

30

2,566,813

65

Frank, MJ

By carrot or by stick: cognitive reinforcement learning in Parkinsonism

Science

2004

837

64.38

15,528,409

66

Fahn, S

Levodopa and the progression of Parkinson’s disease

New England Journal of Medicine

2004

823

63.31

15,590,952

67

Obeso, JA

Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson’s disease

New England Journal of Medicine

2001

823

51.44

11,575,287

68

Hirsch, E

Melanized dopaminergic-neurons are differentially susceptible to degeneration in Parkinson’s disease

Nature

1988

823

28.38

2,899,295

69

Olanow, CW

A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson’s disease

Annals of Neurology

2003

818

58.43

12,953,276

70

Wu, DC

Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease

Journal of Neuroscience

2002

812

54.13

11,880,505

71

Laitinen, LV

Leksells posteroventral pallidotomy in the treatment of Parkinson’s disease

Journal of Neurosurgery

1992

806

32.24

1,727,169

72

Lindvall, O

Grafts of fetal dopamine neurons survive and improve motor function in Parkinson’s disease

Science

1990

805

29.81

2,105,529

73

Parker, WD

Abnormalities of the electron-transport chain in idiopathic Parkinson’s disease

Annals of Neurology

1989

800

28.57

2,557,792

74

Auluck, PK

Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson’s disease

Science

2002

787

52.47

11,823,645

75

Bjorklund, LM

Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model

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

2002

781

52.07

11,782,534

76

Gill, SS

Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease

Nature Medicine

2003

778

55.57

12,669,033

77

Cummings, JL

Depression and Parkinson’s disease—a review

American Journal of Psychiatry

1992

756

30.24

1,372,794

78

Shimura, H

Ubiquitination of a new form of alpha-synuclein by parkin from human brain: Implications for Parkinson’s disease

Science

2001

753

47.06

11,431,533

79

Dexter, DT

Increased nigral iron content and alterations in other metal-ions occurring in brain in Parkinson’s disease

Journal of Neurochemistry

1989

747

26.68

2,723,638

80

Liberatore, GT

Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease

Nature Medicine

1999

733

40.72

10,581,083

81

Markey, SP

Intraneuronal generation of a pyridinium metabolite may cause drug-induced parkinsonism

Nature

1984

731

22.15

6,332,988

82

Wernig, M

Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson’s disease

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

2008

725

80.56

18,391,196

83

Hughes, AJ

What features improve the accuracy of clinical-diagnosis in Parkinson’s disease—a clinicopathological study

Neurology

1992

723

28.92

1,603,339

84

Taylor, AE

Frontal-lobe dysfunction in Parkinson’s disease—the cortical focus of neostriatal outflow

Brain

1986

718

23.16

3,779,372

85

Lang, AE

Parkinson’s disease—second of two parts

New England Journal of Medicine

1998

717

37.74

9,770,561

86

Fahn, S

The oxidant stress hypothesis in Parkinson’s disease-evidence supporting it

Annals of Neurology

1992

716

28.64

1,471,873

87

Gash, DM

Functional recovery in parkinsonian monkeys treated with GDNF

Nature

1996

709

33.76

8,637,574

88

Moore, DJ

Molecular pathophysiology of Parkinson’s disease

Annual Review of Neuroscience

2005

697

58.08

16,022,590

89

Sian, J

Alterations in glutathione levels in Parkinson’s disease and other neurodegenerative disorders affecting basal ganglia

Annals of Neurology

1994

692

30.09

8,080,242

90

Jahanshahi, M

Self-initiated versus externally triggered movements. 1. An investigation using measurement of regional cerebral blood-flow with PET and movement-related potentials in normal and Parkinson’s disease subjects

Brain

1995

690

31.36

7,655,888

91

Cooper, AA

alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson’s models

Science

2006

688

62.55

16,794,039

92

Aarsland, D

Prevalence and characteristics of dementia in Parkinson disease—an 8-year prospective study

Archives of Neurology

2003

688

49.14

12,633,150

93

Yoritaka, A

Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease

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

1996

688

32.76

8,610,103

94

Anglade, P

Apoptosis and autophagy in nigral neurons of patients with Parkinson’s disease

Histology and Histopathology

1997

685

34.25

9,046,040

95

Gradinaru, V

Optical deconstruction of parkinsonian neural circuitry

Science

2009

681

85.13

19,299,587

96

Hirsch, EC

Neuroinflammation in Parkinson’s disease: a target for neuroprotection?

Lancet Neurology

2009

676

84.5

19,296,921

97

Bender, A

High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease

Nature Genetics

2006

675

61.36

16,604,074

98

Li, JY

Lewy bodies in grafted neurons in subjects with Parkinson’s disease suggest host-to-graft disease propagation

Nature Medicine

2008

672

74.67

18,391,963

99

Spencer, PS

Guam amyotrophic-lateral-sclerosis parkinsonism dementia linked to a plant excitant neurotoxin

Science

1987

670

22.33

3,603,037

100

Blum, D

Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson’s disease

Progress in Neurobiology

2001

669

41.81

11,403,877

The 100 most-cited articles were published between 1967 and 2010, and 51% of these papers were published between 1996 and 2005. Three articles were published before 1970 and none of the articles was produced after 2010. The most productive period was 2001 to 2005, during which 27 articles were published. However, when calculating the mean citation number for each article, those published in 1966 to 1970 had the largest citation number (n = 3023) (Fig. 1). The single year with the most cited articles was 2003 (n = 10). The number of citations was highest for the period 2001 to 2005 (31,937). The Spearman test indicated an uptrend between the citation index and time (r = 0.649, p < 0.001). There is low correlation between time and number of citations (r = − 0.299, p = 0.03), but there was a positive correlation between time and citation index (r = 0.375, p < 0.001).
Fig. 1

Numbers and number of citations of top 100 cited articles in 5-year periods

Journals publishing the top 100 articles

The 100 most-cited articles on PD were published in 31 different journals. All the journals with more than one article are listed in Supplemental Material 1; these were predominantly comprehensive medical publications, led by the Science with 15 articles, followed by the New England Journal of Medicine (NEJM) with 13. In addition, Nature, Proceedings of the National Academy of Sciences of the United States of America, and the Annals of Neurology contributed seven, seven, and six of the most cited articles, respectively. The IFs of the 100 most-cited articles ranged from 4.083 to 72.406. Half of the top 100 articles (50 articles) were published in the high-IF journals (IF > 20). The journal IF was significantly correlated with the number of top 100 articles (r = 0.645, p = 0.005) and a low correlation with the number of citations (r = 0.455, p = 0.067).

Authorship, origins and institutions

A majority (84%) of the top 100 articles were produced by 3 or more authors. A list of the most frequently appearing authors is presented in Supplemental Material 2. With regard to individual contributions, A.J. Lees was the most frequently cited author, with listings on 8 of the top 100 articles (as first author, 1; as corresponding author, 3) and a total of 12,132 citations. Dr. Lees was followed by P. Jenner and A.E. Lang, both of whom authored 6 of the top 100 articles, with 5425 and 5340 citations, respectively (Supplemental Material 2). A total of 14 countries contributed to the top 100 articles. As expected, the USA was the most productive country with 44 publications, followed by England (17), France (9), Germany (7), and Canada (5 articles), with all other countries contributing less than 5 publications, as shown in Fig. 2. Articles originating from the USA also had the highest number of citations (total = 57,234). Of the top 100 articles, 8 institutions provided three or more articles. Among them, the leading institutions were University of London with 13 articles, followed by the U.S. National Institutes of Health (NIH) with 6 articles and Harvard University with 5 articles (Supplemental Material 3).
Fig. 2

The top 100 articles were analyzed in terms of their country of origin. a Number of articles from each country. b Number of citations for the articles from each country

Publication type

Among the 100 most-cited articles, there were 24 clinical studies, 54 laboratory studies, 20 reviews, and 2 clinical guidelines (Fig. 3). The number of total citations per article ranged from 688 to 6902 (median, 869) for clinical studies and from 670 to 4873 (median, 1007) for laboratory studies. Of the 24 clinical articles, surgical therapies were addressed by 10 articles, medical therapies by 5, clinical function by 4, clinical genetics by 2, case reports by 2 articles, and clinical staging by 1 article. In particular, the surgical studies focused on deep brain stimulation (five studies), cellular transplantation (three studies), pallidotomy (one study), and intraputaminal delivery of glial cell-derived neurotrophic factor (GDNF) (one study). All the reports of medical therapy were published in high-IF journals, four in the NEJM and one in Science. We found that 8 of the 10 surgical research papers were published in high-IF journals: 5 in the NEJM and 1 each in the Lancet, Science, and Nature Medicine. The earliest study included in the top 100 cited articles on medical therapy was published in 1967, while the earliest study on surgical therapy was published in 1990. Furthermore, the studies of medical therapy had higher median citations per article than the surgical studies (median 964 vs. 856). In the laboratory studies, 18 articles used animal models and 15 articles addressed brain pathology, 11 articles focused on identifying genetic mutations, and 10 articles evaluated the cellular and molecular biology of PD. We also found that 52% of the laboratory studies appeared in the NEJM, Lancet, Science, or one of the Nature journals (Nature, Nature Genetics, Nature Medicine, and Nature Neuroscience). Among them, the articles about brain pathology were most frequently cited (n = 22,475), followed by articles addressing genetic mutations (n = 21,200).
Fig. 3

Distributions of research type of the top 100 cited articles on Parkinson’s disease

Discussion

PD is the second most common neurodegenerative disease, affecting approximately 1% of the population over the age of 60 and 4% over 80 [14]. The current study is the first to assess the characteristics of the 100 most-cited articles in the field of PD, and it allowed us to recognize historical patterns and trends in PD research, which has undergone considerable change in recent years. The results may facilitate recognition of important advances and prevalent areas of research interest in PD and may help basic scientists and clinicians design future research. The current study helps to identify classical research and high-impact journals by providing information regarding authors, institutions, and journals.

Citation analysis is a useful bibliometric method, introduced in 1987, that has been widely used in various fields and has proven to be important for both authors and journals. For authors, citation analysis not only helps them to recognize important research progress but also helps add useful perspectives on historical developments in areas of academic interest. For journals, data from citation analyses may attract manuscripts with higher citation potentials. In addition, citation analysis may, to some extent, help researchers produce better work. However, we must recognize that since the citation number for any given paper is strongly influenced by the prominence of the journal of publication, it may not have a great relationship with the scientific merit of the manuscript [15, 16], and at the same time, the citation number could also be affected by factors such as the author’s geographical origin, language, and gender [17, 18]. Although there are some disadvantages with evaluating the quality of the article by its citation rating, it is still the most widely accepted current method to determine the merits of a paper or journal [19]. At present, more and more articles are labeled as “top cited” or “the most cited” in various medical disciplines, but there is a paucity of literature on citations of articles about PD.

PD, the incidence of which gradually increases with age, is a major global health problem that is associated with increased medical costs and thus places a heavy burden on some communities. In recent years, there have been significant changes in strategies for the prevention, diagnosis, and treatment of PD. Therefore, there is an urgent need to find appropriate directions for research as well as to better design future studies. This may be accomplished through analyzing classic articles to better understand the history and development of PD research. The current study is the first to assess the leading article citations in PD research and will contribute to the ability of authors or readers to recognize the quality of the research reports, identify the key discoveries that have been made as a result of past efforts, and illuminate developing trends in scientific research.

It is well established that the number of citations an article garners is affected by the date of publication [20]. The longer the time since the article was published, the greater the chance of being cited. However, unlike the majority of citation analyses which report peaks between 1980 and 1995, in this analysis, the most productive period was 1996 to 2005, which may be partially accounted for by an increase in numbers of articles and improvements in research quality. In order to overcome the impact of the publication time on the likelihood of citation, we also assessed the citation index as a measure of the true impact of an article independent of short-term trends. The results were consistent with an increase of articles and improvements in research quality.

High-IF journals attract submissions from authors because they not only potentially provide prominence for the research results but also help the author get more attention. The IF of a journal is the most important predicator for citations, and most top-cited articles are published in high-IF journals [21, 22]. This study also confirmed that the IF was positively related to the top 100 cited articles and the number of citations. When taking into account the 5-year IF of the journals, 52 articles were published in the high-IF journals (IF > 20), 23 articles were published in journals with IF between 10 and 20, and only 12 articles were published in the low-IF journals (IF < 5). In the clinical realm, most articles on medical and surgical therapies were published in the highest impact general medical journal (the NEJM). And most animal and basic laboratory studies were published in the high-IF science journals Nature and Science. These results further validate the hypothesis that researchers tend to cite papers from a few core journals in their specialty [23]. In addition, the Proceedings of the National Academy of Sciences of the United States of America and the Annals of Neurology were the sources for several articles in this study.

Fourteen countries contributed to the 100 most-cited articles. The USA ranked first, similar to the citation analyses in other specialties [24, 25, 26]. This finding confirms the important influence of the USA in the study of PD worldwide, which can be explained by the large scientific community and enormous financial resources available to it. Among the top 16 institutions, 11 (69%) are in the USA. Moreover, although authors usually prefer to publish in their local journals, authors in American and European countries tended to publish in American journals [27]. However, the leading institution for publications in PD is the University College of London, which published 13 of the 100 most-cited articles with 17,048 total citations. The most frequently cited authors, A.J. Lees and P. Jenner, were both from the University College of London and had 8 and 6 articles that were on the list, respectively, that reported results of laboratory studies. In addition, we found that no authors from Africa, Oceania, or South America contributed to the 100 most-cited works, which may be related to information access, difficulties in research, and language barriers in these areas, indicating a great disparity in scientific publications between the developing and developed regions of the world.

PD was first described in 1817, and although significant efforts have been made during the past several decades, the pathogenesis of PD remains unclear. Therefore, the study of the pathogenesis of PD is still an area of active interest, which is consistent with our findings that most of the top 100 cited articles (54%) in the present study report the results of basic research. The median citation number per basic research article was higher than that of clinical research articles (1007 vs. 869). Among laboratory studies, the most frequent types were descriptive animal models (n = 18), followed by neuropathological studies (n = 15), characterizing genetics (n = 11), and evaluations of cellular and molecular biology (n = 10).

Research directions constantly change with time. In the 1970s, research was mainly focused on motor fluctuations from l-dopa therapy, assessment of secondary PD, and attempts to further characterize PD. In the 1980s, in addition to the side effects of levodopa treatment, studies addressed cognitive dysfunction, surgical transplantation of stem cells, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) models, and the role of oxidative degeneration in the pathogenesis of PD. In the 1990s, attention focused on surgical treatments such as pallidotomy, deep brain stimulation, and stem cell transplantation, as well as the role of gene mutations and synuclein in the pathogenesis of disease. After 2000, the studies tended to focus on the efficacy of deep brain stimulation (DBS), the therapeutic effects of stem cells and neurotrophic factors, and other gene mutations such as leucine-rich repeat kinase 2 (LRRK2), DJ-1 (protein deglycase, also known as Parkinson disease protein 7), and PTEN-induced putative kinase 1 (PINK1) that can also lead to PD.

Limitations

Although we attempted to rule out all possible design flaws, there are still some limitations in the current study. First, we applied a direct and reproducible approach that clearly limits the references to those with “Parkinson’s disease” in the title of the article, which may lead to omission of some publications related to the disease. For instance, papers that referenced “Parkinson’s disease” in the abstract or keywords, but not in the title, were omitted from our study. Second, despite a meticulous search of the Web of Science, citation information can also be obtained from Google Scholar and Scopus, which may show different results [28, 29] and lead to some research reports being missed. Third, this kind of study of IFs favors earlier published articles, often excluding newly published high-quality studies that have not had the opportunity yet to gain sufficient citations. Fourth, the number of citations alone cannot fully quantify the value of the contribution to the field and may miss important, influential but less frequently cited papers. Fifth, the effect of self-citation and citations of irrelevant articles can also increase the overall citation rate, and this possibility was not addressed in the design of our study. Finally, the language of publication was restricted to English, which would also generate bias.

Conclusions

The current citation analysis dealt with most of the influential studies on PD and presented a detailed list that will change dynamically as the field moves forward. Our analysis has collected a number of highly influential articles from a variety of perspectives, including medical and surgical treatment, basic research, clinical research, and characterization and classification of the disease using pathological methods, and highlights the research trends and academic achievements. Our analysis also provides an insight into the frequency of citations on PD and reveals the quality of research, discoveries, and trends steering PD research worldwide.

Notes

Acknowledgements

This work was supported by the Bureau of Education of Jiangxi province (150972, GJJ13686), Health Department of Jiangxi Provincial (20122032). De-qing Cai would like to thank the Health and Family Planning Commission of Jiangxi Province (20175559). We are grateful for the efforts of Yuan-hui Liu, MD, of the Department of Cardiology, Guangdong Cardiovascular Institute, Guangdong General Hospital, Guangzhou 510100, China.

Compliance with ethical standards

Conflict of interest

None declared.

Supplementary material

10072_2018_3450_MOESM1_ESM.docx (33 kb)
ESM 1 Journals with more than one of the top 100 cited articles on Parkinson’s disease (DOCX 32 kb)
10072_2018_3450_MOESM2_ESM.docx (29 kb)
ESM 2 Authors with two or more of the top-100 cited articles on Parkinson’s disease (DOCX 28 kb)
10072_2018_3450_MOESM3_ESM.docx (29 kb)
ESM 3 Institutions with two or more of the top-100 cited articles on Parkinson’s disease (DOCX 29 kb)

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Copyright information

© Springer-Verlag Italia S.r.l., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Physiology, School of Basic Medical SciencesGannan Medical UniversityGanzhouChina
  2. 2.Department of Cardiologythe First Affiliated Hospital of Gannan Medical UniversityGanzhouChina
  3. 3.Department of Library and Information CenterGannan Medical UniversityGanzhouChina

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