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Contemporary Oncology/Współczesna Onkologia
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Original paper

The top 100 cited articles in lung cancer – a bibliometric analysis

Nilay Sengul Samanci
1
,
Emir Celik
1

1.
Department of Medical Oncology, Istanbul University-Cerrahpasa, Cerrahpasa Medical Faculty, Istanbul, Turkey
Contemp Oncol (Pozn) 2019; 24 (1): 17-28
Online publish date: 2020/03/30
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Introduction

Lung cancer is an important health problem with an increasing incidence. In most European countries, lung cancer has increased so dramatically that it may be considered one of the major health problems in the last century [1]. The most common causes of cancer-related death are cancers of the lung and bronchus (24%), prostate (10%) and colorectum (9%) in men, and lung and bronchus (23%), breast (15%), and colorectum (8%) in women [2]. Although lung cancer has long been characterized by late-stage diagnosis and poor survival, encouraging results have been achieved for lung cancer screening in high-risk populations in the last decade and there has been significant progress in systemic treatments for molecular subgroups of patients with advanced disease. Furthermore, within the last ten years, new molecular targets have emerged, next-generation drugs with more specific target effects have been introduced, and targeting specific resistant mutations is expected to advance the treatment of lung cancer by creating a chronic therapeutic pathway [3]. This bibliometric study demonstrates the development of lung cancer treatment over the years.

Bibliometric studies represent an important study type showing the trend topics in a given field. Numerous medical and surgical specialists have published the most cited articles in their specialties in the form of bibliometric analysis such as general surgery [4], anesthesiology [5], orthopedics [6], otolaryngology [7], radiology [8] and plastic surgery [9]. The first bibliometric analysis was penned by Garfield and published in JAMA in 1987 [10]. He also continued with new bibliometric studies in different fields of medical science.

The purpose of our study was to identify and analyze the 100 most cited lung cancer articles published in biomedical literature in the last 44 years. We determined the number of citations with ranking, average citations per year (ACY), citations and publications by year, publishing journal, institution and country of origin, the most common subject of frequently cited articles, authorship status of classical papers and correlation analyses between citation, ACY, Impact Factor (IF) and length of time since publication in years.

Material and methods

Study design

Study type: retrospective clinical study, Level of evidence: 3 or Group B (Scottish Intercollegiate Guidelines Network; SIGN) [11].

Data collection and inclusion criteria: In this paper reporting a bibliometric citation analysis, data were obtained from Thomson Reuters’ WoS Core Collection database (Philadelphia, Pennsylvania, USA) and PubMed (US National Library of Medicine-National Institutes of Health). We accessed the WoS database (accessed: 15.07.2019) using the keyword “lung cancer” between 1975 and 2019. We identified 240,701 articles and conducted an analysis of the top 100 cited articles among these hits shown in Table 1 [12111]. Articles not relevant to lung cancer were excluded from our study and we included original research articles, editorials, correspondences, review articles and case reports. We also utilized the PubMed database to obtain additional data related to the study. Two of the authors (NSS and EC) independently identified T100 with consensus. The difference in time since publication among the top 100 articles may cause a bias as older articles may be more likely to have obtained more citations owing to a longer citable period. The Web of Science, Citation Report feature displays bar charts for the number of items published each year and calculates the average number of citations per year per publication. Due to this bias, we used the ACY for each article.

Table 1

The top 100 cited articles in lung cancer

RankArticleCitationsACY*
1Lynch TJ, Bell D, Sordella R, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of nonsmallcell lung cancer to gefitinib. N Engl J Med 2004; 350: 2129-21397751484.44
2Aaronson NK, Ahmedzai S, Bergman B, et al. The European Organization for Research and Treatment of Cancer QLQC30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst 1993; 85: 365-3767190266.30
3Paez JG, Jänne PA, Lee JC, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004; 304: 1497-15006599412.44
4Mok TS, Wu YL, Thongprasert S, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009; 361: 947-9574907446.09
5Shepherd FA, Rodrigues Pereira J, Ciuleanu T, et al. Erlotinib in previously treated nonsmallcell lung cancer. N Engl J Med 2005; 353: 123-1324163277.53
6Sandler A, Gray R, Perry MC, et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med 2006; 355: 2542-25504076291.14
7Schiller JH, Harrington D, Belani CP, et al. Comparison of four chemotherapy regimens for advanced non-small-cell lung cancer. N Engl J Med 2002; 346: 92-983672204
8Mountain CF. Revisions in the International System for Staging Lung Cancer. Chest 1997; 111: 1710-17173663159.26
9National Lung Screening Trial Research Team, Aberle DR, Adams AM, et al. Reduced lung-cancer mortality with lowdose computed tomographic screening. N Engl J Med 2011; 365: 395-4093539393.22
10Maemondo M, Inoue A, Kobayashi K, et al. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med. 2010; 362: 2380-23883077307.7
11Temel JS, Greer JA, Muzikansky A, et al. Early palliative care for patients with metastatic non-small-cell lung cancer. N Engl J Med 2010; 363: 733-7423042304.2
12Engelman JA, Zejnullahu K, Mitsudomi T, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007; 316: 1039-10433000230.77
13Brahmer J, Reckamp KL, Baas P, et al. Nivolumab versus Docetaxel in Advanced Squamous-Cell Non-Small-Cell Lung Cancer. N Engl J Med 2015; 373: 123-1352966593.2
14Soda M, Choi YL, Enomoto M, et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 2007; 448: 561-5662960227.69
15Kwak EL, Bang YJ, Camidge DR, et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med 2010; 363: 1693-17032910291
16Borghaei H, Paz-Ares L, Horn L, et al. Nivolumab versus Docetaxel in Advanced Nonsquamous Non-Small-Cell Lung Cancer. Engl J Med 2015; 373: 1627-16392907581.40
17Rosell R, Carcereny E, Gervais R, et al. Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial. Lancet Oncol 2012; 13: 239-2462804350.5
18Cole SP, Bhardwaj G, Gerlach JH, et al. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992; 258: 1650-1654278699.50
19Kobayashi S, Boggon TJ, Dayaram T, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 2005; 352: 786-7922549169.93
20Rizvi NA, Hellmann MD, Snyder A, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015; 348: 124-1282501500.2
21Non-small Cell Lung Cancer Collaborative Group. Chemotherapy in non-small cell lung cancer: a meta-analysis using updated data on individual patients from 52 randomised clinical trials. BMJ 1995; 311: 899-909247498.96
22Mitsudomi T, Morita S, Yatabe Y, et al. Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol 2010; 11: 121-128.2447244.7
23Travis WD, Brambilla E, Noguchi M, et al. International association for the study of lung cancer/american thoracic society/european respiratory society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol 2011; 6: 244-2852309256.6
24Fukuoka M, Yano S, Giaccone G, et al. Multi-institutional randomized phase II trial of gefitinib for previously treated patients with advanced non-small-cell lung cancer (The IDEAL 1 Trial). J Clin Oncol 2003; 21: 2237-22462256132.71
25Zhou C, Wu YL, Chen G, et al. Erlotinib versus chemotherapy as firstline treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG0802): a multicentre, open-label, randomised, phase 3 study. Lancet Oncol 2011; 12: 735-7422227247.44
26Yanaihara N, Caplen N, Bowman E, et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006; 9: 189-1982201157.21
27Goldstraw P, Crowley J, Chansky K, et al. The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours. J Thorac Oncol 2007; 2: 706-7142185168.08
28Garon EB, Rizvi NA, Hui R, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med 2015; 372: 2018-20282127425.4
29Scagliotti GV, Parikh P, von Pawel J, et al. Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small-cell lung cancer. J Clin Oncol 2008; 26: 3543-35512108175.67
30Pao W, Miller VA, Politi KA, et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2005; 2: e732073138.2
31Kris MG, Natale RB, Herbst RS, et al. Efficacy of gefitinib, an inhibitor of the epidermal growth factor receptor tyrosine kinase, in symptomatic patients with non-small cell lung cancer: a randomized trial. JAMA 2003; 290: 2149-21581998117.53
32Reck M, Rodríguez-Abreu D, Robinson AG, et al. Pembrolizumab versus Chemotherapy for PD-L1-Positive Non-Small-Cell Lung Cancer. N Engl J Med 2016; 375: 1823-18331970492.5
33Shaw AT, Kim DW, Nakagawa K, et al. Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N Engl J Med 2013; 368: 2385-23941906272.29
34Cancer Genome Atlas Research Network. Comprehensive genomic characterization of squamous cell lung cancers. Nature 2012; 489: 519-5251806225.75
35Hanna N, Shepherd FA, Fossella FV, et al. Randomized phase III trial of pemetrexed versus docetaxel in patients with non-small-cell lung cancer previously treated with chemotherapy. J Clin Oncol 2004; 22: 1589-15971773110.81
36Takamizawa J, Konishi H, Yanagisawa K, et al. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res 2004; 64: 3753-37561729108.06
37Sharma SV, Bell DW, Settleman J, Haber DA. Epidermal growth factor receptor mutations in lung cancer. Nat Rev Cancer 2007; 7: 169-1811722132.46
38Herbst RS, Baas P, Kim DW, et al. Pembrolizumab versus docetaxel for previously treated, PD-L1- positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet 2016; 387: 1540-15501705426.5
39Henschke CI, McCauley DI, Yankelevitz DF, et al. Early Lung Cancer Action Project: overall design and findings from baseline screening. Lancet 1999; 354: 99-105166579.29
40Bhattacharjee A, Richards WG, Staunton J, et al. Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci U S A 2001; 98: 13790-13795164586.58
41Sequist LV, Waltman BA, Dias-Santagata D, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med 2011; 3: 75ra261636181.78
42Thatcher N, Chang A, Parikh P, et al. Gefitinib plus best supportive care in previously treated patients with refractory advanced non-small-cell lung cancer: results from a randomised, placebo-controlled, multicentre study (Iressa Survival Evaluation in Lung Cancer). Lancet 2005; 366: 1527-15371628108.53
43Shigematsu H, Lin L, Takahashi T, et al. Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers. J Natl Cancer Inst 2005; 97: 339-3461607107.13
44Shepherd FA, Dancey J, Ramlau R, et al. Prospective randomized trial of docetaxel versus best supportive care in patients with non-small-cell lung cancer previously treated with platinum-based chemotherapy. J Clin Oncol 2000; 18: 2095-2103155177.55
45Murren JR, Buzaid AC, Hait WN. Critical analysis of neoadjuvant therapy for Stage IIIa non-small cell lung cancer. Am Rev Respir Dis 1991; 143: 889-894.150952.03
46Mountain CF. A new international staging system for lung cancer. Chest 1986; 89: 225S-233S150944.38
47Rosell R, Moran T, Queralt C, et al. Screening for epidermal growth factor receptor mutations in lung cancer. N Engl J Med 2009; 361: 958-967148334.82
48Arriagada R, Bergman B, Dunant A, Le Chevalier T, Pignon JP, Vansteenkiste J; International Adjuvant Lung Cancer Trial Collaborative Group. Cisplatin-based adjuvant chemotherapy in patients with completely resected non-small-cell lung cancer. N Engl J Med 2004; 350: 351-360147191.94
49Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med 2008; 359: 1367-13801451120.92
50Rikova K, Guo A, Zeng Q, et al. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007; 131: 1190-12031436110.46
51Johnson DH, Fehrenbacher L, Novotny WF, et al. Randomized phase II trial comparing bevacizumab plus carboplatin and paclitaxel with carboplatin and paclitaxel alone in previously untreated locally advanced or metastatic non-small-cell lung cancer. J Clin Oncol 2004; 22: 2184-2191142889.25
52Tsao MS, Sakurada A, Cutz JC, et al. Erlotinib in lung cancer - molecular and clinical predictors of outcome. N Engl J Med 2005; 353: 133-144142394.87
53Kim CF, Jackson EL, Woolfenden AE, et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005; 121: 823-835135590.33
54Timmerman R, Paulus R, Galvin J, et al. Stereotactic body radiation therapy for inoperable early stage lung cancer. JAMA 2010; 303: 1070-10761337133.7
55Giaccone G, Herbst RS, Manegold C, et al. Gefitinib in combination with gemcitabine and cisplatin in advanced non-small-cell lung cancer: a phase III trial – INTACT 1. J Clin Oncol 2004; 22: 777-784133383.31
56Herbst RS, Giaccone G, Schiller JH, et al. Gefitinib in combination with paclitaxel and carboplatin in advanced non-small-cell lung cancer: a phase III trial – INTACT 2. J Clin Oncol 2004; 22: 785-794131482.13
57Solomon BJ, Mok T, Kim DW, et al. First-line crizotinib versus chemotherapy in ALK-positive lung cancer. N Engl J Med 2014; 371: 2167-21771301216.83
58Denissenko MF, Pao A, Tang M, Pfeifer GP. Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53. Science 1996; 274: 430-432129453.92
59Olaussen KA, Dunant A, Fouret P, et al. DNA repair by ERCC1 in non-small-cell lung cancer and cisplatinbased adjuvant chemotherapy. N Engl J Med 2006; 355: 983-991129092.14
60Hecht SS. Tobacco smoke carcinogens and lung cancer. J Natl Cancer Inst 1999; 91: 1194-1210128861.33
61Molina JR, Yang P, Cassivi SD, Schild SE, Adjei AA. Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc 2008; 83: 584-5941280106.67
62Cuttitta F, Carney DN, Mulshine J, et al. Bombesin-like peptides can function as autocrine growth factors in human small-cell lung cancer. Nature 1985; 316: 823-826128036.57
63Cappuzzo F, Hirsch FR, Rossi E, et al. Epidermal growth factor receptor gene and protein and gefitinib sensitivity in non-small-cell lung cancer. J Natl Cancer Inst 2005; 97: 643-655127885.2
64Sordella R, Bell DW, Haber DA, Settleman J. Gefitinib-sensitizing EGFR mutations in lung cancer activate antiapoptotic pathways. Science 2004; 305: 1163-1167121375.81
65Winton T, Livingston R, Johnson D, et al. Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N Engl J Med 2005; 352: 2589-2597120280.13
66Takahashi T, Nau MM, Chiba I, et al. p53: a frequent target for genetic abnormalities in lung cancer. Science 1989; 246: 491-494119438.52
67Maheswaran S, Sequist LV, Nagrath S, et al. Detection of mutations in EGFR in circulating lung-cancer cells. N Engl J Med 2008; 359: 366-377115896.5
68Iggo R, Gatter K, Bartek J, Lane D, Harris AL. Increased expression of mutant forms of p53 oncogene in primary lung cancer. Lancet 1990; 335: 675-679115538.5
69Ji P, Diederichs S, Wang W, et al. MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene 2003; 22: 8031-8041114367.24
70Shaw AT, Yeap BY, Mino-Kenudson M, et al. Clinical features and outcome of patients with non-small-cell lung cancer who harbor EML4-ALK. J Clin Oncol 2009; 27: 4247-42531140103.64
71Crawford J, Ozer H, Stoller R, et al. Reduction by granulocyte colony-stimulating factor of fever and neutropenia induced by chemotherapy in patients with small-cell lung cancer. N Engl J Med 1991; 325: 164-170114039.31
72Hayashita Y, Osada H, Tatematsu Y, et al. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005; 65: 9628-9632111274.13
73Herbst RS, Prager D, Hermann R, et al. TRIBUTE: a phase III trial of erlotinib hydrochloride (OSI-774) combined with carboplatin and paclitaxel chemotherapy in advanced non-small-cell lung cancer. J Clin Oncol 2005; 23: 5892-5899110673.73
74Eberhard DA, Johnson BE, Amler LC, et al. Mutations in the epidermal growth factor receptor and in KRAS are predictive and prognostic indicators in patients with non-small-cell lung cancer treated with chemotherapy alone and in combination with erlotinib. J Clin Oncol 2005; 23: 5900-5909109973.27
75Eramo A, Lotti F, Sette G, et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008; 15: 504-514108090
76Fabbri M, Garzon R, Cimmino A, et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A 2007; 104: 15805-15810107182.38
77Yun CH, Mengwasser KE, Toms AV, et al. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci U S A 2008; 105: 2070-2075105487.83
78Schaake-Koning C, van den Bogaert W, Dalesio O, et al. Effects of concomitant cisplatin and radiotherapy on inoperable non-small-cell lung cancer. N Engl J Med 1992; 326: 524-530104737.39
79Furuse K, Fukuoka M, Kawahara M, et al. Phase III study of concurrent versus sequential thoracic radiotherapy in combination with mitomycin, vindesine, and cisplatin in unresectable stage III non-small-cell lung cancer. J Clin Oncol 1999; 17: 2692-2699104649.81
80International Early Lung Cancer Action Program Investigators, Henschke CI, Yankelevitz DF, Libby DM, et al. Survival of patients with stage I lung cancer detected on CT screening. N Engl J Med 2006; 355: 1763-1771.103073.57
81Pignon JP, Tribodet H, Scagliotti GV, et al. Lung adjuvant cisplatin evaluation: a pooled analysis by the LACE Collaborative Group. J Clin Oncol 2008; 26: 3552-3559102285.17
82Reck M, von Pawel J, Zatloukal P, et al. Phase III trial of cisplatin plus gemcitabine with either placebo or bevacizumab as first-line therapy for nonsquamous non-small-cell lung cancer: AVAil. J Clin Oncol 2009; 27: 1227-1234101592.27
83Jackson EL, Willis N, Mercer K, et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001; 15: 3243-3248100853.05
84Pirker R, Pereira JR, Szczesna A, et al. Cetuximab plus chemotherapy in patients with advanced nonsmall- cell lung cancer (FLEX): an open-label randomised phase III trial. Lancet 2009; 373: 1525-1531100291.09
85Kim ES, Hirsh V, Mok T, et al. Gefitinib versus docetaxel in previously treated non-small-cell lung cancer (INTEREST): a randomised phase III trial. Lancet 2008; 372: 1809-181898782.25
86Govindan R, Page N, Morgensztern D, et al. Changing epidemiology of small-cell lung cancer in the United States over the last 30 years: analysis of the surveillance, epidemiologic, and end results database. J Clin Oncol 2006; 24: 4539-454498170.07
87Jänne PA, Yang JC, Kim DW, et al. AZD9291 in EGFR inhibitor-resistant non-small-cell lung cancer. N Engl J Med 2015; 372: 1689-1699977195.4
88Fossella FV, DeVore R, Kerr RN, et al. Randomized phase III trial of docetaxel versus vinorelbine or ifosfamide in patients with advanced non-small-cell lung cancer previously treated with platinum-containing chemotherapy regimens. The TAX 320 Non-Small Cell Lung Cancer Study Group. J Clin Oncol 2000; 18: 2354-236297548.75
89Pfister DG, Johnson DH, Azzoli CG, et al. American Society of Clinical Oncology treatment of unresectable non-small-cell lung cancer guideline: update 2003. J Clin Oncol 2004; 22: 330-35396760.44
90Lardinois D, Weder W, Hany TF, et al. Staging of non-small-cell lung cancer with integrated positronemission tomography and computed tomography. N Engl J Med 2003; 348: 2500-250796356.65
91Dillman RO, Seagren SL, Propert KJ, et al. A randomized trial of induction chemotherapy plus high-dose radiation versus radiation alone in stage III non-small-cell lung cancer. N Engl J Med 1990; 323: 940-94596132.03
92Mountain CF, Dresler CM. Regional lymph node classification for lung cancer staging. Chest 1997; 111: 1718-172395241.39
93Aupérin A, Arriagada R, Pignon JP, et al. Prophylactic cranial irradiation for patients with small-cell lung cancer in complete remission. Prophylactic Cranial Irradiation Overview Collaborative Group. N Engl J Med 1999; 341: 476-48493344.43
94Rosell R, Gómez-Codina J, Camps C, et al. A randomized trial comparing preoperative chemotherapy plus surgery with surgery alone in patients with non-small-cell lung cancer. N Engl J Med 1994; 330: 153-15892735.65
95Rittmeyer A, Barlesi F, Waterkamp D, et al. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet 2017; 389: 255-265926308.67
96Douillard JY, Rosell R, De Lena M, et al. Adjuvant vinorelbine plus cisplatin versus observation in patients with completely resected stage IB-IIIA non-small-cell lung cancer (Adjuvant Navelbine International Trialist Association [ANITA]): a randomised controlled trial. Lancet Oncol 2006; 7: 719-72792566.07
97Kosaka T, Yatabe Y, Endoh H, Kuwano H, Takahashi T, Mitsudomi T. Mutations of the epidermal growth factor receptor gene in lung cancer: biological and clinical implications. Cancer Res 2004; 64: 8919-892392757.56
98Cappuzzo F, Ciuleanu T, Stelmakh L, et al. Erlotinib as maintenance treatment in advanced non-small-cell lung cancer: a multicentre, randomised, placebo-controlled phase 3 study. Lancet Oncol 2010; 11: 521-52989489.4
99Pignon JP, Arriagada R, Ihde DC, et al. A meta-analysis of thoracic radiotherapy for small-cell lung cancer. N Engl J Med 1992; 327: 1618-162489131.82
100Imielinski M, Berger AH, Hammerman PS, et al. Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 2012; 150: 1107-1120889111.13

[i] ACY – average citations per year

Statistical analysis

A commercial software (SPSS version 16.0, SPSS, Chicago IL, USA) was used for the statistical analysis. The Kolmogorov-Smirnov test was used to analyze the normal distribution of data. Spearman’s correlation was used to evaluate the associations between citation, ACY, IF and length of time since publication. A p-value < 0.05 was accepted as statistically significant.

Ethical statement

All authors declare that the study was conducted according to the principles of the World Medical Association Declaration of Helsinki: Ethical Principles for Medical Research Involving Human Subjects. This study did not require approval from an ethics committee as it was designed as a bibliometric analysis or citation analysis of existing published classical studies.

Results

We identified 240,701 articles from 1975 to 2019. The language was English for all articles. The 100 most cited articles in lung cancer are listed in Table 1, arranged in descending order according to the number of times cited. The number of citations ranged from 7751 to 889, and the mean number of citations per article was 1879.82 ±1264.78 (range: 7751–889). We found that the most cited article (times cited: 7751) on lung cancer was a study by Lynch et al. with the following title: “Activating mutations in the epidermal growth factor receptor underlying responsiveness of nonsmallcell lung cancer to gefitinib” published in N Engl J Med 2004; 350: 2129-1239. The least cited article (times cited: 889) on lung cancer was penned by Imielinski et al. with the following title: “Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing” and published in Cell 2012; 150: 1107-1120. Additionally, we determined that there were 84 articles that got more than 1000 citations and the article with the highest ACY was the article that ranked 16 in the T100 list. The article with the highest ACY was a randomized phase 3 trial by Borghaei et al., titled “Nivolumab versus docetaxel in advanced nonsquamous non-smallcell lung cancer” and published in N Engl J Med 2015; 373: 1627-1639. The highest number of citations was seen in 2017 with 18,393 citations while the highest number of publications was seen in 2005 with 12 publications.

The oldest article was a review published in Nature 1985; 316: 823-826 titled “Bombesin-like peptides can function as autocrine growth factors in human small-cell lung cancer” by Cuttitta et al. with 1280 citations and ACY 36.57 ACY. The newest study in the T100 list was a phase 3 trial conducted by Rittmeyer et al. published in Lancet 2017; 389: 255-265 with the following title: “Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial”, with 926 citations and ACY 308.67.

In the T100 list, 82 were clinical studies and 18 were experimental studies. The 82 clinical articles included 42 randomized controlled studies, 8 review articles, 4 meta-analyses, 2 case reports and other clinical studies. Fifty-nine of these 82 clinical articles were treatment-based studies. The treatment-based studies are classified in Table 2 according to the level of evidence.

Table 2

Type of treatment and level of evidence of the treatment based clinical articles (n = 59)

TreatmentLevel 1Level 2Level 3Level 4
EGFR mutations176
Chemotherapy191
Palliative care1
Immunotherapy511
ALK mutations21
Radiotherapy311

[i] EGFR – epidermal growth factor receptor, ALK – anaplastic lymphoma kinase

While 32 of these articles were published in NEJM, 16 were published in the Journal of Clinical Oncology, 7 in The Lancet, 7 in Science, etc. (Table 3).

Table 3

List of journals with published articles

JournalNumber of articlesImpact Factor*Quartile score**
New England Journal of Medicine (NEJM)3279.258Q1
Journal of Clinical Oncology1626.303Q1
Lancet753.254Q1
Science741.058Q1
Lancet Oncology536. 418Q1
Journal of the National Cancer Institute (JNCI)411.238Q1
Cancer Research39.13Q1
Cell331.398Q1
Chest37.652Q1
Nature341.577Q1
Proceedings of the National Academy of Sciences of the United States of America39.504Q1
Journal of the American Medical Association (JAMA)247.661Q1
Journal of Thoracic Oncology210.336Q1
American Review of Respiratory Disease16.27Q1
British Medical Journal (BMJ)12.12Q1
Cancer Cell122.844Q1
Cell Death & Differentiation18.000Q1
Genes & Development19.462Q1
Mayo Clinic Proceedings17.199Q1
Nature Reviews Cancer142.784Q1
Oncogene16.854Q1
PLOS Medicine111.675Q1
Science Translational Medicine116.710Q1

* 2017 Journal Citation Reports (Clarivate Analytics)

** 2019 SCImago Journal and Country Rank

All of the T100 articles were published across 23 different journals. Eighty-five of the T100 articles were published in 14 journals that had IF ≥ 10.336. We determined that the mean IF of these 23 journals was 23.42 ±19.90 (range: 79.26–2.12) (according to Clarivate Analytics, 2017). The “Quartile Score” category was Q1 for all the journals (according to SCImago Journal and Country Rank, 2019). Most of the articles were published in NEJM, and NEJM was also the journal with the highest IF. The correlation analysis for the number of citations, ACY, IF and length of time since publication parameters in the T100 list revealed a positive correlation between citation and ACY (r = 0.744, p = 0.00) and between ACY and IF (r = 0.236, p = 0.018), whereas a negative correlation was observed between ACY and length of time since publication (r = –0.562, p = 0.00) and between IF and length of time since publication (r = –0.266, p = 0.008). There was no correlation between citation and length of time since publication or between citation and IF (Fig. 1).

Fig. 1

Correlation analysis for the citation numbers, ACY, IF, length of time since publication parameters

/f/fulltexts/WO/40482/WO-24-94725-g001_min.jpg

According to the geographic origin of the T100 list, the USA (n = 74) was the most contributing country, followed by Japan and Canada (Table 4). We determined that the most commonly listed institution was the University of Harvard (USA), which was listed 27 times in the top 100 cited articles (Table 5). Moreover, 11/19 of the institutions that published eight or more publications were found to be in USA.

Table 4

Geographic origin of the top 100 articles

CountryNumber of articles
United States of America74
Japan20
Canada19
Germany19
Italy19
England18
Spain18
France18
Netherlands10
South Korea10
Poland9
Australia9
Brazil8
China7
Switzerland6
Belgium5
Chile5
Russia5
Taiwan5
Denmark4
Table 5

Institutions of origin with 8 or more of the top 100 cited articles

RankInstitutionNumber*
1Harvard University27
2VA Boston Healthcare System26
3Dana Farber Cancer Institute17
4University of Texas System17
5Memorial Sloan Kettering Cancer Center16
6University of California System16
7UT MD Anderson Cancer Center16
8Massachusetts General Hospital15
9Unicancer15
10Vanderbilt University15
11University of Toronto10
12Princess Margaret Cancer Centre9
13Ruprecht Karls University Heidelberg9
14University Health Network Toronto9
15Astrazeneca8
16Gustave Roussy8
17National Institutes of Health NIH USA8
18Samsung Medical Center8
19Sungkyunkwan University8
20University of California Los Angeles8

* Number of times listed of highest ranking 20 institutions in the top 100 cited articles.

It was seen that 3 authors were the first author in more than one article in the T100 list’s top 12 authors (Table 6). Herbst RS contributed to 8 articles and was the first author in 4 of them. Janne PA, Johnson BE and Johnson DH also contributed to 8 articles. However, Herbst RS had the highest number of articles as first author. The “Web of Science” category analysis of the T100 in the field of the lung cancer revealed that these articles ranked under general internal medicine (n = 47), oncology (n = 33), multidisciplinary sciences (n = 13), cell biology (n = 8) and respiratory system (n = 6) as the most featured branches.

Table 6

The most common authors with 6 or more in the top 100 cited articles

AuthorNumber of top 100 articles
AuthorFirst authorCo-author
Herbst RS844
Janne PA817
Johnson BE88
Johnson DH817
Lynch TJ716
Rosell R734
Takahashi T716
Von Pawel J77
Felip E66
Meyerson M66
Settleman J66
Shepherd FA624

Discussion

Lung cancer is the major cause of cancer-related deaths worldwide. There are two main types of this cancer: small-cell lung cancer (SCLC) and non-small cell lung cancer (NSCLC). NSCLC accounts for 80% of all lung cancers. Despite the advances in surgical methods and advances in radiotherapy and chemotherapy, non-small-cell lung cancer continues to account for the majority of lung cancers and is associated with a 5-year survival rate of 15% [112].

There have been significant advances in the treatment of lung cancer in the last 40 years, and this is reflected in the scientific literature. A better understanding of disease progression coupled with targeted immunological therapies has led to increased survival rates.

We found that in our top 100, 28% of the articles were less than 10 years old while 72% of them were older than 10 years. Articles with a higher number of citations are indeed expected to be older. Year of publication and number of citations for an article are closely linked, and the number of citations grows over time. Needless to say, citation is an important metric, which shows the quality and attractiveness of an article; however, a certain amount of time should be allowed to pass after the publication of an article for it to reach a higher number of citations. For that reason, number of citations alone is inadequate to determine the quality of an article. In this study, ACY was used to eliminate the time bias when evaluating older articles against newer articles. Of the T100, 18% were comparative studies, and there were 2 case reports in the T100 list. The two case reports were published in 2005. One of them was published in NEJM (times cited: 2549), and the other in Plos Med (times cited: 2073). Both were about EGFR mutations. It is noteworthy that a case report receives such a high number of citations. This may be due to the fact that EGFR mutations were popular in the 2000s. In the T100, 29% of the articles were noted to concern erlotinib (anti-EGFR), gefitinib (anti-EGFR) and EGFR mutations. The 1st study with the highest number of citations was a study related to EGFR mutations, showing that EGFR mutations play an important role in the development stages of lung cancer treatments.

Immunotherapy has become one of the most promising treatments for several human cancers. In fact, James P. Allison and Tasuku Honjo were awarded with the Nobel Prize in medicine for their research on immune checkpoint blockade [113, 114]. As a result, the immune check-point inhibitor (ICPI) may be regarded as an immunotherapy modality that started a new era in cancer treatment and remains a new trend topic. Especially in advanced non-small cell lung cancer (NSCLC), significant improvement has been observed in survival results with anti-PD-1 and PDL-1 drugs compared to chemotherapy. That shows the changing trends in cancer immunotherapy during the last decade. We can also see studies on immunotherapy in the T100 list. The most cited immunotherapy-related study in T100 was published in 2015 and received 2966 citations (ACY 593.2). It was published in N Engl J Med 2015; 373: 123-135 by Brahmer et al. with the following title: “Nivolumab versus docetaxel in advanced squamouscell non-smallcell lung cancer”. This study currently remains a new study of only 4 years old, and despite being a very young article, the number of citations it has received shows that the study in question involves a very important innovation. Moreover, this article has the highest ACY score in the T100 list. This shows that scientists are currently focused on immunotherapy. There are only 7 studies about immunotherapy in the T100, and the newest article in the T100 was published in Lancet 2017; 389: 255-265 by Rittmeyer, titled “Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial”. It is only a 2-year-old article; however, it has 926 citations with an ACY score of 308.67. When we list the articles based on ACY scores in descending order, the first 4 articles are immunotherapy-related and recent articles.

The correlation analysis showed a positive correlation between citation and ACY and between ACY and IF, whereas a negative correlation was found between ACY and length of time since publication and between IF and length of time since publication. This indicates that articles with high ACY scores have been published in journals with a high IF. Furthermore, younger articles have higher ACY scores and have been published in journals with a higher IF.

When we looked at the T100 list, another point of interest also caught our attention: there were very few articles related to small-cell lung cancer (SCLC). Only 3 articles were on small-cell lung cancer [115117]. This either means that there has not been any significant advance in SCLC or scientists are less interested in this topic.

Conclusions

To the best of our knowledge, this is the first report of a citation analysis of lung cancer in the English literature. The first 100 articles in our analysis not only identify landmark articles that have the greatest impact on lung cancer research, but also acknowledge the most productive authors and institutions that contributed to the list with their articles. Oncology is a developing field in science, and we have seen its evolution through the treatment of lung cancer over the years. Briefly, bibliometric analyses for different medical disciplines and sub-specialties demonstrate the improvements in a given field from a nominative perspective. The present bibliometric citation analysis on lung cancer has covered several scientific fields, and we believe it enables the systematic identification of true landmark publications as well as the distribution of citations of these publications by year, main topic, institution, scientific journal, level of evidence, and correlation analysis, thereby providing a substantial contribution for oncological research.

Notes

[6] Conflicts of interest The authors declare no conflict of interest.

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