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. 2020 Jan 15;48(1):0300060519896149. doi: 10.1177/0300060519896149

The top 100 most impactful articles and recent trends in nasopharyngeal carcinoma from 1970 to 2018: a bibliometric analysis

QingWu Wu 1, Tian Yuan 1, Zongping Zhang 2, Qintai Yang 1,✉, Mingyuan Chen 3, Qiong Wang 4, Huiyi Deng 1, Huijun Qiu 1, Xinyue Wang 1, Xuekun Huang 1
PMCID: PMC7113718  PMID: 31937171

Short abstract

Objective

To identify the top 100 most impactful articles in nasopharyngeal carcinoma (NPC).

Methods

Articles on NPC from 1970 to 2018 were retrieved from the Web of Science (WoS). These articles were ranked in descending order based on the number of times they were cited, and all titles and abstracts were screened to identify the top 100 most-cited articles.

Results

The earliest and most recent articles were published in 1971 and 2016, respectively. The most prolific decade was the 2000s, with 51 articles published. The highest citation count reached 1223 and the lowest was 155. Thirty-four journals contributed to the 100 articles, with the International Journal of Radiation Oncology Biology Physics contributing the most articles (n=16). Notable contribution origins were Hong Kong (n=34), the United States (n=26), and China (mainland, n=12). The top three contributors were Chan ATC, Lee AWM, and Lo KW who were from Hong Kong. The types of articles included basic research (n=50), clinical research (n=36), and reviews (n=14).

Conclusions

This study identified the top 100 most impactful articles in NPC and stressed the multidisciplinary and multimodal nature of NPC management. Understanding historical articles may guide future NPC study.

Keywords: Bibliometric, citation analysis, Web of Science, radiotherapy, chemotherapy, nasopharyngeal carcinoma

Introduction

Over the past decades, the mortality rate associated with nasopharyngeal carcinoma (NPC) has decreased,1 reflecting years of research that was focused on innovative techniques for controlling and managing NPC. However, an abundance of NPC literature involving different researchers, countries, specialties, and scientific journals has emerged and it is difficult to identify the important papers.

Citation analysis is a bibliometric analysis method2 that evaluates the influence and importance of an article in a certain field by analyzing the citation count.3 It is also an affirmation to authors, institutions, and countries that have made important contributions. This method has been frequently applied and widely recognized in various disciplines, such as orthopedics,4 neurosurgery,5 ophthalmology,6 and otolaryngology.7,8 However, few articles have analyzed the highly cited NPC papers. Therefore, we aimed to identify the top 100 most-cited NPC articles from 1970 to 2018 using citation analysis.

In addition, recently published papers may not have sufficient citations mainly because of the time-dependent citation analysis.9 For example, none of the clinical articles published from 2013 to 2018 were in our top 100 most-cited list. Therefore, to more comprehensively reveal the NPC development trend and research focus, we also conducted a corresponding analysis to identify the top 10 clinical research articles from 2013 to 2018.

Methods

Search strategy

We searched “TI = (nasopharyngeal carcinoma* OR nasopharyngeal cancer* OR nasopharyngeal neoplasm* OR nasopharyngeal tumor*)” on the Web of Science (WoS). The articles ranged from January 1970 to August 2018 and the document types were original articles and reviews. The retrieved articles were ranked from highest to lowest based on the number of citations. Two researchers reviewed and screened the title and abstract of the articles. If necessary, some studies with mixed NPC factors, such as head and neck cancer and Burkitt lymphoma, were excluded. Because no human subjects were enrolled, ethics approval was not required for this study.

Data extraction

After filtering the articles, we extracted the contents including the title of each article, the number of citations, the source journal, the first author, and the research institute and its country. Next, based on the type of article, the literature records were further divided into basic research, clinical research, and review. We extracted the type of study and the clinical evidence.

Statistical analysis

Data were analyzed using IBM SPSS 22.0 package (IBM Corp., Armonk, NY, USA). Descriptive statistics are presented as the count or percentage of the parameters. This study did not involve statistically significant differences.

Results

Our literature search yielded 17,116 articles between 1970 and 2018, and the top 100 articles on AR were identified based on the number of times they were cited (Table 1).

Table 1.

The top 100 most impactful articles on NPC.

Rank Title Journal Year First Author Institute Citation Class
1 Chemoradiotherapy versus radiotherapy in patients with advanced nasopharyngeal cancer: Phase III randomized intergroup study 0099 Journal of Clinical Oncology 1998 Al-Sarraf M Providence Cancer Center 1223 2
2 Nasopharyngeal carcinoma Lancet 2005 Wei WI Queen Mary Hospital 724 Review
3 Intensity-modulated radiotherapy in the treatment of nasopharyngeal carcinoma: An update of the UCSF experience International Journal of Radiation Oncology Biology Physics 2002 Lee N University of California–San Francisco 638 4
4 The enigmatic epidemiology of nasopharyngeal carcinoma Cancer Epidemiology Biomarkers and Prevention 2006 Chang ET Northern California Cancer Center 604 Review
5 Epidemiology of nasopharyngeal carcinoma Seminars in Cancer Biology 2002 Yu MC Norris Comprehensive Cancer Center 517 Review
6 Epstein-Barr virus-specific IgA serum antibodies as an outstanding feature of nasopharyngeal carcinoma International Journal of Cancer 1976 Henle G the Children’s Hospital of Philadelphia and School of Medicine 491 Technique
7 Retrospective analysis of 5037 patients with nasopharyngeal carcinoma treated during 1976-1985 - overall survival and patterns of failure International Journal of Radiation Oncology Biology Physics 1992 Lee AWM Queen Elizabeth Hospital 446 4
8 Phase III study of concurrent chemoradiotherapy versus radiotherapy alone for advanced nasopharyngeal carcinoma: Positive effect on overall and progression-free survival Journal of Clinical Oncology 2003 Lin JC Taichung Veterans General Hospital 431 2
9 Expression of Epstein-Barr virus-encoded proteins in nasopharyngeal carcinoma International Journal of Cancer 1988 Fahraeus R Karolinska Institute 414 Technique
10 EB viral genomes in epithelial nasopharyngeal carcinoma cells Nature-New Biology 1973 Wolf H University of Erlangen Nuremberg 413 Technique
11 Epstein-Barr virus gene-expression in nasopharyngeal carcinoma Journal of General Virology 1988 Young LS University of Birmingham 411 Technique
12 Quantitative analysis of cell-free Epstein-Barr virus DNA in plasma of patients with Nasopharyngeal carcinoma Cancer Research 1999 Lo YMD The Chinese University of Hong Kong 407 Technique
13 Xerostomia and quality of life after intensity-modulated radiotherapy vs. conventional radiotherapy for early-stage nasopharyngeal carcinoma: Initial report on a randomized controlled clinical trial International Journal of Radiation Oncology Biology Physics 2006 Pow Edmond HN University of Hong Kong 392 2
14 Prospective randomized study of intensity-modulated radiotherapy on salivary gland function in early-stage nasopharyngeal carcinoma patients Journal of Clinical Oncology 2007 Kam MKM Prince of Wales Hospital 386 2
15 Epstein-Barr-virus latent gene-transcription in nasopharyngeal carcinoma-cells - coexpression of EBNA1, LMP1, and LMP2 transcripts Journal of Virology 1992 Brooks L University of Binningham 383 Technique
16 Clonal proliferations of cells infected with Epstein-Barr virus in preinvasive lesions related to nasopharyngeal carcinoma New England Journal of Medicine 1995 Pathmanathan R University of North Carolina 377 Technique
17 Quantification of plasma Epstein-Barr virus DNA in patients with advanced nasopharyngeal carcinoma New England Journal of Medicine 2004 Lin JC Taichung Veterans General Hospital 375 Technique
18 Chemotherapy in locally advanced nasopharyngeal carcinoma: An individual patient data meta-analysis of eight randomized trials and 1753 patients International Journal of Radiation Oncology Biology Physics 2006 Baujat B Institut Gustave Roussy 367 1
19 Randomized trial of radiotherapy versus concurrent chemoradiotherapy followed by adjuvant chemotherapy in patients with American Joint Committee on Cancer/International Union against Cancer stage III and IV Nasopharyngeal Cancer of the Endemic Variety Journal of Clinical Oncology 2005 Wee J National University of Singapore 356 2
20 Epstein-Barr virus in the pathogenesis of NPC Seminars in Cancer Biology 2002 Raab-Traub N Lineberger Comprehensive Cancer Center 346 Review
21 Focus on nasopharyngeal carcinoma Cancer Cell 2004 Lo KW Prince of Wales Hospital 335 Review
22 Treatment results for nasopharyngeal carcinoma in the modern era: The Hong Kong experience International Journal of Radiation Oncology Biology Physics 2005 Lee AWM Pamela Youde Nethersole Eastern Hospital 325 4
23 Treatment of nasopharyngeal carcinoma with intensity-modulated radiotherapy: The Hong Kong experience International Journal of Radiation Oncology Biology Physics 2004 Kam MKM Prince of Wales Hospital 313 4
24 MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, up-regulating mRNAs encoding extracellular matrix proteins Proceedings of the National Academy of Sciences of the United States of America 2008 Sengupta Srikumar National Cancer Institute 297 Technique
25 How does intensity-modulated radiotherapy versus conventional two-dimensional radiotherapy influence the treatment results in nasopharyngeal carcinoma patients? International Journal of Radiation Oncology Biology Physics 2011 Lai SZ Sun Yat-Sen University Cancer Center 285 4
26 Intensity-modulated radiation therapy (IMRT) for nasopharynx cancer: Update of the memorial Sloan-Kettering experience International Journal of Radiation Oncology Biology Physics 2006 Wolden SL Memorial Sloan-Kettering Cancer Center 282 4
27 Intensity-modulated radiation therapy with or without chemotherapy for nasopharyngeal carcinoma: Radiation therapy oncology group phase II trial 0225 Journal of Clinical Oncology 2009 Lee Nancy Memorial Sloan-Kettering Cancer Center 280 3
28 Concurrent chemotherapy-radiotherapy compared with radiotherapy alone in locoregionally advanced nasopharyngeal carcinoma: Progression-free survival analysis of a phase III randomized trial Journal of Clinical Oncology 2002 Chan ATC Prince of Wales Hospital 278 2
29 Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line Cancer Research 2007 Wang J Sun Yat-Sen University Cancer Center 262 Technique
30 Overall survival after concurrent cisplatin-radiotherapy compared with radiotherapy alone in locoregionally advanced nasopharyngeal carcinoma Journal of the National Cancer Institute 2005 Chan ATC Prince of Wales Hospital 262 2
31 Bmi-1 is a novel molecular marker of nasopharyngeal carcinoma progression and immortalizes primary human nasopharyngeal epithelial cells Cancer Research 2006 Song LB Sun Yat-sen University Cancer Center 256 Technique
32 Preliminary results of a randomized study on therapeutic gain by concurrent chemotherapy for regionally-advanced nasopharyngeal carcinoma: NPC-9901 trial by the Hong Kong nasopharyngeal cancer study group Journal of Clinical Oncology 2005 Lee AWM Pamela Youde Nethersole Eastern Hospital 256 2
33 Nasopharyngeal carcinoma cell line (C666-1) consistently harbouring Epstein-Barr virus International Journal of Cancer 1999 Cheung ST Prince of Wales Hospital 249 Technique
34 Mir-26a inhibits cell growth and tumorigenesis of nasopharyngeal carcinoma through repression of ezh2 Cancer Research 2011 Lu J Nanfang Hospital 247 Technique
35 Serologic markers of Epstein-Barr virus infection and nasopharyngeal carcinoma in Taiwanese men New England Journal of Medicine 2001 Chien YC National Taiwan University 243 Technique
36 High frequency of promoter hypermethylation of rassf1a in nasopharyngeal carcinoma Cancer Research 2001 Lo KW Prince of Wales Hospital 242 Technique
37 Results of a prospective randomized trial comparing neoadjuvant chemotherapy plus radiotherapy with radiotherapy alone in patients with locoregionally advanced nasopharyngeal carcinoma Journal of Clinical Oncology 2001 Ma J Sun Yat-Sen University Cancer Center 242 2
38 Quantitative and temporal correlation between circulating cell-free Epstein-Barr virus DNA and tumor recurrence in nasopharyngeal carcinoma Cancer Research 1999 Lo YMD The Chinese University of Hong Kong 241 Technique
39 Abundant expression of eber1 small nuclear-RNA in nasopharyngeal carcinoma - a morphologically distinctive target for detection of Epstein-Barr virus in formalin-fixed paraffin-embedded carcinoma specimens American Journal of Pathology 1991 Wu TC Johns Hopkins School of Medicine 240 Technique
40 The additional value of chemotherapy to radiotherapy in locally advanced nasopharyngeal carcinoma: A meta-analysis of the published literature Journal of Clinical Oncology 2004 Langendijk JA University Hospital Vrije Universiteit 235 1
41 Norepinephrine up-regulates the expression of vascular endothelial growth factor, matrix metalloproteinase (MMP)-2, and MMP-9 in nasopharyngeal carcinoma tumor cells Cancer Research 2006 Yang Eric V. The Ohio State University Medical Center 234 Technique
42 Nasopharyngeal carcinoma: Molecular biomarker discovery and progress Molecular Cancer 2007 Cho William Chi-shing Queen Elizabeth Hospital 230 Review
43 Coexpression of hypoxia-inducible factors 1 alpha and 2 alpha, carbonic anhydrase ix, and vascular endothelial growth factor in nasopharyngeal carcinoma and relationship to survival Clinical Cancer Research 2002 Hui EP Prince of Wales Hospital 230 Technique
44 Treatment of nasopharyngeal carcinoma with Epstein-Barr virus-specific T lymphocytes Blood 2005 Straathof KCM Baylor College of Medicine 226 4
45 Nasopharyngeal carcinoma Annals of Oncology 2002 Chan ATC Prince of Wales Hospital 226 Review
46 The differentiated form of nasopharyngeal carcinoma contains Epstein-Barr virus-DNA International Journal of Cancer 1987 Raab-Traub N Lineberger Cancer Research Center 223 Technique
47 Randomized phase II trial of concurrent cisplatin-radiotherapy with or without neoadjuvant docetaxel and cisplatin in advanced nasopharyngeal carcinoma Journal of Clinical Oncology 2009 Hui Edwin P Prince of Wales Hospital 221 2
48 Isolation and sequencing of the Epstein-Barr virus bnlf-1 gene (LMP1) from a Chinese nasopharyngeal carcinoma Journal of General Virology 1991 Hu LF Karolinska Institute 219 Technique
49 Modulation of lmp1 protein expression by EBV-encoded microRNAs Proceedings of The National Academy of Sciences of the United States of America 2007 Lo Angela KF Sidney Kimmel Cancer Center 214 Technique
50 An unusualvirus in cultures from a human nasopharyngeal carcinoma Journal of the National Cancer Institute 1971 Achong BG University of Bristol Medical School 213 Technique
51 The infratemporal fossa approach for nasopharyngeal tumors Laryngoscope 1983 Fisch U University of Zurich Kantonsspital 211 4
52 Plasma Epstein-Barr virus DNA and residual disease after radiotherapy for undifferentiated nasopharyngeal carcinoma Journal of the National Cancer Institute 2002 Chan ATC Prince of Wales Hospital 208 Technique
53 Cantonese-style salted fish as a cause of nasopharyngeal carcinoma - report of a case-control study in Hong-Kong Cancer Research 1986 Yu MC University of Southern California 207 Technique
54 Bcl-2 proto-oncogene expression in Epstein-Barr virus-associated nasopharyngeal carcinoma International Journal of Cancer 1993 Lu QL Imperial Cancer Research Fund 205 Technique
55 Comparison of treatment plans involving intensity-modulated radiotherapy for nasopharyngeal carcinoma International Journal of Radiation Oncology Biology Physics 2000 Xia P University of California 201 4
56 MicroRNA deregulation and pathway alterations in nasopharyngeal carcinoma British Journal of Cancer 2009 Chen HC Chang Gung University 200 Technique
57 A prospective randomized study of chemotherapy adjunctive to definitive radiotherapy in advanced nasopharyngeal carcinoma International Journal of Radiation Oncology Biology Physics 1995 Chan ATC Prince of Wales Hospital 200 2
58 A genome-wide association study of nasopharyngeal carcinoma identifies three new susceptibility loci Nature Genetics 2010 Bei JX Sun Yat-sen University Cancer Center 199 Technique
59 Concurrent chemoradiotherapy plus adjuvant chemotherapy versus concurrent chemoradiotherapy alone in patients with locoregionally advanced nasopharyngeal carcinoma: A phase 3 multicentre randomised controlled trial Lancet Oncology 2012 Chen L Sun Yat-sen University Cancer Center 198 2
60 Preliminary report of the Asian-Oceanian clinical oncology association randomized trial comparing cisplatin and epirubicin followed by radiotherapy versus radiotherapy alone in the treatment of patients with locoregionally advanced nasopharyngeal carcinoma Cancer 1998 Chua DTT Queen Mary Hospital 198 2
61 Reirradiation of recurrent nasopharyngeal carcinoma - treatment techniques and results International Journal of Radiation Oncology Biology Physics 1987 Wang CC Massachusetts General Hospital Cancer Center 198 4
62 Adjuvant chemotherapy with vincristine, cyclophosphamide, and doxorubicin after radiotherapy in local-regional nasopharyngeal cancer - results of a 4-year multicenter randomized study Journal of Clinical Oncology 1988 Rossi A Istituto Nazionale Tumori 197 2
63 Induction of cyclooxygenase-2 by Epstein-Barr virus latent membrane protein 1 is involved in vascular endothelial growth factor production in nasopharyngeal carcinoma cells Proceedings of The National Academy of Sciences of The United States of America 2001 Murono S Lineberger Comprehensive Cancer Center 195 Technique
64 Molecular prognostication of nasopharyngeal carcinoma by quantitative analysis of circulating Epstein-Barr virus DNA Cancer Research 2000 Lo YMD The Chinese University of Hong Kong 195 Technique
65 Preliminary results of a randomized trial comparing neoadjuvant chemotherapy (cisplatin, epirubicin, bleomycin) plus radiotherapy vs radiotherapy alone in stage IV (≥n2, m0) undifferentiated nasopharyngeal carcinoma: a positive effect on progression-free survival International Journal of Radiation Oncology Biology Physics 1996 Cvitkovic E Institute Gustave Roussy 193 2
66 Deletions within the LMP1 oncogene of Epstein-Barr virus are clustered in Hodgkin’s-disease and identical to those observed in nasopharyngeal carcinoma Blood 1993 Knecht H CHUV University Hospital 190 Technique
67 Carcinoma of the nasopharynx treated by radiotherapy alone: Determinants of local and regional control International Journal of Radiation Oncology Biology Physics 1997 Sanguineti G M.D. Anderson Cancer Center 187 4
68 Linkage of a nasopharyngeal carcinoma susceptibility locus to the HLA region Nature 1990 Lu SJ People’s Regional Hospital 186 Technique
69 Analysis of 1379 patients with nasopharyngeal carcinoma treated by radiation Cancer 1988 Qin DX Chinese Academy of Medical Sciences 186 Technique
70 Histo-pathology of nasopharyngeal carcinoma - correlations with epidemiology, survival rates and other biological characteristics Cancer 1979 Shanmugaratnam K University of Singapore 186 Technique
71 Nasopharyngeal cancer detection based on blood plasma surface-enhanced Raman spectroscopy and multivariate analysis Biosensors & Bioelectronics 2010 Feng SY Fujian Normal University 184 Technique
72 Intensity-modulated radiotherapy in nasopharyngeal carcinoma: Dosimetric advantage over conventional plans and feasibility of dose escalation International Journal of Radiation Oncology Biology Physics 2003 Kam MKM Prince of Wales Hospital 184 4
73 Blood diffusion and th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells Blood 2009 Klibi Jihene Universite Paris-Sud 183 Technique
74 miR-218 suppresses nasopharyngeal cancer progression through downregulation of survivin and the SLIT2-ROBO1 pathway Cancer Research 2011 Alajez Nehad M Ontario Cancer Institute 182 Technique
75 Cloning and characterization of the latent membrane-protein (LMP) of a specific Epstein-Barr virus variant derived from the nasopharyngeal carcinoma in the Taiwanese population Oncogene 1992 Chen ML Chang-Gung Medical College 182 Technique
76 Establishment and characterization of 3 transplantable EBV-containing nasopharyngeal carcinomas International Journal of Cancer 1988 Busson P Institut Gustave Roussy 182 Technique
77 Nasopharyngeal carcinoma - review of the molecular mechanisms of tumorigenesis Head and Neck-Journal for the Sciences and Specialties of the Head and Neck 2008 Chou Josephine University of California 180 Review
78 A prospective, randomized study comparing outcomes and toxicities of intensity-modulated radiotherapy vs. conventional two-dimensional radiotherapy for the treatment of nasopharyngeal carcinoma Radiotherapy and Oncology 2012 Peng G Cancer Center of Union Hospital 179 2
79 Undifferentiated, nonkeratinizing, and squamous-cell carcinoma of the nasopharynx - variants of Epstein-Barr virus-infected neoplasia American Journal of Pathology 1995 Pathmanathan R Lineberger Comprehensive Cancer Center 178 Technique
80 Significant prognosticators after primary radiotherapy in 903 nondisseminated nasopharyngeal carcinoma evaluated by computer tomography International Journal of Radiation Oncology Biology Physics 1996 Teo P Prince of Wales Hospital 175 Technique
81 Nasopharyngeal carcinoma Lancet 1997 Vokes EE The University of Chicago 174 Review
82 Three-dimensional intensity-modulated radiotherapy in the treatment of nasopharyngeal carcinoma: The university of California-San Francisco experience International Journal of Radiation Oncology Biology Physics 2000 Sultanem K University of California 173 4
83 Etiology of nasopharyngeal carcinoma - a review Epidemiologic Reviews 1993 Hildesheim A National Cancer Institute 172 Review
84 Genome-wide scan for familial nasopharyngeal carcinoma reveals evidence of linkage to chromosome 4 Nature Genetics 2002 Feng BJ Sun Yat-sen University Cancer Center 171 Technique
85 Nasopharyngeal carcinoma Lancet 2016 Chua MLK National Cancer Centre Singapore 167 Review
86 Genetic and epigenetic changes in nasopharyngeal carcinoma Seminars in Cancer Biology 2002 Lo KW Prince of Wales Hospital 166 Technique
87 Promoter hypermethylation of multiple genes in nasopharyngeal carcinoma Clinical Cancer Research 2002 Kwong J The Chinese University of Hong Kong 164 Technique
88 Concurrent and adjuvant chemotherapy for nasopharyngeal carcinoma: A factorial study Journal of Clinical Oncology 2004 Kwong DLW Queen Mary Hospital 163 2
89 Demonstration of Epstein-Barr virus-associated nuclear antigen in nasopharyngeal carcinoma cells from fresh biopsies International Journal of Cancer 1974 Huang DP Queen Elizabeth Hospital 163 Technique
90 Hypermethylation of the p16 gene in nasopharyngeal carcinoma Cancer Research 1996 Lo KW Prince of Wales Hospital 162 Technique
91 Nasopharyngeal cancer - epidemiology, staging, and treatment Seminars in Oncology 1994 Fandi A Institute Gustave Roussy 162 Review
92 2 Epithelial tumor-cell lines (HNE-1 and HONE-1) latently infected with Epstein-Barr virus that were derived from nasopharyngeal carcinomas Proceedings of the National Academy of Sciences of the United States of America 1989 Glaser R The Ohio State University Medical Center 161 Technique
93 High level expression of delta n-p63: A mechanism for the inactivation of p53 in undifferentiated nasopharyngeal carcinoma (NPC)? Oncogene 2000 Crook T Imperial College of Science, Technology and Medicine 160 Technique
94 Prognostic factors of nasopharyngeal carcinoma - a review of 759 patients British Journal of Radiology 1990 Sham JST Queen Mary Hospital 160 Review
95 Identification of serum amyloid a protein as a potentially useful biomarker to monitor relapse of nasopharyngeal cancer by serum proteomic profiling Clinical Cancer Research 2004 Cho WCS Queen Elizabeth Hospital 159 Technique
96 Plasma Epstein-Barr viral deoxyribonucleic acid quantitation complements tumor-node-metastasis staging prognostication in nasopharyngeal carcinoma Journal of Clinical Oncology 2006 Leung SF Sir YK Pao Centre for Cancer 158 Technique
97 Multicenter, phase II study of cetuximab in combination with carboplatin in patients with recurrent or metastatic nasopharyngeal carcinoma Journal of Clinical Oncology 2005 Chan ATC Prince of Wales Hospital 158 4
98 Prognostic value of a microRNA signature in nasopharyngeal carcinoma: A microRNA expression analysis Lancet Oncology 2012 Liu N Sun Yat-sen University Cancer Center 157 Technique
99 Randomized trial of radiotherapy plus concurrent-adjuvant chemotherapy vs radiotherapy alone for regionally advanced nasopharyngeal carcinoma JNCI-Journal of the National Cancer Institute 2010 Lee AWM Pamela Youde Nethersole Eastern Hospital 155 2
100 The aetiology of nasopharyngeal carcinoma Clinical Otolaryngology 2001 McDermott AL Queen Elizabeth Hospital 155 Review
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There were 6675 articles between 2013 and 2018, and the top 10 most-cited clinical research papers were identified (Table 2).

Table 2.

The top 10 most impactful clinical research articles on NPC from 2013 to 2018.

Rank Title Journal Year First Author Institute Citation Class
1 Long-term outcomes of intensity-modulated radiotherapy for 868 patients with nasopharyngeal carcinoma: An analysis of survival and treatment toxicities Radiotherapy and Oncology 2014 Sun XM Sun Yat-sen University Cancer Center 135 4
2 Chemotherapy and radiotherapy in nasopharyngeal carcinoma: An update of the MAC-NPC meta-analysis Lancet Oncology 2015 Blanchard P Paris-Saclay University 130 1
3 Induction chemotherapy plus concurrent chemoradiotherapy versus concurrent chemoradiotherapy alone in locoregionally advanced nasopharyngeal carcinoma: A phase 3, multicentre, randomised controlled trial Lancet Oncology 2016 Sun Y Sun Yat-sen University Cancer Centre 84 2
4 Concurrent chemo-radiation with or without induction gemcitabine, carboplatin, and paclitaxel: A randomized, phase 2/3 trial in locally advanced nasopharyngeal carcinoma International Journal of Radiation Oncology Biology Physics 2015 Tan T National Cancer Centre Singapore 71 2
5 Adoptive T-cell transfer and chemotherapy in the first-line treatment of metastatic and/or locally recurrent nasopharyngeal carcinoma Molecular Therapy 2014 Chia WK National Cancer Centre Singapore 70 4
6 Significant efficacies of neoadjuvant and adjuvant chemotherapy for nasopharyngeal carcinoma by meta-analysis of published literature-based randomized, controlled trials Annals of Oncology 2013 OuYang PY Sun Yat-sen University Cancer Center 69 1
7 Evolution of treatment for nasopharyngeal cancer - success and setback in the intensity-modulated radiotherapy era Radiotherapy and Oncology 2014 Lee AWM University of Hong Kong-Shenzhen Hospital 66 4
8 Progress report of a randomized trial comparing long-term survival and late toxicity of concurrent chemoradiotherapy with adjuvant chemotherapy versus radiotherapy alone in patients with stage III to IVB nasopharyngeal carcinoma from endemic regions of China Cancer 2013 Chen Y Sun Yat-sen University Cancer Center 65 2
9 Preliminary results of trial NPC-0501 evaluating the therapeutic gain by changing from concurrent-adjuvant to induction-concurrent chemoradiotherapy, changing from fluorouracil to capecitabine, and changing from conventional to accelerated radiotherapy fractionation in patients with locoregionally advanced nasopharyngeal carcinoma Cancer 2015 Lee AWM Pamela Youde Nethersole Eastern Hospital 61 2
10 Phase I trial of recombinant modified vaccinia ankara encoding Epstein-Barr viral tumor antigens in nasopharyngeal carcinoma patients Cancer research 2013 Hui EP The Chinese University of Hong Kong 55 4
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Number of articles published

The Top 100 articles were mostly published from 1971 to 2016 (Figure 1). Among them, the greatest number of articles was published in the 2000s (n=51), followed by 1990s (n=24). The number of articles in the 2010s was equal to that in the 1980s (n=10) and the 1970s had the fewest articles (n=5).

Figure 1.

Figure 1.

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Number of articles published by decade.

Number of articles cited

In these articles, the highest and lowest citation counts were 1223 and 155, respectively. The average citation count for a single article in the 1970s, 1980s, 1990s, 2000s, and 2010s was 293.2, 239.0, 271.2, 274.5, and 195.3, respectively.

Published journals

The 100 most influential papers were published in 34 journals. Among these journals, those with more than one article published and their impact factor are presented in Table 3. The top three journals were International Journal of Radiation Oncology Biology Physics (n=16), Journal of Clinical Oncology (n=14), and Cancer Research (n=11).

Table 3.

Journals with more than one published article.

Journal Number of Articles (n=83) Impact Factor 2017
International Journal of Radiation Oncology Biology Physics 16 5.6
Journal of Clinical Oncology 14 26.4
Cancer Research 11 9.1
International Journal of Cancer 7 7.4
Proceedings of the National Academy of Sciences of the United States of America 4 9.5
Blood 3 15.1
Cancer 3 6.5
Clinical Cancer Research 3 10.2
Journal of the National Cancer Institute 3 11.2
Lancet 3 53.3
New England Journal of Medicine 3 79.3
Seminars in Cancer Biology 3 10.2
American Journal of Pathology 2 4.1
Journal of General Virology 2 2.5
Lancet Oncology 2 36.4
Nature Genetics 2 27.1
Oncogene 2 6.9
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Origins

These articles were mainly from 12 countries/regions (Figure 2). Among these countries/regions, the top three were Hong Kong (n=34), USA (n=26), and China (China mainland, n=12). The second tier of countries/regions were Britain (n=7), France (n=5), Taiwan (n=5), Sweden (n=3), and Singapore (n=3). An equal number of articles originated from Canada, Germany, Italy, and the Netherlands (n=1 each).

Figure 2.

Figure 2.

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Origins of the top 100 most impactful articles on NPC.

First authors

There were 81 first authors who had contributed to these articles. Nine of the first authors had published more than one article. The top three authors were Chan ATC (n=6), Lee AWM (n=4), and Lo KW (n=4). They were followed by Kam MKM and Lo YMD (n=3 each) and by Lin JC, Pathmanathan R, Raab-Traub N, and Yu MC (n=2 each).

Institutions

These articles came from 55 institutions. There were 15 institutions with more than one published article (Table 4). Among them, the top three were the Prince of Wales Hospital (n=13), Sun Yat-Sen University Cancer Center (n=8), and Queen Elizabeth Hospital (n=5).

Table 4.

Institutions contributing to more than one published article.

Institutions Number of Articles (n=58)
Prince of Wales Hospital 17
Sun Yat-Sen University Cancer Center 8
Queen Elizabeth Hospital 5
Institute Gustave Roussy 4
Queen Mary Hospital 4
The Chinese University of Hong Kong 4
Lineberger Comprehensive Cancer Center 3
Pamela Youde Nethersole Eastern Hospital 3
Memorial Sloan-Kettering Cancer Center 2
National Cancer Institute 2
Taichung Veterans General Hospital 2
The Ohio State University Medical Center 2
University of Binningham 2
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The type of articles

Among the 100 articles, the number of articles on basic research, clinical research, and reviews was 50, 36, and 14, respectively. Most of the basic research articles focused on the pathogenesis, detection, and diagnosis of NPC (Figure 3).

Figure 3.

Figure 3.

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The type of articles.

Study types of clinical articles

The types of studies were 36 clinical articles, of which most were randomized trials (n=18), followed by case-series (n=15), systematic reviews (n=2), and non-randomized controlled cohort study (n=1).

The level of evidence

Among the 36 clinical articles, two, 18, one, and 15 articles were graded as having Level 1, 2, 3, and 4 evidence, respectively, based on “The Oxford 2011 Levels of Evidence” (Figure 4).

Figure 4.

Figure 4.

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Level of 36 clinical articles based on “The Oxford 2011 Levels of Evidence”.

Classification of treatment methods

The 36 clinical articles were mainly divided into nine treatment categories (Table 5). The top three were concurrent chemotherapy (n=11), intensity-modulated radiation therapy (IMRT, n=10), concurrent chemoradiotherapy plus adjuvant chemotherapy (n=4), and radiotherapy (n=4).

Table 5.

Treatment reported by 36 clinical articles on the top 100 list.

Treatment Number of Articles (n=36)
Concurrent chemotherapy 11
IMRT 10
Concurrent chemoradiotherapy plus adjuvant chemotherapy 4
Radiotherapy 4
Neoadjuvant chemotherapy 3
Surgery 1
T lymphocytes 1
Chemotherapy after recurrent tumor 1
Radiotherapy after recurrent tumor 1
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IMRT, intensity-modulated radiation therapy.

Comparation between 1970–2018 and 2013–2018 in the top 10 most-cited clinical articles

Based on the level of clinical evidence, the ratios (1970–2018 vs. 2013–2018) of Level 1, Level 2, and Level 4 evidence were 1:2, 5:4, and 4:4, respectively. None of the top 10 most-cited articles described Level 3 evidence (non-randomize controlled cohorts).

Comparing the clinical treatment patterns, the ratios (1970–2018 vs. 2013–2018) of concurrent chemotherapy, IMRT, radiotherapy, neoadjuvant chemotherapy, T lymphocytes, and recombinant vaccinia virus were 4:5, 4:2, 2:0, 0:1, 0:1, and 0:1, respectively.

Discussion

In our study, bibliometric analysis was used to identify the top 100 most impactful articles in NPC. These articles are representative of the many landmarks that have taken place in NPC over the past decades.

Our study showed that the highest ranking article was published by the Journal of Clinical Oncology in 1998.10 It suggested that concurrent chemoradiotherapy was superior to radiotherapy alone and that patients benefited from progression-free survival and overall survival. Because it had a large enough sample size and was a randomized controlled trial, it provided reliable evidence for clinicians to use for treating patients with NPC in the future.

The second highest ranking article was a review of NPC that was published by The Lancet in 2005.11 It provided researchers with a notable and useful summary of the pathology, clinical symptoms, diagnosis, tumor grading system, and treatment methods for NPC, and thus, it was well accepted and cited by other researchers.

The third highest ranking article was the application of IMRT in NPC, which was published by the International Journal of Radiation Oncology Biology Physics in 2002.12 It showed that IMRT can better control the recurrence of primary tumors and can protect salivary glands and adjacent important tissues to the greatest extent. Thus, this result had a significant impact on the future application of IMRT in NPC.

With the exception of the 2010s, the number of articles increased by decades. Thus, over half of the articles in our study were published in the 2000s. The finding is consistent with those of other bibliometric studies.6,13,14 The result demonstrates that new articles with novel discoveries and advanced technologies continue to be published.

Based on the average citation count for a single article over the past decades, the highest citation count was the 1970s, whereas the lowest count was the 2010s. This finding shows that because of the time-dependent citation analysis,9 previous articles have more citations compared with current articles.

Some bibliometric studies reported that journals with high impact factors, such as NEJM and The Lancet, were the leading journals.15,16 However, we found that the International Journal of Radiation Oncology Biology Physics was the most productive journal, despite having an impact factor of 5.6. This result shows that highly impactful articles are published in a specialized journal and are not limited to well-known general medical journals.

It has been shown that the most productive authors and institutions were always from the USA.13,16,17 In our study, Hong Kong was the most prolific region and Chan ATC, who contributed six articles, was from the Prince of Wales Hospital in Hong Kong. NPC has regional characteristics such as being common in the eastern and southeastern parts of Asia and eastern Africa. Thus, there are enough clinical research cases in Hong Kong. The findings indicate that Hong Kong has advanced technology and management concepts, and this region is good for researchers to learn and collaborate.

For the type of article, basic research articles on NPC accounted for half of the articles. They were mostly concerned with the epidemiology, pathogenesis, detection, and diagnostic techniques, such as Epstein−Barr virus (EBV)-associated DNA, microRNA, and its associated genomes. Among them, a noteworthy article was published in 1976 by Henle and Henle18 in the International Journal of Cancer, which was a study on NPC and EBV. It revealed the close relationship between EBV-related immunoglobulin A and NPC in serum, which was a milestone and laid the foundation for the determining the diagnosis and prognosis of NPC.

Some bibliometric articles on surgical tumors reported that more than half of the articles were of low-quality (Level 4).19 In our study, most clinical articles were scored as Levels 1 or 2 on the level-of-evidence grading scale. These results indicate that a high-quality NPC study was relatively easy to conduct and receive more citations compared with a low-quality study.

One of the Level 1 articles20 showed that concurrent chemoradiotherapy can confer survival benefits to patients with NPC, which was consistent with another highly cited article.21 This article also pointed out that the efficacy of induction chemotherapy and intensive chemotherapy before concurrent chemoradiotherapy would need to be further confirmed.

Based on the only article regarding surgery in the top 100 articles, the NPC tumor in patients with stage T1 or T2 did not disappear after radiotherapy, and radical resection of the tumor can prolong their survival time. For patients with stage T4 NPC, palliative cytoreductive surgery failed to confer benefits because of extensive tumor invasion of the skull base and cranial nerves.22 However, surgery is mostly used for some patients who needed a biopsy to confirm the diagnosis or who had tumor recurrence after radiotherapy based on a recent guideline (NCCN Clinical Practice Guidelines for Head and Neck Cancer, Version 3, 2019).23

Among the top 10 clinical articles from 1970 to 2018, one article on retrospective analysis written by Lee AWM in 1992 suggested that radiotherapy can increase the local tumor control rate and prolong overall survival and progression-free survival.24 His subsequent and highly cited article published in 2005 described a retrospective analysis of 2687 patients in Hong Kong, and confirmed the therapeutic effect of radiotherapy.25 Therefore, his articles provided a basis for future randomized clinical trials of IMRT.

For the top 10 clinical articles from 2013 to 2018, half were focused on concurrent chemoradiotherapy, while IMRT was described in only 20% of these articles. The findings show that the effect of IMRT was confirmed26,27 and related research was reduced accordingly. Additionally, neoadjuvant chemotherapy,28 T-lymphocyte immunotherapy,29 and recombinant vaccinia virus gene therapy30 had emerged. The results show that these new therapies are the current research priorities and the trends for future treatments.

There are some limitations in this paper. First, the citation count used for the citation analysis did not include self-citation. Second, because of the influence of certain time factors, it would be unfavorable for the most recently published articles in the citation analysis. Third, the database used in this article was the WoS. Although it is the most commonly used database with citation analysis capabilities, a small number of articles may have been missed.

Conclusions

To the best of our knowledge, this study is the first bibliometric study to identify the most impactful articles in the area of NPC. The findings indicate that articles with novel discoveries, advanced technologies, and a high quality level of evidence will receive more citations. Recognition of important historical contributions to this field may guide future investigations into NPC.

Acknowledgements

We thank Wenhao Zhou and Weifeng Kong (Department of Otolaryngology-Head and Neck Surgery, The Third Affiliated Hospital of Sun Yat-sen University) for assistance with the statistical analysis.

Author contributions

All authors were involved in the study. Q.-T. Yang and M.-Y. Chen conceived and designed the study. Q.-W. Wu, T. Yuan, and Z.-P. Zhang analyzed the data and wrote the paper. Q. Wang, H.-Y. Deng, and H.-J. Qiu performed the search strategy. X.-Y. Wang, and X.-K. Huang collected the data.

Declaration of conflicting interest

The authors declare that there is no conflict of interest.

Funding

This work was supported by the National Natural Science Foundation of China (Grant No. 81670912 and 81870704), the Industry-Academic Cooperation Foundation of Guangzhou (No. 201704030046), Sun Yat-sen University Clinical Research 5010 Program (No.2019006), and Science Technology Innovation Commission of Shenzhen Municipality (No. JCYJ20180305163629056).

ORCID iD

Qintai Yang http://orcid.org/0000-0003-3377-737X

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