Systematic Reviews Open Access
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World J Hepatol. Nov 28, 2016; 8(33): 1478-1488
Published online Nov 28, 2016. doi: 10.4254/wjh.v8.i33.1478
Bibliometric analysis of top 100 cited articles in nonalcoholic fatty liver disease research
Tong-Shuo Zhang, Hua-Lei Qin, Tong Wang, Hai-Tao Li, Hai Li, Shi-Hai Xia, Xiao-Hui Xiang, Department of Hepatopancreatobiliary and Splenic Medicine, Affiliated Hospital, Logistics University of People’s Armed Police Force, Tianjin 300162, China
Author contributions: Zhang TS, Qin HL, Wang T, Li HT, Li H and Xiang XH prepared the manuscript; Xia SH and Xiang XH contributed to the conception of this work, revised and approved the manuscript.
Supported by The National Natural Science Foundation of China, No. 81173393; the Natural Science Foundation of Tianjin City, No. 12JCZDJC25500; and the Innovation Team Program from Logistics University of People’s Armed Police Force, No. WHTD201310.
Conflict-of-interest statement: No conflicts of interest, financial or otherwise, are declared by the authors.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See:
Correspondence to: Dr. Xiao-Hui Xiang, Department of Hepatopancreatobiliary and Splenic Medicine, Affiliated Hospital, Logistics University of People’s Armed Police Force, 220 Chenglin Road, Hedong District, Tianjin 300162, China.
Telephone: +86-22-60578765 Fax: +86-22-24370605
Received: June 10, 2016
Peer-review started: June 15, 2016
First decision: July 20, 2016
Revised: August 10, 2016
Accepted: September 21, 2016
Article in press: September 22, 2016
Published online: November 28, 2016


To identify and assess the research situation of top 100 cited articles in nonalcoholic fatty liver disease (NAFLD).


The global scientific research articles in the Science Citation Index-Expanded relevant to NAFLD were retrieved and listed according to their citation times from the most to the least. The 100 most frequently cited original articles were selected to systematically evaluate their bibliometric parameters including times cited, publication year, journals, subject categories, and the highly related concepts of NAFLD, which reflected the history and current situation, publication distribution of leading countries and institutes as well as the research hotspots of NAFLD.


Top 100 cited articles in NAFLD were published from 1965 to 2015 with a citation ranging of 227 to 2151 times since publication, in which the United States was the most predominant country and Mayo Clin was the most productive institution. The majority of the top 100 cited articles were concentrated in SCI subject category of Gastroenterology and Hepatology. Hepatology and Gastroenterology is the top journal that published over half 100 top-cited articles. The significant peak of top cited articles present in the first half of the 2000s while the highest mean number of citation presents in first half of the 1980s. In addition, concepts related to pathology characteristics, epidemiology and medicalization, metabolic syndrome and its combination of symptoms including insulin resistance, biomarkers of lipid metabolism and obesity are listed as the highly related concepts.


The 100 top-cited articles marked with the leading countries, institutions, journals, hotspots and development trend in NAFLD field that could provide the foundation for further investigations.

Key Words: Bibliometrics, Top-cited articles, Metabolic syndrome, Prevalence, Medicalization, Nonalcoholic fatty liver disease

Core tip: Bibliometrics was used to quantitatively analyze top 100 cited articles from the database of the Science Citation Index Expanded to reveal the global publication trends about nonalcoholic fatty liver disease (NAFLD). This study is the first global look at the history and current situation of NAFLD research to assess the performances of leading countries/territories and institutes and research hotspots of this disease. The performances and research hotspots are related to the potential pathogenesis of NAFLD. Incidence and prevalence as well as treatment progress for NAFLD were systematically reviewed, and their relationships with global performances results were also discussed.


Nonalcoholic fatty liver disease (NAFLD) is defined by liver fat deposition with a concentration of hepatic triglycerides exceeding 5% of liver weight in the absence of excessive alcohol intake. NAFLD is an umbrella term used to describe a histological spectrum ranging from simple steatosis to nonalcoholic steatohepatitis (NASH). NASH is virtually indistinguishable histologically from alcoholic steatohepatitis, which is designated the disease with inflammation and liver cell injury in some NAFLD patients[1]. It was thought that hepatic fatty change was a kind of benign lesions previously. However, the recent research showed that about 10%-30% of NAFLD could evolve into NASH, accompanying by fibrosis, cirrhosis, liver failure and even hepatocellular carcinoma[2]. NAFLD patients are more likely to be accompanied with obesity, diabetes, cardiovascular and cerebrovascular diseases to increase death and disability rate. Owing to the high morbidity rate of obesity and metabolic syndrome worldwide, NAFLD has become the leading cause of chronic liver disease[1]. It is time to identify and evaluate the high citation articles to get insight into history and current situation of NAFLD research.

Citation rank list has been often used in medicine to characterize works with the remarkable intellectual influence[3]. Many highly cited articles have stimulated further standard-breaking investigations and discussions[4]. However, the bibliometric analysis of the most influential articles in NAFLD field remains unexploited. As the most frequently used source database for a broad review of scientific value in a specific research field, Science Citation Index-Expanded (SCI-Expanded) from Thomson Reuters is a highly effective research tool for evaluating scientific performance and tracking evolution trends. In this study, bibliometric method was applied to analyze the citation times, publication year, countries and institutes, journals, subspecialty, and key words of the 100 most cited articles in NAFLD field in SCI-Expanded from 1965 to 2015.


The data were obtained from the SCI-Expanded from the Institute for Scientific Information, which indexed 8618 major journals with citation references across 176 categories in science edition in 2015. The keywords for bibliography retrieval in database consisted of “nonalcoholic steatohepatitis”, “nonalcoholic fatty liver disease”, and their heteromorphic form and abbreviation limited in liver or hepatology fields. Papers were listed according to their citation times from the most to the least. Only the top 100 original articles from the most citation list were included for further analysis. The retrieve process of the top 100 citied articles was shown in Figure 1. In detail, the retrieved data for statistical process were imported to Excel 2010. According to JCR in 2014 (available in June 2015), the reported impact factor (IF) of each journal was referred. The 100 top cited articles were assessed by decreasing orders of articles and citation. Bibliometric parameters including publication productions of countries and institutes with five indexes including total, independent, collaborative, first author, and corresponding author articles; distribution of journals and subspecialties; top 10 of most cited articles were assessed.

Figure 1
Figure 1 Flow chart of the selection process for the top 100 cited in nonalcoholic fatty liver disease. NAFLD: Nonalcoholic fatty liver disease.

Furthermore, the most frequent key words and concepts were also discussed. Part of concepts such as “NAFLD” and “NASH” were abandoned since they completely overlap with the study content. Highly related concepts including all concepts from the Gene Ontology (GO) and the Medical Subject Headings (MeSH) were categorized by semantic search technology using GoPubMed® search engine (

Publication year

After screening, 8828 meaningful articles related to NAFLD were retrieved in the period of 1965 to 2015. It can be seen that the number of total articles increased at an exponential rate, which entered an exponential growth phase since 2004 (Figure 2). A power exponential function can describe the growth curve: Y = 1 × 10-233e0.2701x, R2 = 0.9668.

Figure 2
Figure 2 Number of global SCI Journal articles varies with time. Remarks: Fitting equation during 1985-2015 is: Y = 1 × 10-233e0.2701x, R2 = 0.9668. In the equation, Y is the number of accumulation articles and X is the sequence number of year. It indicated that research on NAFLD entered an exponential growth phase since 2004. NAFLD: Nonalcoholic fatty liver disease.

The publication years of the top 100 cited articles in NAFLD field spanned from 1980 to 2012 with a citation ranging from 227 to 2151 times since publication. The majority of top 100 cited articles (74%) were concentrated in the 2000s (Figure 3). The most cited article published by Kleiner DE (National Cancer Institute, United States) in 2005 was cited 2151 times according to the SCI-Expanded database (Table 1).

Table 1 The information of top 100 cited articles in nonalcoholic fatty liver disease.
RankTitle of articleJournalFirst author/instituteYearTimes cited
1Design and validation of a histological scoring system for nonalcoholic fatty liver diseaseHepatologyKleiner DE/NCI, United States20052151
2Nonalcoholic steatohepatitis: A proposal for grading and staging the histological lesionsAm J GastroenterolBrunt EM/Saint Louis University, United States19991609
3Nonalcoholic fatty liver disease: A spectrum of clinical and pathological severityGastroenterologyMatteoni CA/Cleveland Clin Fdn, United States19991506
4Prevalence of hepatic steatosis in an urban population in the United States: Impact of ethnicityHepatologyBrowning JD/Univ Texas, United States20041320
5Non-alcoholic steatohepatitis - Mayo-Clinic experiences with A hitherto unnamed diseaseMayo Clin ProcLudwig J/Mayo Clin, United States19801206
6Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndromeHepatologyMarchesini G/Università di Bologna, Bologna, Italy20031134
7Nonalcoholic fatty liver disease - a feature of the metabolic syndromeDiabetesMarchesini G/Univ Bologna, Italy20011072
8The natural history of nonalcoholic fatty liver disease: A population-based cohort studyGastroenterologyAdams LA/Mayo Clin, United States2005974
9Nonalcoholic steatohepatitis: Association of insulin resistance and mitochondrial abnormalitiesGastroenterologySanyal AJ/Virginia Commonwealth Univ, United States2001935
10The natural-history of nonalcoholic steatohepatitis - a follow-up-study of 42 patients for up to 21 yrHepatologyPowell EE/University of Queensland, Australia1990864
11Independent predictors of liver fibrosis in patients with nonalcoholic steatohepatitisHepatologyAngulo P/Mayo Clin, United States1999802
12Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver diseaseJ Clin InvestDonnelly KL/Univ Minnesota, United States2005801
13Nonalcoholic steatohepatitis - an expanded clinical entityGastroenterologyBacon BR/St. Louis UNIV, United States1994756
14Association of nonalcoholic fatty liver disease with insulin resistanceAm J MedMarchesini G/Univ Bologna, United States1999736
15Long-term follow-up of patients with NAFLD and elevated liver enzymesHepatologyEkstedt M/Linkoping Univ Hosp, Sweden2006719
16Expanding the natural history from cryptogenic cirrhosis to of nonalcoholic steatohepatitis: Hepatocellular carcinomaGastroenterologyBugianesi E/Univ Turin, Italy2002712
17The utility of radiological imaging in nonalcoholic fatty liver diseaseGastroenterologySaadeh S/Inova Fairfax Hosp, United States2002708
18The fat-derived hormone adiponectin alleviates alcoholic and nonalcoholic fatty liver diseases in miceJ Clin InvestXu AM/Univ Auckland, China2003696
19Nonalcoholic fatty liver disease: Predictors of nonalcoholic steatohepatitis and liver fibrosis in the severely obeseGastroenterologyDixon JB/Monash Univ, Australia2001666
20A placebo-controlled trial of pioglitazone in subjects with nonalcoholic steatohepatitisN Engl J MedBelfort R/Univ Texas, Italy2006662
21Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver diseaseNature GenetRomeo S/Univ Texas, United States2008614
22NASH and insulin resistance: Insulin hypersecretion and specific association with the insulin resistance syndromeHepatologyChitturi S/Univ Sydney, Australia2002610
23Sampling variability of liver biopsy in nonalcoholic fatty liver diseaseGastroenterologyRatziu V/Grp Hosp Pitie Salpetriere, France2005572
24Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal menJ Clin Endocrinol MetabSeppala-Lindroos A/Univ Helsinki, Finland2002563
25Beyond insulin resistance in NASH: TNF-alpha or adiponectin?HepatologyHui JM/Westmead Hosp, Australia2004552
26Magnetic resonance spectroscopy to measure hepatic triglyceride content: Prevalence of hepatic steatosis in the general populationAm J Physiol -Endocrinol MetabSzczepaniak, LS/Univ Texas, United States2005551
27Pioglitazone, Vitamin E or Placebo for Nonalcoholic SteatohepatitisN Engl J MedSanyal AJ/Virginia Commonwealth Univ, United States2010550
28The natural history of nonalcoholic fatty liver: A follow-up studyHepatologyTeli MR/Univ Newcastle, United Kingdom1995544
29Mechanism of hepatic insulin resistance in non-alcoholic fatty liver diseaseJ. Biol. Chem.Samuel VT/Yale Univ, Australia2004537
30Obesity increases sensitivity to endotoxin liver injury: Implications for the pathogenesis of steatohepatitisProc Natl Acad Sci USAYang SQ/Johns Hopkins Univ, United States1997504
31Prevalence of fatty liver in children and adolescentsPediatricsSchwimmer JB/Univ Calif San Diego, United States2006454
32Diabetes increases the risk of chronic liver disease and hepatocellular carcinomaGastroenterologyEl-Serag HB/Houston Dept Vet Affairs Med Ctr, United States2004452
33Hepatocyte apoptosis and Fas expression are prominent features of human nonalcoholic steatohepatitisGastroenterologyFeldstein AE/Mayo Clin, United States2003451
34Prevalence of and risk factors for nonalcoholic fatty liver disease: The Dionysos Nutrition and Liver StudyHepatologyBedogni G/Fondo Studio Malattie Fegato ONLUS, Italy2005449
35CYP2E1 and CYP4A as microsomal catalysts of lipid peroxides in murine nonalcoholic steatohepatitisJ Clin InvestLeclercq IA/Univ Sydney, United States2000435
36Probiotics and antibodies to TNF inhibit inflammatory activity and improve nonalcoholic fatty liver diseaseHepatologyLi ZP/Johns Hopkins Univ, United States2003433
37Increased hepatic iron concentration in nonalcoholic steatohepatitis is associated with increased fibrosisGastroenterologyGeorge DK/Royal Brisbane Hosp, Australia1998431
38Clinical and histologic spectrum of nonalcoholic fatty liver disease associated with normal ALT valuesHepatologyMofrad P/Virginia Commonwealth Univ, U United States2003427
39The NAFLD fibrosis score: A noninvasive system that identifies liver fibrosis in patients with NAFLDHepatologyAngulo P/Mayo Clin, United Kingdom2007425
40A pilot study of ploglitazone treatment for nonalcoholic steatohepatitisHepatologyPromrat K/NIDDK, United States2004410
41Improved nonalcoholic steatohepatitis after 48 wk of treatment with the PPAR-gamma ligand rosiglitazoneHepatologyNeuschwander-Tetri BA/St. Louis Univ, United States2003406
42Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesityNatureHenao-Mejia J/Yale Univ, United States2012399
43Liver pathology and the metabolic syndrome X in severe obesityJ Clin Endocrinol MetabMarceau P/SUNY Hlth Sci Ctr, Canada1999389
44The metabolic syndrome as a predictor of nonalcoholic fatty liver diseaseAnn Intern MedHamaguchi M/Asahi Univ, Japan2005387
45Metformin in non-alcoholic steatohepatitisLancetMarchesini G/Univ Bologna, Italy2001376
46Nonalcoholic steatohepatitis, insulin resistance, and metabolic syndrome: Further evidence for an etiologic associationHepatologyPagano G/Univ Turin, Italy2002373
47Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant miceProc Natl Acad Sci USADumas ME/Univ London Imperial Coll Sci Technol & Med, United Kingdom2006361
48Hepatic cytochrome p450 2E1 is increased in patients with nonalcoholic steatohepatitisHepatologyWeltman MD/Westmead Hosp, Sweden1998355
49The histological course of nonalcoholic fatty liver disease: A longitudinal study of 103 patients with sequential liver biopsiesJ HepatolAdams LA/Mayo Clin, United States2005349
50Nonalcoholic steatohepatitis - A study of 49 patientsHum PatholLee RG/Oregon Health Sciences University, United States1989346
51Prevalence of Nonalcoholic Fatty Liver Disease and Nonalcoholic Steatohepatitis Among a Largely Middle-Aged Population Utilizing Ultrasound and Liver Biopsy: A Prospective StudyGastroenterologyWilliams CD/Brooke Army Med Ctr, United States2011343
52Free fatty acids promote hepatic lipotoxicity by stimulating TNF-alpha expression via a lysosomal pathwayHepatologyFeldstein AE/Mayo Clin, United States2004336
53In vivo assessment of liver cell apoptosis as a novel biomarker of disease severity in nonalcoholic fatty liver diseaseHepatologyWieckowska A/Cleveland Clin Fdn, United States2006330
54Therapeutic effects of restricted diet and exercise in obese patients with fatty liverJ HepatolUeno T/Kurume University School of Medicine, Japan1997329
55Gene expression of tumor necrosis factor alpha and TNF-receptors, p55 and p75, in nonalcoholic steatohepatitis patientsHepatologyCrespo J/Hosp Univ Marques Valdecilla, Spain2001327
56Inhibiting triglyceride synthesis improves hepatic steatosis but exacerbates liver damage and fibrosis in obese mice with nonalcoholic steatohepatitisHepatologyYamaguchi K/Duke Univ, United States2007324
57Nonalcoholic fatty liver disease: Improvement in liver histological analysis with weight lossHepatologyDixon JB/Monash Univ, Australia2004324
58The role of small intestinal bacterial overgrowth, intestinal permeability, endotoxaemia, and tumour necrosis factor alpha in the pathogenesis of non-alcoholic steatohepatitisGutWigg AJ/Queen Elizabeth Hosp, Australia2001324
59Intrahepatic fat, not visceral fat, is linked with metabolic complications of obesityProc Natl Acad Sci USAFabbrini E/Washington Univ, Greece2009323
60Ursodeoxycholic acid or clofibrate in the treatment of non-alcohol-induced steatohepatitis: A pilot studyHepatologyLaurin J/Mayo Clin, United States1996317
61Vitamin E treatment of nonalcoholic steatohepatitis in children: A pilot studyJ PediatrLavine JE/Univ Calif San Diego, United States2000312
62A randomized controlled trial of metformin vs vitamin E or prescriptive diet in nonalcoholic fatty liver diseaseAm J GastroenterolBugianesi E/Univ Bologna, Italy2005309
63Ursodeoxycholic acid for treatment of nonalcoholic steatohepatitis: Results of a randomized trialHepatologyLindor KD/Mayo Clin, Canada2004305
64Deletion of NEMO/IKK gamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinomaCancer CellLuedde T/Univ Cologne, Belgium2007285
65NAFLD may be a common underlying liver disease in patients with hepatocellular carcinoma in the United StatesHepatologyMarrero JA/Univ Michigan, United States2002283
66Vitamin E and vitamin C treatment improves fibrosis in patients with nonalcoholic steatohepatitisAm J GastroenterolHarrison SA/Univ Texas, United States2003281
67High glucose and hyperinsulinemia stimulate connective tissue growth factor expression: A potential mechanism involved in progression to fibrosis in nonalcoholic steatohepatitisHepatologyParadis V/Hop Bicetre, France2001281
68Prevalence of obesity and diabetes in patients with cryptogenic cirrhosis: A case-control studyHepatologyPoonawala A/Johns Hopkins Univ, United States2000281
69Insulin resistance-associated hepatic iron overloadGastroenterologyMendler MH/Hop Pontchaillou, France1999281
70Free fatty acids induce JNK-dependent hepatocyte lipoapoptosisJ Biol ChemMalhi H/Mayo Clin, United States2006280
71Dietary habits and their relations to insulin resistance and postprandial lipemia in nonalcoholic steatohepatitisHepatologyMusso G/Univ Turin, Italy2003279
72Cytokines and NASH: A pilot study of the effects of lifestyle modification and vitamin EHepatologyKugelmas M/Univ Louisville, United States2003275
73Nonalcoholic fatty liver disease and risk of future cardiovascular events among type 2 diabetic patientsDiabetesTargher G/Osped Sacro Cuore don G Calabria, Italy2005271
74A lipidomic analysis of nonalcoholic fatty liver diseaseHepatologyPuri P/Virginia Commonwealth Univ, United States2007269
75The Incidence and Risk Factors of Hepatocellular Carcinoma in Patients with Nonalcoholic SteatohepatitisHepatologyAscha MS/Cleveland Clin, United States2010268
76Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patientsDiabetes CareTargher G/Osped Sacro Cuore don Calabria, United Kingdom2007268
77Burden of liver disease in the United States: Summary of a workshopHepatologyKim WR/Mayo Clin, United States2002266
78Plasma Endotoxin Concentrations In Patients With Alcoholic And Nonalcoholic Liver-Disease - Reevaluation With An Improved Chromogenic AssayJ HepatolFukui H/ROBERT BOSCH KRANKENHAUS, Germany1991264
79Histopathology of pediatric nonalcoholic fatty liver diseaseHepatologySchwinnner JB/Univ Calif San Diego, USA2005262
80A position statement on NAFLD/NASH based on the EASL 2009 special conferenceJ HepatolRatziu V/Azienda USL Modena, Italy2010259
81Increased intestinal permeability in obese mice: New evidence in the pathogenesis of nonalcoholic steatohepatitisAm J Physiol-Gastroint Liver PhysiolBrun P/Univ Padua, Italy2007258
82Endothelial dysfunction and cardiovascular risk profile in nonalcoholic fatty liver diseaseHepatologyVillanova N/Alma Mater Studiorum Univ Bologna, Italy2005258
83Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitisHepatologyPerez-Carreras M/Hosp Univ 12 Octubre, Spain2003254
84Survival, liver failure, and hepatocellular carcinoma in obesity-related cryptogenic cirrhosisHepatologyRatziu V/Hop La Pitie Salpetriere, France2002254
85A pilot study of a thiazolidinedione, troglitazone, in nonalcoholic steatohepatitisAm J GastroenterolCaldwell SH/Univ Virginia, United States2001247
86Hepatocyte-specific Pten deficiency results in steatohepatitis and hepatocellular carcinomasJ Clin InvestHorie Y/Akita Univ, Japan2004240
87Randomized Controlled Trial Testing the Effects of Weight Loss on Nonalcoholic SteatohepatitisHepatologyPromrat K/Brown Univ, United States2010239
88Insulin resistance in chronic hepatitis C: Association with genotypes 1 and 4, serum HCV RNA level, and liver fibrosisGastroenterologyMoucari R/Hop Beaujon, France2008239
89Betaine, a promising new agent for patients with nonalcoholic steatohepatitis: Results of a pilot studyAm J GastroenterolAbdelmalek MF/Mayo Clin, United States2001239
90Steatosis in chronic hepatitis C: Relative contributions of obesity, diabetes mellitus, and alcoholHepatologyMonto A/Univ Calif San Francisco, United States2002237
91Therapeutic efficacy of an angiotensin II receptor antagonist in patients with nonalcoholic steatohepatitisHepatologyYokohama S/Dokkyo Univ, Japan2004235
92Hepatic-Effects Of Dietary Weight-Loss In Morbidly Obese SubjectsJ HepatolAndersen T/Univ Copenhagen, Denmark1991236
93Rosiglitazone for nonalcoholic steatohepatitis: One-year results of the randomized placebo-controlled fatty liver improvement with rosiglitazone therapy trialGastroenterologyRatziu V/Univ Paris, France2008234
94Diagnosis of Fibrosis and Cirrhosis Using Liver Stiffness Measurement in Nonalcoholic Fatty Liver DiseaseHepatologyWong VWS/Hop Haut Leveque, China2010232
95Increased hepatocyte CYP2E1 expression in a rat nutritional model of hepatic steatosis with inflammationGastroenterologyWeltman MD/Univ Sydney, Australia1996230
96Effect of steatohepatitis associated with irinotecan or oxaliplatin pretreatment on resectability of hepatic colorectal metastasesJ Am Coll SurgFernandez FG/Washington Univ, United States2005229
97Adiponectin and its receptors in non-alcoholic steatohepatitisGutKaser S/Univ Innsbruck Hosp, Spain2005229
98Long-term outcomes of cirrhosis in nonalcoholic steatohepatitis compared with hepatitis CHepatologyHui JM/Univ Sydney, Australia2003229
99Noninvasive markers of fibrosis in nonalcoholic fatty liver disease: Validating the European liver fibrosis panel and exploring simple markersHepatologyGuha IN/Guha, United Kingdom2008228
100Plasma adiponectin in nonalcoholic fatty liver is related to hepatic insulin resistance and hepatic fat content, not to liver disease severityJ Clin Endocrinol MetabBugianesi E/Univ Turin, Italy2005227
Figure 3
Figure 3 Number of the top 100 cited papers in nonalcoholic fatty liver disease per five year and the mean of the citation of the top cited paper with five years bin.
Publication distribution of countries and institutes

The top 100 cited articles were originated from 19 countries. The most productive country was the United States (55), followed sequentially by Italy (20), Australia (14), France (9), United Kingdom (7). The rest of the countries had less than four publications (Table 2). The numbers in the brackets refer to the publication number (similarly hereinafter).

Table 2 Countries of origin of the top 100 articles in nonalcoholic fatty liver disease.
1United States554845104926975
5United Kingdom752521826
16New Zealand100110
18South Africa100100

Twelve institutions published more than 4 top cited articles. Mayo Clin (12) ranked the first place in NAFLD research, followed by University of Bologna (9), University of Turin (9), The University of Sydney (7) and University of California, San Diego (6). And the rest of the Institutes such as University of Texas, Saint Louis University and Virginia Commonwealth University contributed five each to the top 100 cited articles (Table 3).

Table 3 Top productive institutions list with top 100 cited articles in nonalcoholic fatty liver disease.
1Mayo Clinic121284115950
2University of Bologna951853627
2University of Turin941841591
4The University of Sydney741621504
5University of California, San Diego630631028
6University of Texas551443428
7Saint Louis University533232771
8Virginia Commonwealth University542322181
9Westmead Hospital42043907
10Washington University42041552
11University of Paris41041234
12University of California, San Francisco41130237
13National Cancer Institute410412151
14MetroHealth Medical Center400400
Subspecialties and journals

According to the JCR in 2014, the top 100 articles of NAFLD were scattered in 13 SCI subject categories (Table 4). These main subspecialties were Gastroenterology and Hepatology (71), Endocrinology and Metabolism (7), General and Internal Medicine (6), Research and Experimental Medicine (4) and Science and Technology (4).

Table 4 Most frequent subspecialties with the top 100 cited articles in nonalcoholic fatty liver disease.
RankSubject categoriesNo. of articlesTotal citation
1Gastroenterology and Hepatology7133290
2Endocrinology and Metabolism73341
3General and Internal Medicine63917
4Research and Experimental Medicine42172
5Science and Technology41587
6Biochemistry and Molecular Biology2817
9Genetics and Heredity1614
11Cell Biology1285

The top 100 articles were distributed in 25 journals including professional journals and other disciplines journals. Eleven (44%) journals published 2 or more articles (Table 5), among which the most productive journal was Hepatology (42), followed by Gastroenterology (16), Am J Gastroenterol (5), J Hepatol (5), J Clin Invest (4), Proc Natl Acad Sci USA (3) and J Clin Endocrinol Metab (3).

Table 5 Journal distribution of top 100 cited articles in nonalcoholic fatty liver disease.
RankJournalNo. of articlesTotal citationImpact factor (2014)
3Am J Gastroenterol5268510.755
3J Hepatol5143711.336
5J Clin Invest4217213.215
6Proc Natl Acad Sci USA311889.674
7J Clin Endocrinol Metab311793.457
9New Engl J Med2121255.873
10J Biol Chem28174.573
The most frequently cited articles

As elaboration of all the top 100 cited articles is difficult, the top 10 citation articles were further discussed instead. United States (7), Italy (2) and Australia (1) respectively published the top 10 most frequently cited articles (Table 1). Three in ten focused on epidemiological subjects to investigate the regional and ethnic differences and explore the genetic mechanism implied in NAFLD, which were published respectively in the year of 1990 (864 citations), 2004 (1320 citations) and 2005 (974 citations) (Table 1). Other three articles discussed the pathogenic role of metabolic syndrome where insulin resistance and obesity were repeatedly mentioned. The rest of articles analyzed NAFLD from the clinical and histological aspect, among which two were about the histological grading and staging of NAFLD.

Highly related concepts

Highly related concepts of the top 100 cited papers from GO and MeSH with frequency more than 10 times were listed in Table 6. The analysis indicated that multisystem metabolic syndrome and its related key words (obesity, insulin resistance, etc.) occupied a majority of proportion. Some key words discussed histological and pathology characteristics of NAFLD including hepatic steatosis, fibrosis, biopsies, etc. Noteworthy, the topic of epidemiology covering prevalence, male/men, female/women, middle aged and adolescent was also involved in frequent concepts (Table 7).

Table 6 High frequency key words in the top 100 cited articles in nonalcoholic fatty liver disease (frequency > 2).
RankKey wordFrequency
1Hepatic steatosis4
4Metabolic syndrome2
4Insulin resistance2
4Intestinal bacteria2
Table 7 Highly related concepts of the top 100 articles in nonalcoholic fatty liver disease categorized by GoPubMed® search engine.
RankHighly related conceptsFrequencyRankHighly related conceptsFrequency
1Fatty liver9724Wounds and injuries15
2Male9125Aspartate Aminotransferases14
4Female8427Carcinoma, Hepatocellular13
5Middle aged7228Tumor necrosis factor-alpha12
6Patients7129Multivariate analysis12
7Fibrosis5930Prospective studies12
8Biopsy4531Follow-up studies12
9Liver4532Hepatitis C11
10Obesity4233cell killing11
13Serum3236Metabolic syndrome X10
14Body mass index3137Fatty acids, nonesterified10
15Syndrome2538Aspartic acid10
16Risk Factors2439Hypoglycemic agents10
17Alanine transaminase2340Homeostasis10
18Alanine transaminase activity1941Severity of illness index10
20Prevalence1843Personal autonomy10

This paper used bibliometrics method to evaluate top 100 cited articles to reveal the global publication performance of NAFLD. The high citation articles can reflect the development evolution direction and scientific level in the NADLD research field to a certain extent.

Publication trends and distribution of NAFLD-related literature

In recent five decades, exponential increase of published articles reflects the globally development trend of NAFLD. In line with the increased prevalence of obesity, diabetes, and hyperlipemia, NAFLD has been increasing worldwide over recent half century[5]. As a result of modern sedentary and over-nutrition lifestyle which makes a very large population fall risk of NAFLD, research on NAFLD would develop more rapidly in the near future[6].

East Asian countries/territories such as Japan, China (mainland), South Korea and Taiwan occupied an important place in NAFLD research and their importance tended to be more and more obvious. This might owe to the rising prevalence of NAFLD in Asia recently as well as the growth of economic power and the advance of scientific research which prompted these countries/territories to invest more in research to prevent and control NAFLD[6]. A global scientific review covered total articles relevant to NAFLD from 1986 to 2013 were performed to analyze distribution of publication number and found that Japan, China (mainland) and South Korea ranked second, fourth and ninth respectively among the most productive country/territories[7]. However, only six of top 100 cited papers originate these countries/territories. It shows that the quality and influence of research in NAFLD need to improve for East Asian countries.

It was found that most of the 100 most cited papers were published in 2000s (74 articles), while the most of high citation times per articles distributed in 1990s. These distributions suggested that the older paper had the more citation times[8]. The opinions in 1990s and 2000s were neither too old to be outdated nor too nearly to be cited. Actually, academic community has recognized that the real importance and influence of a work often can’t be precisely assessed for at least 2 decades after it is published[9].

The research hotspots of NAFLD

Highly related concepts and top keywords could partly reflect the profile of hotspots in NAFLD research. GoPubMed® search engine connect text (abstracts from the MEDLINE database) to background knowledge in the form of semantic networks of concept categories, which is done by meaning and not by keywords only. These results are approximately consistent with our contemporaneous bibliometric analysis in high frequency keywords that covered total articles relevant to NAFLD[7].

Potential pathogenesis: According to highly related concepts list, a cluster of pathogenesis related keywords occupied a majority of high frequency words mentioned by NAFLD researches. The research hotspots extracted using bibliometrics analysis informs the underlying pathogenesis of NAFLD. The results indicated that multisystem metabolic syndrome and its combination of symptoms including insulin resistance, obesity as well as oxidative stress and dyslipoproteinemia played a vital role in the pathogenesis of NAFLD. In fact, although pathogenesis of NAFLD remains elusive, the severity of NAFLD seems to increase in parallel with the features of metabolic syndrome[10-12]. NAFLD/NASH is increasingly regarded as a hepatic manifestation of metabolic syndrome. However, considering that not all patients with NAFLD/NASH suffer from one of these conditions[1], still uncertain pathogenesis of NAFLD might hinder the people and needs to be explored[13].

Epidemic studies: Concepts related to epidemiology such as humans, male/men, female/women, middle aged and adolescent make up another high frequency concepts cluster, which might be closely involved in the accelerating incidence of this disease. The morbidity rate of NAFLD has doubled during last 20 years, whereas the morbidity rate of other chronic liver diseases has remained stable or even decreased. Epidemic investigations of NAFLD primarily focus on human genetic and metabolic studies[14]. Several epidemiological investigations such as case series, familial and twin studies have widely revealed the function of heritability[15]. Noteworthy, in comparison to high-risk population of NAFLD clustering around middle-aged and elderly adults before, younger age trend has gradually shown especially in Asian countries during the last two decades. Following the epidemics of childhood obesity, NAFLD as the most common form of chronic liver disease in adolescents has become a reality[16].

Medicalization progress: Medicalization is also a high frequency concepts cluster. Lack of uniformed diagnosis regulation and no established therapy remains a hindrance to be broken through in this field. NASH is characterized by hepatocellular damage, lobular necroinflammation and fibrogenesis. The early diagnosis of advanced fibrosis in NAFLD is therefore crucial[17,18]. The liver biopsy remains the most reliable diagnostic method to appropriately evaluate the severity of liver fibrosis. Facing to limitations of this invasive technique in current use, a number of experimental biomarkers have been developed in order to predict the degree of liver fibrosis[19]. Moreover, as a promising method for evaluation of patients with NAFLD, nuclear medicine through liver scintigraphy has recently been proposed[20].

Preventing existing comorbidities such as metabolic disorders, cardiovascular or cerebrovascular events are the primary target for NAFLD treatment, while the secondary goal of NAFLD therapy is reversal of hepatic steatosis[21-23]. Lifestyle modification such as weight loss and balanced diet remains the main way of management in NAFLD/NASH. In addition, the benefit of nutritional supplementation on disease progression has attracted growing interest[24]. Most recent data has evidenced the effects of nutrients and dietary bioactive compounds intake (i.e., long-chain PUFA, Vitamin E, Vitamin D, minerals and polyphenols) on the modulation of molecular mechanisms leading to fat accumulation, oxidative stress, inflammation and liver fibrosis in NAFLD patients[25]. In the field of pharmaceutical therapies, a wide range of drugs have been applied in clinical trials, including antioxidants, lipid lowering agents, and rennin-angiotensin system blockers[26-28]. Up to the present, lifestyle modification is the main clinical recommendation as an initial step. Although promising results have shown that long-term insulin sensitizers such as metformin, rosiglitazone, and thiazolidinediones are effective in NAFLD therapy, there are no approved drugs[29-31].

In conclusion, it is important to acknowledge the top 100 cited articles because they marked with the leading countries, institutions, journals, hotspots, past and current trends in NAFLD field that could provide the foundation for further investigations. Highly related concepts of the top 100 cited papers in NAFLD suggest that pathogenesis mainly related to metabolic syndrome, epidemiology, and medicalization including diagnosis and treatment are attracting ever-growing attention.


We would like to thank Professor Yuh-Shan Ho from Asia University and Hui-Min Guo, PhD, from Logistics University of People’s Armed Police Force for their comments on drafting and polishing the manuscript.


Due to the increasing prevalence of obesity and metabolic syndrome worldwide, nonalcoholic fatty liver disease (NAFLD) becomes the leading cause of chronic liver disease. The rapid growth of NAFLD research recently drives top cited articles in the field to be identified and bibliometric analysis to assess the history and current situation, publication distribution of leading countries and institutes as well as the research hotspots of NAFLD.

Research frontiers

A systematic review in 2015 covered total articles relevant to NAFLD from Science Citation Index-Expanded (SCI-Expanded) showed article amount has appeared to geometric growth in recent decades. However, bibliometric result from total articles is not sufficient to indicate the evolution and direction in NAFLD research. The citation times by other authors has been used as a measurable comparison to evaluate the academic impact of an article in its subject field. To date, there have no top cited articles analysis were carried out in NAFLD field.

Innovations and breakthroughs

This paper summarized the current findings from the analysis of the top 100 cited articles in NAFLD field. It is the first global look at the history and current situation of NAFLD research to assess the performances of leading countries/territories and institutes and research hotspots of this disease. In terms of the number of published 100 top-cited articles in NAFLD, United States was the most predominant country and Mayo Clin was the most productive institution. Highly related concepts of the top 100 cited papers in NAFLD suggest that pathogenesis (mainly related to metabolic syndrome), epidemiology, and medicalization (including diagnosis and treatment) are attracting ever-growing attention.


Top 100 cited articles marked with the leading countries, institutions, journals, hotspots, past and current trends in NAFLD field that could provide the foundation for further investigations. Medical bibliometric analysis on top 100 cited articles is expected to provide a reference for the researchers to get involved in NAFLD area.


The articles involved in bibliometric analysis were collected based on online version of SCI-Expanded from Thomson Reuters. Keywords for bibliography retrieval in database consisted of “nonalcoholic steatohepatitis” and “nonalcoholic fatty liver disease”.


This study retrieved the top 100 cited articles in the field of NAFLD and determined the country of origin, peak of highly-cited articles and international collaborations. The present study is very interesting on a high prevalent chronic liver disease.


Manuscript source: Invited manuscript

Specialty type: Gastroenterology and hepatology

Country of origin: China

Peer-review report classification

Grade A (Excellent): A

Grade B (Very good): B

Grade C (Good): 0

Grade D (Fair): D

Grade E (Poor): 0

P- Reviewer: Clouston AD, Mendez-Sanchez N, Streba LA S- Editor: Gong ZM L- Editor: A E- Editor: Li D

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