Global scientific trends on aflatoxin research during 1998–2017: a bibliometric and visualized study

Aflatoxins are toxic secondary metabolites, affected by fungal species, of Aspergillus molds that are largely distributed in nature and have contaminated the food supplies of animals and humans, resulting in serious health hazards and even death [1, 2]. Additional health impacts of aflatoxins include hepatotoxicity, teratogenicity, genotoxicity, and cytotoxicity [3]. It has been estimated about 5 billion people globally are particularly affected by exposed to dietary aflatoxins [4]. Tropical and subtropical areas of the world are the highest areas for aflatoxin contamination of the food products, where food storage conditions for cereals (e.g. maize and peanuts), spices, and milk are suboptimal [4, 5, 6].

Bibliometrics and evaluation of research performance have been carried out on a wide range of health topics [7, 8, 9, 10, 11, 12, 13, 14, 15], and several have been carried out in the fields of environmental studies [16, 17], and toxicology [18, 19, 20, 21, 22, 23, 24]. Yet, to the best of my knowledge, only a few bibliometric studies in food contamination have been done recently [25, 26, 27, 28], and only one bibliometric study explicitly focused on aflatoxin has been published by using Web of Science (WoS) database for data collection [28]. Because the aflatoxin bibliometric study [28] found that aflatoxin research is now being given increased scientific attention internationally, it is therefore necessary to thoroughly evaluate and classify the existing literature from different aspects, including the countries/region of origin, journals, authors, institutes, citations, and content analysis to discover any hot and emerging topics using a large and comprehensive database. Therefore, the aim of this study is to evaluate the global scientific output of research of aflatoxin by using bibliometric techniques, and flag areas of concern.

Identifying the most productive and influential research, can be useful to anyone involved on the field of aflatoxin. Drawing on these insights may aid understanding of historical progress in aflatoxin research over the last 20 years and offer guidance researchers, and policy makers, regarding best scientific and publishing practices for future health research of this scientific field.

The search engine of the Scopus database found 18,342 documents published in the field of aflatoxin from 1963 to 2018 (Additional file 1). The first publications appeared in 1963 [41, 42, 43]. After this, the number of publications grew gradually and slowly each year, with little fluctuation (Additional file 1). Of them, 9845 documents published in the field of aflatoxin from 1998 to 2017. Within this batch, this study juggled 8288 articles, 687 reviews, and 870 other types of documents, including letters, article end notes, editorials, and minutes of meetings. Figure 1 shows the publication trend related to aflatoxin from 1998 to 2017. The results reveal that the number of annual publications had gradually increased during 1998–2004, indicating that research output showed steady growth during those years. Prominently, the number of relevant publications increased sharply since 2004; meanwhile, 2017 netted the largest haul of aflatoxin research (850 documents published). The data indicates indeed that issues related to aflatoxin are becoming increasingly important in the investigation of food safety and human health. English is the predominant language of publications on aflatoxin, constituting 93.8% of the total, with only 6.2% of the publications in another language. The most common non-English language is Chinese, which constitutes 2.1% of the total, followed by Portuguese (0.8%). The reason for this finding is that Scopus has a better coverage of English language journal than those in other languages [44]. A previously published study on aflatoxin [28] had shown different results (5122 documents worldwide from 1963 to 2016) from those presented in the current study. The difference was due to (1) different databases used to retrieve the documents and (2) research domains being investigated. The study by Klingelhöfer et al. [28] was conducted using WoS and was limited to biomedical research areas. In the current study, Scopus database was used without limiting the results to any particular research area.

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Among the top 10 countries, five (i.e. India, Iran, Brazil, Turkey, and Egypt) were developing countries as defined by the United Nations, which suggests that each perceive this issue as a serious problem. Among this grouping, there was international diversity not associated with the traditional researching nations’ scientific productivity ranking [18, 34, 35, 36, 54, 55, 56]. The current data verified that Turkey, Egypt and Iran have been the main research contributors from the Middle Eastern countries. Consecutive outbreaks of acute aflatoxicosis in developing countries [4, 6, 57] (specifically, Turkey [58, 59], Iran [60], India [61, 62, 63, 64], Brazil [51, 65], and Egypt [66]) caused exceptionally large morbidity and mortality connected with such outbreaks [1, 67, 68, 69], and this may explain why more research has emphasized on aflatoxin since that time [28].

Analysis of international collaborations (i.e., link strength) showed that the United States had the highest number of collaborators (n = 87) followed by the United Kingdom (n = 63), and Italy (n = 54) (Fig. 2 and Table 1). The h-index, or Hirsch index, has been demonstrated for each country in Table 1, and it is a measure that combines both the productivity (number of publications) and their citations (perceived as an index of research quality) [70].

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Figure 3 illustrates the network visualization map for author collaboration, showing 149 authors with more than 20 documents published. Approximately 23,224 unique authors participated in publishing the retrieved publications, an average of 2.36 authors per publication. D. Bhatnagar was the most active author with 118 publications. The top 10 journals that published on this topic are listed in Table 2. Food Control published the highest number of articles (384, 3.90%), followed by Food and Chemical Toxicology (158, 1.60%) and Toxins (158, 1.60%). The top 10 journals with the greatest contribution to aflatoxin research accounted for 16.70% of all publications included in this study.

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Table 2

Most influential journals publishing aflatoxin research

Rankinga	Journal	Number of publications (%)	IFb	SNIPc
1st	Food Control	384 (3.90)	4.248	1.731
2nd	Food and Chemical Toxicology	158 (1.60)	3.775	1.277
2nd	Toxins	158 (1.60)	3.895	1.245
4th	Mycotoxin Research	151 (1.53)	3.741	1.187
5th	Food Additives and Contaminants: Part A	146 (1.48)	2.170	0.909
5th	International Journal of Food Microbiology	146 (1.48)	4.006	1.556
7th	Journal of Agricultural and Food Chemistry	143 (1.45)	3.571	1.321
8th	World Mycotoxin Journal	140 (1.42)	2.406	0.840
9th	Journal of Food Protection	115 (1.17)	1.559	0.744
10th	Food Additives and Contaminantsd	103 (1.05)	NA	1.355

SNIP Source Normalized Impact per Paper, IF Impact factor, NA Not available

^aEqual journals have the same ranking number, and then a gap is left in the ranking numbers

^bImpact factors (IF) based on Journal Citation Reports (JCR) 2018 from Clarivate Analytics

^cSNIP based on Scopus data which was freely available at www.scopus.com/sources

^dContinued as: Food Additives & Contaminants: Part A (2008 - current), and Food Additives & Contaminants: Part B: Surveillance (2008 - current)

The network visualisation term map for aflatoxin research undertaken globally over the 20-year period from 1998 to 2017 is shown in Fig. 4a. One hundred twenty-eight thousand four hundred twenty different terms were found from the collected publications; however, only 1243 of them appeared more than 40 times. In the term map (Fig. 4a), four thematic research clusters or areas can be noticed, consisting of 1243 co-occurring terms categorising the aflatoxin research field with different four colors. The terms with similarity in research topics are grouped together and the 4 clusters were analyzed as follows:

• Cluster 1 (in red color): this cluster mainly includes the terms related to the topic of detection and quantification of aflatoxin, such as “sample”, “detection”, “solution”; “validation”, “antibody”, “quantification”, “immune sensor”, and “column”.

• Cluster 2 (in blue color): this cluster mainly includes the terms related to the topic of sources and biosynthesis of aflatoxin, such as “Aspergillus flavus”, “A. flavus”, “spore”, harvest”, “fungus”, “mycotoxin contamination”, and “biosynthesis”.

• Cluster 3 (in yellow color): this cluster mainly includes the terms related to the topic of health effects by aflatoxin, such as “hepatocellular carcinoma”, “disease”, “effect”, “gene”, and “biomarker”.

• Cluster 4 (in green color): this cluster mainly includes the terms related to the topic of detoxification and care regarding aflatoxin, such as “treatment”, “administration”, “diet”, glutathione” and “induction”.

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The color of terms was coded by VOSviewer, based on the average time they appeared in the 9845 related publications (Fig. 4b). The blue color indicates the keyword appeared early and red indicates the keywords appeared later. Before 2010, namely in the early stage of research, most aflatoxins’ studies focused on terms related to the topics of “sources and biosynthesis of aflatoxin”, “health effects by aflatoxin”, and “detoxification and treatment of aflatoxin”. The latest trends showed that the terms related to the topic of detection and quantification of aflatoxin would be of concern widely in the future.

One clear theme to emerge from the findings is that the most top-cited aflatoxin publications emphasised the diversity of sub-topics similar to the research hotspots from co-occurring terms including “health effects by aflatoxin” [5, 71, 72, 75, 77, 78, 80, 84, 85, 86, 87], “sources and biosynthesis of aflatoxin” [76, 81, 82, 89], “detoxification and treatment of aflatoxin” [74, 79, 88], and “detection and quantification of aflatoxin” [73, 83].

This study utilizes a bibliometric approach to analyze the current status and trend of development of aflatoxin research. But there were a few limitations within which are similar to previous studies. First, the current study was limited by the use of the search term “aflatoxin” in title and/or abstract search only. Particularly, any publications that used “aflatoxin” as a keyword or inside of the publication may have been missed in this analysis. However, if such false-negative results did exist, they will have little effect on the overall findings [7, 35, 38, 39]. Second, it surveyed just the publications in the Scopus database. Although Scopus is the most frequently used and trusted search engine, a few outlier publications might not have been included. Despite that, the current bibliometric study characterises the first concise analysis of the global publications related to aflatoxin by using Scopus and VOSviewer© and illustrates the benefits of bibliometric analysis for assessing research productivity in the field of aflatoxin in a standardised way. Third, the standardization of author names, and terms were completed based on findings on the VOSviewer© and may not be accurate because in certain cases, some authors might have different name spelling or more than one name. This might generate inaccurate research output for these authors. Despite these limitations, this study provides a relatively solid global view on aflatoxin research from these recent two decades.

The main purpose of this study was to present an overview on the past, present and future scientific research directions of the research field of aflatoxin by combining a bibliometric analysis with a literature review. The quantity of global research output on aflatoxin has substantially increased over the past 20 years, accounting for more than 9800 publications on relevant journals. In earlier years, researchers focused on terms related to the topics of “sources and biosynthesis of aflatoxin”, “health effects by aflatoxin”, and “detoxification and treatment of aflatoxin”. In recent years, researchers paying more attention to the topic of detection and quantification of aflatoxin would be concerned widely with the future. The USA was the largest contributor to aflatoxin scientific research and had the leading position in global research in this field, followed by China. Quite different from other research domains, some developing economies such as India, Iran, Brazil, Turkey, and Egypt were also among the largest contributors. This bibliometric analysis should be of interest to all governmental decisions, healthcare, industries, and educational institutions, involved in the ongoing advances in aflatoxin biosynthesis, better allocation of monitoring efforts, and improved management procedures.