key: cord-0977285-bswt77zi
authors: Wu, Rao; Yakhkeshi, Saeed; Zhang, Xiaoying
title: Scientometric analysis and perspective of IgY technology study
date: 2022-01-10
journal: Poult Sci
DOI: 10.1016/j.psj.2022.101713
sha: c425e96bd4a719767c2bc2efd7078b91bd0d3c03
doc_id: 977285
cord_uid: bswt77zi

Egg yolk immunoglobulin (IgY) is a class of antibody that is produced in birds against pathogens. Therefore, hyperimmunization of birds can produce a specific antibody in the egg against target antigen for a wide range of applications in diagnostic, prophylactic or treatment in human and veterinary medicine which is known today as IgY technology. Until now, the number of articles, patents and clinical studies on IgY technology has increased significantly. Hence, there is a fact that scientometric studies are needed to gain a deeper understanding of the research for the commercialization of IgY technology. Until now, no scientometric research has been directed toward IgY technology. In view of this, we conducted scientometric analysis in the WoS database. A total of 1,029 IgY-related papers were obtained including 981 journal articles and 48 reviews. The visualization of this literature showed an increasing trend in the number of IgY-related publications over the 4 decades, especially after 2008 to 2021. China, the United States, Canada, Japan, and Germany had the largest number of publications, with 220, 148, 91, 76, and 72, respectively. Among all the research institutions, Dalian University of Technology, Alberta University and Northwest Agriculture and Forestry University published the most of the articles, respectively. Among authors, Dr. Xiaoying Zhang had the highest number of publications with 21. The top most cited publications were from Dr. da Silva with 38 citations. Keywords co-occurrence network analysis showed that the correlation between different keywords is large, especially IgY, antibodies and immunoglobulin which is consistent with the rapid increase in the number of publications. Finally, through this data analysis, we hope that our result could help IgY technology to more maturity toward industrialization and commercialization.

Egg yolk immunoglobulin (IgY) is a class of antibody that is produced in birds, amphibians, and reptiles to protect them against pathogens and also their embryos after transferred to egg yolk in a passive immunity manner (Schade et al., 1994; Ulmer-Franco, 2012 ). Therefore, it is possible to have sufficient and specific antibodies in egg yolk for the prophylactic, treatment, and diagnostic purposes by hyper immunization of avian against a specific target or pathogens for humans and animals use, which is known today as IgY technology (Baloch et al., 2015; Leiva et al., 2020) . In the last 2 decades, the number of studies on the antibacterial, antiviral, antifungal, and antiparasitic actions of IgY in both in vitro and in vivo has increased significantly (Lee et al., 2021) . The first study on egg yolk immunoglobulin was performed by Klemperer (1893) . He observed the protective effect of yolk immunoglobulin from hens vaccinated with tetanus toxin on mice challenged with the toxin. Then in 1959, with the rise of the animal welfare debate, the importance of yolk immunoglobulin production in birds became more apparent (Russell and Burch, 1959) , and in 1969 the term "IgY" was coined by Leslie and Clem. In 1996, because of animal welfare the use of IgY technology as an international standardized technology instead of mammalian IgG was recommended by the European Centre for the Validation of Alternative Method (ECVAM) (Schade et al., 1996) . From then until now, the number of articles, patents, and clinical studies on IgY technology has increased significantly ( Figure 1 ). IgY is known as homolog of immunoglobulin G (IgG) in mammals but has different structural and functional properties (Pereira et al., 2019) . The molecular weight of IgY is higher than IgG (180 kDa vs. 150 kDa), it is more hydrophobic and more resistant to proteases (Chalghoumi et al., 2009) . It is stable and active for 6 mo at room temperature and 5 yr at 4°C (Abbas et al., 2019) . Due to the phylogenetic distance, IgY is unable to bind or activate the mammalian complement system, Fc gamma receptors (FcgRs), and rheumatoid factors (Lee et al., 2017) . Therefore, its use for oral/topical administration in mammals does not induce reactogenic effects and cannot activate the antibody-dependent enhancement (ADE), especially for viral dieses (O'Donnell et al., 2019) . In addition, for diagnostic or immunoassays, IgY may result in less background noise, fewer false positives, and decreased aggregation of antibodies than IgG (Lee et al., 2021; Da Silva and Tambourgi, 2010) . IgY production, in addition to being a noninvasive method in terms of animal welfare, also has a lower cost in large-scale production (Pereira et al., 2019) . Given that there are about 100 mg of IgY in each egg yolk, then one hen can produce about 325 eggs with about 32 g of IgY annually (Da Silva and Tambourgi, 2010) . This is 5 times higher in specific pathogen free birds (500 mg vs. 100 mg) (Lee et al., 2021) . Therefore, due to the properties of IgY, it can have a wide range of applications in prophylaxis and treatment in human and veterinary medicine (Leiva et al., 2020) , for examples, periodontitis, gingivitis, dental caries, gastric ulcer, enteric infectious diseases, dysbiosis, toxins, nutritional and metabolic diseases, chronic diseases, and neoplasms in human medicine and also calf diarrhea, bovine mastitis, infectious and respiratory diseases of birds, shrimp white spot virus and diarrhea of pets in the veterinary field (Kumaran and Citarasu, 2016; Amro et al., 2018; Budama-Kilinc et al., 2018; Lanzarini et al., 2018; Criste et al., 2019; Constantin et al., 2020; Leiva et al., 2020; Hakalehto et al., 2021; Shen et al., 2021) . From 2010 to 2021, more than 400 patents have been registered, 56% of which are related to therapeutic use, 33% to diagnostic and 11% to IgY purification methods (Patentscope). The first clinical trial on IgY (Identifier: NCT01455675) began in 2011 to study the prevention of Pseudomonas aeruginosa infections in patients with cystic fibrosis. To date, about 14 clinical trials have been recorded in FDA (www.Clinical Trials.gov), and one in particular has been commercialized (IgY Max, Identifier: NCT02972463). Also, with the outbreak of coronavirus, clinical trial on IgY as anti-SARS-CoV-2 drug (Identifier: NCT04567810) is in phase I study (www.ClinicalTrials.gov) . There are at least 9 IgY veterinary drugs licensed by Chinese veterinary drug authority (http://www.ivdc.org.cn/), and one IgY human drug in clinical trial according to the disclosure of Sino FDA (http://www.chictr.org.cn/). In the research area (primary or secondary antibodies and diagnostic kits), more than 40 companies have produced IgY products, but their share of the total market of antibodies is about 0.24% (www.benchsci.com). The current number of commercial IgY products in the market is low, but observations show that this technology is being development (Leiva et al., 2020; Zhang et al., 2021a) . So, it is now a right time to analysis the technology retrospectively and prospectively. Hence, there is a fact that scientometric studies are needed to gain a deeper understanding of the research and studies process for the commercialization of IgY technology. Scientometric analysis can be used in quantitative evaluation and analysis on all aspects of the literature in different development stages by computational approaches (Mooghali et al., 2012) . In particular, measurement and analyze of the citation data, research community, technology, and innovation, understanding of scientific citations and mapping scientific fields can facilitate the exploration of the field at issue (Rajendran et al., 2011; Mooghali et al., 2012) . Until now, no scientometric research has been directed toward IgY technology. In view of this, we conducted a scientometric analysis of studies on IgY technology research published from 1980 to 2021. The aims of this study were to identify the major players and their cooperation networks, including countries, academic groups, and individuals; to analyze research status and hotspots, especially the key study findings in this field; to summarize the main research themes and clusters, discuss the potentially valuable research directions, including drug delivery systems (Lee et al., 2021; Zhang et al., 2021a) and the broad prospect of clinical application (Leiva et al., 2020) .

Web of Science (WoS, Clarivate Analytics) is the authoritative database for bibliometric research owning to the existence of the Journal Citation Reports (JCR) and the large amount of citation data. CiteSpace software is developed based on the WoS database, which ensures that the use of WoS data will be better adapted to the diverse functions of the CiteSpace (Boyack et al., 2005; Leeuwen, 2006) . Web of Science Core Collection (WoSCC), as the premier resource on the WoS database, was used to collect information on IgY-related literature and the searched time span 1980-2021 (Data as of 25 Oct. 2021). Combining all keywords related to the topic (including synonyms and alternative terms) with Boolean operators before starting the search for documents is an effective search strategy (Timmins and McCabe, 2005) . The search terms and retrieval strategies were developed as follows: TI (Tittle) = (IgY OR Immunoglobulin Y OR egg yolk antibodies) OR AK (Author Keywords) = (IgY OR Immunoglobulin Y OR egg yolk antibodies); the language type = English; and the document type = articles or reviews or book or book chapter. All data obtained were saved in text format, named "download_xx.txt", and imported into software for analysis.

Microsoft Office Excel (v.2016) was conducted for literature quantity analysis, and the CiteSpace 5.8. R1 was used for scientometric analysis, including country, institution, author, journal, literature cocitation and keyword analysis. The software parameters were set as follows: the time partition was 1980-2021, the time slice (year per slice) was "1", and term sources were selected as "title", "abstract", "author keywords" and "keywords plus"; node types included country, author, institution, keyword and reference; Top N value was set to 50, and the overall graph was simplified by using pathfinder, pruning sliced network and pruning the merged network. The size of nodes and their font in the graph indicated their occurrence times, and the thickness of the connecting line between 2 nodes represented their closeness of connection; the thickness of the node chronology was proportional to the frequency of literature occurrence, and the cold tone of blue to the warm tone of red in the outer circle indicated the change of time from early to recent (Chen, 2006) .

A total of 1029 IgY-related papers were obtained on the database Web of Science, including 981 journal articles and 48 reviews. The visualization of this literature showed an increasing trend in the number of IgY-related publications over the 4 decades from 1980 to 2021, with a corresponding increase in the frequency of citations per year. The number of publications and citation frequencies were low for more than 20 yr before 2007, but from 2008 onward, the relevant literature and citation frequencies spiked, eventually maintaining a high level that fluctuated up and down. Moreover, the highest number of publications and frequency of citations was in 2019 with 70 and 1,450, followed by 59 and 1,420 in 2020, and both indicators may be the same in 2021 as in 2020 ( Figure 1 ). In terms of global distribution, research on IgY has been concentrated in Asia, the Americas (including North and South America) and Europe. In terms of population proportion, African countries contribute the least to IgY research, mainly from Egypt and South Africa ( Figure 2 ). Regarding to IgY related books and chapters, from 2000 to 2021, the results show that the number of books published on IgY was low, but the number of book chapters in relation to IgY was relatively higher (Table 1 ). In 2001, the world's first IgY laboratory manual was published in Germany which standardized the laboratory practices of IgY technology (Schade et al., 2001) . In 2011, a first IgY monograph in Chinese was published (Xiaoying Zhang 2011). Then, in 2021, the second IgY monograph published by Dr. Zhang et al in springer which is now known as the latest and most complete reference (Zhang et al., 2021a) . Most IgY chapters have been published in different books related to egg properties include nutritional or functional foods and bioactive compounds.

In total, 69 countries have done studies on IgY, establishing 197 links between each other (i.e., connecting lines between 2 nodes). Among these 69 countries, China (including Taiwan and Hong Kong, 220), the United States (148), Canada (91), Japan (76), and Germany (72) had the highest number of publications, accounting for 21.38%, 14.38%, 8.84%, 7.39% and 7.00%, respectively. However, in terms of research importance, the top 5 countries were the United States, Germany, Canada, China, and India. In addition, compared with European and American countries, the research on IgY in China, India and Brazil was mainly concentrated in the past 10 yr ( Figure 3 , Table 2 ).

A total of 457 journals published articles or reviews in this field. The top 10 journals by publication volume published nearly 20% (123 articles) of the articles in the top 10 journals. Among the top 10 journals, Poultry Science (impact factor or IF 2020, 3.352), Journal of Immunological Methods (IF 2020, 2.303) and Food and Agricultural Immunology (IF 2020, 3.101) contributed considerably to the number of publications, with 37, 35 and 18 publications, respectively. As of October 2021, the total number of publications corresponding to the 3 journals was 79,878, 4,998, and 2,432, respectively (Table 3) . On the other hand, a total of 915 cited journals were present in IgY study and these journals formed 4531 connections. The top ten journals were cited more Notes: ※ Centrality is an indicator of the importance of a node in the network, and a larger centrality value means that the node is more important in the whole network. (458), followed by Poultry Science (374), and Journal of Immunology (263) ( Table 4 ). In addition, the dual map overlay of journals showed that the most contributed journals were from molecular, biology, and immunology fields and veterinary, animal, and science fields, and these journals mostly cited journals from molecular, biology, and genetics fields (Figure 4 ). Table 5 ).

A total of 987 researchers are involved in IgY research, forming a collaborative network with 1,323 collaborations. Among them, Dr. Xiaoying Zhang had the highest number of publications with 21, followed by A Larsson (12), Xiaoyu Li (11), Yongping Xu (11), and Atsushi Mural (10). In addition, the teams with the most and closest collaborators are represented by Xiaoyu Li, Yongping Xu and Agnieszka Lupickaslowik ( Figure 6 , Table 5 ).

The total 1,029 IgY publications have 1,345 co-citations, resulting in 3,462 links. The 6 most cited articles were all review, focusing on the use of IgY antibodies in immunoassays, veterinary medicine, and human medicine. The most cited study was published by Vega et al. (2011) in Veterinary Immunology and Immunopathology, entitled "Egg yolk IgY: protection against rotavirus-induced diarrhea and modulation of systemic and mucosal antibody responses in newborn calves". In addition to the above 6 review articles, the top ten cited papers are Abbas AT (2019), Pauly (2009), Zhen YH (2008), with 19, 17, 17 times respectively (Figure 7) . On the other hand, the top 20 cited articles were mainly published after 2007, with 16 articles, accounting for 80% (Table 6 ). Cluster analysis revealed that these literatures were clustered into 187 categories, with the largest category being venom neutralization with 125 literatures and a silhouette of 0.935. In this category, Middle East Respiratory Syndrome Coronavirus (MERS-CoV) and Coronavirus Disease 2019 (COVID-19) were presented as 2 candidate terms. The subsequent categories were norovirus and avidin-biotinylated IgY with 117 and 79 publications, respectively, with silhouette values of 0.904 and 0.944 (Table 7) . Figure 8 showed the timeline of significant cited references under different clusters. Influenza a, neuropeptides and bothrops alternatus were previously studied based on IgY antibodies, but after 2000, there was no literature on this subject and attention decreased. In contrast, the main topics being studied in recent years are venom neutralization (#0), norovirus (#1), quail (#3), teleost (#6) and ELISA (#12), and accordingly, the references under these clusters are mainly published in the last decade ( Figure 8 ).

A total of 793 keywords were extracted from the titles, abstracts, and author keywords of 1,029 papers, and 1,862 links were created. Visualizations network map of keyword co-occurrence showed that the most frequently occurring keywords in articles published between 1980 and 2021 were IgY (365), antibody (219), immunoglobulin (182), chicken (163), purification (154), and egg yolk (148), which are highly correlated and are all related to the IgY antibody's own properties. In addition to the above, keywords related to IgY applications also appear many times, such as infection (109), ELISA (106), passive immunization (78), and Escherichia coli (75) (Figure 9 , Table 8 ). Based on the keyword co-occurrence mapping, the Burstness label was adjusted by setting the parameters g = 0.5 and minimum duration = 2, and 112 burst items were generated. Of the 112 keywords or phrases with the strongest citation bursts, the earliest and longest-lasting occurrence was antigen, followed by immunized hen and dental caries (Figure 10) . A total of 18 keywords have been highlighted in the last few years and continue to be highlighted until now. The top 5 keywords with the highest intensity are IgY antibody, immunotherapy, chicken IgY, immunoglobulin IgY and therapy, which are consistent with a significant increase in the number of articles published from 2017 onwards. In addition, circulating antigen, biofilm and nanoparticle have seen a significant increase in attention in IgY-related studies in the last 2 yr (Figure 10 ). 

In the last 2 decades, numerous studies on IgY technology for the purposes of diagnosis, prophylactic or treatment have been published (Figure 1 ). Therefore, a deeper understanding of the research and studies process on IgY is needed. We conducted an in-depth scientometric analysis of literature on IgY using a computational tool to explore the trends in publications on IgY technology. To our knowledge, this is the first scientometric study on IgY technology to assess research efforts related to the process on the quantity of articles published in this field. We examined the IgY technology from multiple perspectives including analysis of the literature quantity, country, institution, author, co-citation references and keywords co-occurrence network (Mooghali et al., 2012; Rajendran et al., 2011) . Based on the WoS database, and the analysis of 1029 IgY-related articles since 1980 and IgY related books or chapters, we found that research on IgY technology had been increased significantly especially after 2007 and mainly focused on the following 2 sections: firstly, technical development, include the understanding of IgY molecule, production, extraction and purification; and secondly, drug development, include clinical application of IgY products, companies, regulations and product approval (Lee et al., 2021) . In 1996, with the discussion of animal welfare by the ECVAM and the production of antibodies in mammals as an invasive method, the production of IgY in egg as a noninvasive method, with a lower cost in large-scale production became very prominent (Schade et al., 1996) . Since then, the number of articles, books or chapters published on the production of IgY in chicken has increased. At the same time, the number of articles on methods of extraction and purifying IgY from eggs expanded (Nilsson et al., 2012; Bizanov, 2017) . The number of articles, patents and companies working on diagnostic products also increased (Lee et al., 2021) . IgY technology attracted an increasing number of researchers owning to IgY's unique properties, including lack of binding and activation of the Fc gamma receptors (FcgRs), no reactogenicity and greater phylogenetic distance which has led to an increase in the number of publications in the prophylactic or treatment of some animal and human diseases (Pizarro et al., 2017; Sudjarwo et al., 2017) . Increased publications in the diagnostic or immunoassays branch can be described as less background noise or false positives and decreased aggregation of IgY than mammalian IgG (Lee et al., 2021) . On the other hand, a significant increase in publications over time especially from 2007 onwards may be attributed to growing of the scientific journals for article publishing, growing funding volume or companies' attention to IgY technology. As shown in Figure 1 , after 2007, the number of publications increased significantly. Accordingly, the number of citations significantly increased, which indicates the quality index of articles also increased. The peak of this index was from 2014 and this trend has continued until 2021. The results showed that attention to IgY technology was increasing, and this trend was expected to continue in the future. The results of journal analysis showed that about 20% of IgY articles have been published in highimpact journals (from the JCR indicator), in which, researchers have been more interested in publishing articles in specialized journals, for example Poultry Science or Journal of Immunological Methods. IgY publications in more specialized journals indicates the greater accuracy of published articles related to this technology. In addition, the dual map overlay of these journals showed that IgY study was concentrated in the fields of molecular biology, immunology and veterinary medicine, and that advances in theory and technology in these disciplines could, to some extent, contribute to the development of IgY technology.

Based on the comparative scientometric analysis among these 69 countries, China, the United States, Canada, Japan and Germany were the main countries involved in IgY research, accounted for 59% of the publications. A special phenomenon also emerged, with China having a high number of total publications but less impact due to the short period of research (as shown in Table 2 , the centrality values for China are smaller to that of the US and Germany). As for institutions analysis, more than 600 institutions have participated in IgY research from 1980 to 2021. As can be seen in Figure 5 , the 6 institutions were the most prolific in the field of IgY technology, the greatest number of which existed in Asia, especially in China. The international connection of these institutions has been less than their internal communication, except for the 5 institutes from China, which had good international connections. Nevertheless, these data showed that there was very weak cooperation between institutions. Therefore, to help the better growth of this technology, it may be necessary to strengthen international exchanges or form an international community of IgY technology. The author's Figure 10 . The top 112 keywords with the strongest citation bursts.

analysis in co-citation network map using CiteSpace indicated that more than 987 authors contributed to the IgY publications and had cooperate with 2 or more core authors. This data can provide information on influential research groups and collaboration between individual authors and/or institutions. Dr. Xiaoying Zhang was located at a central position of the author coauthorship network map as "core strength" in this field, with broad research focuses cover IgY molecule and evolution, IgY extraction and purification, IgY based immunoassay and therapy, perspective and popularization of IgY technology, and IgY book and standard editing, etc. Apart from these 6 authors mentioned in the results section, most authors had limited publications and networking, indicating that collaboration between authors, particularly between different research groups in this area has not been very common. Therefore, more attention should be paid to improving and increasing communications between authors and research teams. Citation counts are one of the most significant indicators of scientometric analysis and estimate the scientific relevance of the publications to quantify the relative impact of papers (Mooghali et al., 2012; Rajendran et al., 2011) .

Looking at the results of this section, as shown in Figure 7 and Table 6 , out of 10 articles that had the most citations that were 7 review and 3 research articles.

The main topics of the review articles were immunodiagnostic or immunotherapeutic, while the research articles were on the extraction and purification of IgY. Also, the highest rate of citation was in the period of 2010-2013. But high-quality articles have been published recently that have less citations. The reason could be that the citation rate in this section has been more influenced by the year since published than the quality of the article (Lee et al., 2021) . The clustering results of the cited documents showed that "venom neutralization" and "norovirus" were the 2 largest clusters, which are closely associated with coronavirus and passive immunity (Table 7 ; Figure 8 ), indicating the great potential value of IgY antibodies in the context of a global pandemic of COVID-19 (Constantin et al., 2020) . Keyword co-occurrence network analysis showed that IgY, antibody and immunoglobulin were the most frequent keywords (Figure 9 ), which indicates that these words are the core terms in IgY research, and our search strategy is comprehensive and credible. Keywords burstness reflected the dynamics of research priorities and hotspots during the IgY development ( Figure 10 ). Antigen, immunized hen, and dental caries were the key phrases that researchers focused on the earliest and longest, indicating the importance of basic research for IgY technology and the fact that dental caries may be one of the first IgY applications to receive attention (Otake et al., 1991) . In recent years, IgY research has focused on disease prevention and immunotherapy, both in veterinary and human medicine. Studies have shown that IgY antibodies can be used to treat disease by inhibiting the growth of bacterial biofilms that are responsible for certain diseases, such as Porphyromonas gingivalis and Pseudomonas aeruginosa, which cause periodontitis and cystic fibrosis, respectively (Li et al., 2020; Thomsen et al., 2021) . Examples include biofilm and nanoparticles, indicating that this technology is well on its way to conducting clinical trials to commercial products (Pereira et al., 2019) . In conclusion, scientometric analyzes have shown that research on IgY has evolved from the initial discovery and purification methods of antibodies to more extensive research on applications for disease control and health promotion, with commercial applications perhaps in the near future. On the other hand, some welcome change and development tendency in hen egg industry have been emerged in the recent years, including increasing comprehensive utilization of hen egg along with the development of comprehensive extraction and purification techniques, application of bioactive egg compounds in nonfood sectors (Zhang et al., 2021b) , such tendency also promotes the application of IgY antibody. CiteSpace is a Java-based application for detecting and visualizing possible trends and fundamental changes in scientific disciplines over time and is an effective and comprehensive tool for bibliometric analysis (Chen, 2006; Cobo et al., 2011) . As far as IgY technology is concerned, the CiteSpace software-based scientometric analysis has helped to identify the development history and status of IgY studies, influential research individuals and groups, research frontiers and hot spots. However, this software may still have some limitations, the analyzed literatures are largely limited by the search source and the composite query used (Chen, 2017) ; it can only perform a co-citation analysis based on the referenced literature and cannot present the total number of citations of each literature. To better overcome such limitations, multiple databases and combined visualization techniques, such as citation context analysis and VantagePoint software, could be applied for a more indepth analysis of a specialty area like IgY technology.

In summary, IgY technology has made significant progress in the last 2 decades and has proven that it can be applied for diagnostic, prophylactic, or treatment purposes. In this study, for the first time, the structure and the evolution trend of this knowledge over the time were performed using scientometric analyzes. As showed in the results, the ascending trend in the number of publications or citations indicates that this technology has attracted a great deal of interest from researchers, especially in the last 10 yr. Also, the number of research institutions in different countries and the scientific connections between them has increased. In addition, the development of laboratory methods and applying the other technologies to this field has led to more maturity of IgY technology toward commercialization.

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This work was supported by the National Natural Science Foundation of China [grant number 31873006].Notes: The article contains no dealings with human or animal subjects for any analysis.

The authors declare that they have no competing interests.

Supplementary material associated with this article can be found in the online version at doi:10.1016/j. psj.2022.101713.