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Comprehensive bibliometric and visualized analysis of research on fecal microbial transplantation published from 2000 to 2021

BioMedical Engineering OnLine volume 21, Article number: 78 (2022) Cite this article

Abstract

Background

Fecal microbial transplantation has emerged in recent years as a method of treating disease by rebuilding the intestinal flora. However, few bibliometric analyses have systematically studied this area of research. We aimed to use bibliometric analysis to visualize trends and topical research in fecal microbial transplantation to help provide insight into future trends in clinical and basic research.

Materials and methods

Articles and reviews related to fecal microbial transplantation were collected from the Web of Science Core Collection. Significant information associated with this field was visually analyzed by using Biblioshiny and CtieSpace software.

Results

A total of 3144 articles and overviews were included. The number of publications related to fecal microbial transplantation significantly increased yearly. These publications mainly came from 100 countries, led by the US and China, and 521 institutions. The most prolific and influential author is KHORUTS A. The main disciplines and application fields of fecal microbial transplantation included molecular /biology/immunology and medicine/clinical medicine, and the research foundation of fecal microbial transplantation was molecular /biology/genetics and health/nursing/medicine. An alluvial flow visualization showed several landmark articles. New developments were identified in terms of reference and keyword citation bursts. Data analysis showed that different FMT preparation and delivery methods gradually appeared as research hotspots. The main research keywords in the last 3 years were chain fatty acids, Akkermansia muciniphila, and insulin sensitivity, other keywords were current and developing research fields.

Conclusion

Research on fecal microbial transplantation is flourishing and many new applications of fecal microbial transplantation are emerging. Microbial metabolites such as short-chain fatty acids and the microbiota–gut–brain axis have become the focus of current research and are future research trends.

Introduction

The gastrointestinal tract of mammalian is an ideal habitat for various microorganisms, such as bacteria, fungi, viruses and archaea [1, 2]. The gut contains a complex ecosystem of trillions of commensal microbes [3], the intestinal mucosa, where the microbiota and immune system engage in extensive bidirectional communication, is the best-studied interface for host–microbiota interactions [4]. Growing evidence demonstrates that the microbiota and derived microbial compounds play a pivotal role in the development and maintenance of normal intestinal development and physiology, including host immunity, food digestion, tissue development and the regulation of gut endocrine function and neurological signaling [5]. Most of the microorganisms that inhabit the gut are affected by the method of birth, breastfeeding, daily lifestyle, drugs and genes of the host [6]. With exposure to environmental factors, the gut microbiota matures gradually during childhood and remains relatively stable during late childhood, puberty and adulthood [7, 8]. Maturing gut microbe core functions include genes encoding glycosaminoglycan degradation; short-chain fatty acids (SCFAs) production through complex polysaccharide fermentation and, specifically lipopolysaccharide (LPS) synthesis; and the biosynthesis of some critical amino acids and vitamins [9,10,11,12]; whereas, reciprocal interactions between the gut microbiota and host immunity are complicated, dynamic and environment dependent [4]. The use of antibiotics, changes in diet and geographic location can disrupt the host–microbiome interface, and damage to the immune system can lead to systemic dissemination of commensal microorganisms, susceptibility to pathogen intrusion, and abnormal immune reactions.

Fecal microbial transplantation (FMT) is the process of transferring minimally handled prescreened donor feces into a patient's gastrointestinal tract with the aim of correcting dysbiosis by increasing overall diversification and restoring microbiota functions [13]. In 2013 [14], a randomized controlled clinical trial (RCT) showed that FMT was generally safe and highly effective in the treatment of recurrent Clostridioides difficile infection (RCDI), led FMT to become an intriguing but poorly understood intervention in a prevailing condition of global concern. Currently, the only established indication for FMT is CDI [15]. Inflammatory bowel disease (IBD) may be an emerging indication for FMT. To date, four RCTs have been published investigating the use of FMT for the treatment of ulcerative colitis (UC) [16,17,18,19]. Gut microbes not only shape the function of the gut but also influence the physiological function of other important extraintestinal organs, including the liver, lungs and brain [2], so there are many future directions and areas of uncertainty, such as hepatic encephalopathy (HE) [20, 21], primary sclerosing cholangitis (PSC) [22], metabolic syndrome and obesity [23, 24], and neurological disorders such as Parkinson's disease [25, 26] and autism spectrum disorders [27, 28].

Microorganisms that reside in the gastrointestinal tract (GIT) play a critical role in the maturation and development of the immune system, central nervous system and digestive system [29]. Many diseases occur with intestinal microorganism imbalances. FMT can restore intestinal homeostasis and structure, so it is widely used in the treatment of many diseases. However, up to now, no articles have systematically studied FMT using bibliometrics.

Bibliometric analysis is a comprehensive knowledge system focusing on quantification, and has been widely used to gain insight into scientific development trends. Through bibliometric analysis scholars cannot only quickly grasp the research hotspots and development trends of a specific research field, but also evaluate the distribution of countries, authors in the research field. Web of Science Core Collection is a common database used in bibliometric analysis. To analyze the active countries and authors on FMT, the R-bibliometrix package (version 3.0.3, http://www.bibliometrix.org) in R-Studio (version 1.2.1335) was used. Biblioshiny, a shining app provides bibliometrics was used to support the import of metadata from database and subsequent data management [30]. CiteSpace which is focused on the analysis of the potential facts contained in the scientific literature was used to analyze the subject categories, citation bursts of references and keywords, and the alluvial flow visualization of co-cited references [31].

Results

Trends in publications

Annual literature publications in a specific field can directly reflect the development of that field. Figure 1 reflects that the research on FMT before 2009 showed a fluctuating trend; since 2010, research on FMT is increasing in the literature. The period from 2000 to 2009 was an embryonic period. From 2010 to 2014, publications on FMT showed a continuous growth trend, during which the highest annual growth rate of published papers was approximately 169.2% (2011–2012). From 2015 to 2021, the annual publication growth rate was relatively stable, and the highest number of articles published reached 692 per year, indicating that FMT as an emerging therapy may become a research hotspot for basic and clinical research.

Fig. 1
figure 1

Trend of publications in fecal microbial transplantation from 2000 to 2021

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Active countries/regions and authors

A total of 3144 articles were published by 521 institutions in 100 countries. Tables 1 and 2 summarize top 10 countries and institutions based on their total publications, year in tables represent the first posting time of relevant literature in country or institution. Centrality of a node in the network measures the importance of the position of the node in the network. Citespace uses this metric to identify and measure the importance of an article, highlights such literature (or authors, journals, institutions, etc.) with purple circles and nodes with centrality over 0.1 called critical nodes. Table 1 shows that the United States (US) was the most productive country, with the highest centrality of 0.24, followed by China and Italy. Table 2 shows that Harvard Med School was the institution with the most productive country, however its centrality was relatively low when compared to other institutions. By contrast, the University of Minnesota System, University of Michigan and University of Alberta had relatively higher centrality. Figure 2A displays the global country cooperation map produced through the application of the biblioshiny app. There were 1101 pairs of collaborating countries/regions worldwide, and most pairs came from the US, whose total of 501 pairs reflect its close cooperation with the other 14 countries. The top 10 most prolific researchers are shown in Fig. 2B, and the most productive author was Khoruts A, who is from the University of Minnesota, followed by Zhang FM, pioneer of FMT in China. Table 3 shows the information about the outstanding researchers in FMT.

Table 1 Top 10 countries ranked by total publications
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Table 2 Top 10 institutions ranked by total publications
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Fig. 2
figure 2

Analysis of active countries and authors. A Country collaboration map of studies associated with fecal microbial transplantation. B The top ten active researchers in the field of fecal microbial transplantation and their publications over time. Size of circle represents number of publications, and the deeper the color, the more citations

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Table 3 Top 10 active researchers ranked by their total publications
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Subject categories

A dual-map overlay for the journals can reflect the subject categories of FMT and the areas in which FMT is most applied. In Fig. 3, on the left is the distribution of the cited literature in the journals representing the main disciplines and application fields of FMT, which included molecular/biology/immunology and medicine/clinical medicine; on the right is the distribution of the corresponding cited literature in the journals representing the main disciplines citing FMT and the research foundation, which included molecular/biology/genetics and health/nursing/medicine. The colored curves between them are citing paths, which fully show the cited relationships.

Fig. 3
figure 3

The dual-map overlay of journals on fecal microbial transplantation

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Bursts of cited references

The rapid development of a field is characterized by articles that experience a citation burst [32]. Table 4 shows the top 10 references with the strongest citation bursts during 2000–2021. The article with the strongest citation burst was published in The New England Journal of Medicine by van Nood E in 2013, and its burst continued for 5 years, with a burst strength of 101.51 [14]. The article with the second-strongest burst was by Gough E in 2011, with a burst strength of 66.95 [33]. Table 5 shows the top 10 references with the strongest citation bursts during 2019–2021. Among the articles with strong citation bursts, McDonald LC’s 2018 article [34], which was published as a clinical practice guideline for CDI in adults and children, had the strongest citation burst with a burst strength of 52.81. The second article with the most recent citation burst reported the effect of FMT on 8-week remission in patients with UC [19]. This work demonstrated that adults with mild to moderate UC were more likely to be in remission at 8 weeks if they received 1 week of anaerobically prepared donor FMT than if they received autologous FMT. The third article that has drawn much attention was a 2018 article published in Science [36] which found that dysbiosis in gut microbiome composition may result in primary resistance to immune checkpoint inhibitors and proved that the gut microbiome affects the efficacy of PD-1-based immunotherapy for epithelial tumors. The fourth article was a systematic review with a meta-analysis [37] that provided evidence that FMT is an effective treatment for RCDI. The fifth article was a randomized clinical trial about whether the clinical efficacy of FMT for RCDI differed according to the route of delivery, and the results showed that among patients with RCDI, FMT via oral capsules was comparable to colonoscopy in preventing recurrent infection over 12 weeks, suggesting that oral capsule therapy may be a convenient method of treating RCDI [38].

Table 4 Top 10 references with the strongest citation bursts during 2000–2021
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Table 5 Top 10 references with the strongest citation bursts during 2019–2021
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Clusters of co-cited references

Co-citation implies that two related articles (or authors) are cited by the third article (or author) at the same time. A Citespace segments the co-citation network into multiple co-cited reference clusters, keeping references closely connected within the same cluster but loosely connected between distinctive clusters [46]. Figure 4A illustrates the six largest clusters in the network of co-cited references, the details of which are shown in Table 6. The size of each cluster indicates the number of members in it; the larger the cluster, the more representative. The silhouette score, which is an indicator of homogeneity or consistency, can also reflect the quality of a cluster. The silhouette values of homogenous clusters tend to approach 1[46], and most of the clusters in Table 6 are highly homogeneous, which means that the quality of the group is high. LSI, LLR and MI are three different algorithms provided by CiteSpace for extracting clustering labels, in the actual research process, users can use the labels extracted by the LLR algorithm in the visualization network to show the clusters names. The average year of publication of a cluster indicates its recentness. Circles with purple edges show high centrality (which is evaluated by purple edge range of the circle rather than circle size) and act as a bridge between different disciplines [46]. Clearly, cluster #1 and cluster #4 contained the cited references with the highest centrality, and the citation rate of articles in cluster #1 was relatively high, for example, the article with largest circle published by van Nood et al. in cluster #1 and the article with the highest centrality published by Gill et al. [47] in cluster #4 as shown in the table in Fig. 4A. Next, we would focus on these two clusters.

Fig. 4
figure 4

Clusters of co-cited references and visualized timeline for cluster #1. A The six largest clusters in the network of co-cited references and top 4 authors with highest centrality in cluster 4. B A visualized timeline for cluster #1, and five high-impact contributions with large citation patterns and citation bursts colored in red from 2019 to 2020

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Table 6 Top 6 clusters of co-cited references with the highest K value
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Cluster #1 on FMT, which had an average publication year of 2014, was the most recently formed cluster, and it contained numerous nodes with red rings of citation bursts [32]. We selected the 5 most cited references in this cluster and 5 citing articles, as listed in Table 7. The most cited article in this cluster was an initial randomized trial that compared FMT with vancomycin in the treatment of RCDI [14] and demonstrated that for the treatment of RCDI, an infusion of donor feces was more effective than the usage of vancomycin. The second most cited reference came from Moayyedi et al. [17], who found that FMT induced significantly higher remission rates than placebo in active UC patients, with no discrepancy in terms of adverse events. Cluster #1 consisted of 301 co-cited references. The five selected citing articles were all reviews, and two articles were published in 2019. Unlike previous articles, the application of FMT in these two articles was not limited to CDI, it could also be used in HE and cardiometabolic syndrome [15, 50]. Furthermore, we created a visualized timeline for cluster #1, as shown in Fig. 4B. We selected five high-impact contributions with large citation patterns and citation bursts colored in red from 2019–2020; among them, three articles were RCTs [19, 52, 53], and the remaining two were case reports and reviews [54, 55]. DeFilipp et al. described that in two independent clinical trials, extended broad-spectrum β-lactamase (ESBL)-producing Escherichia coli bacteremia occurred in two patients after they received FMT, both from the same fecal donor, and one of the patients died. Therefore, there is a need for enhanced donor screening to limit the spread of microorganisms that may lead to adverse infectious events and continued vigilance to determine the indications for and risks of FMT in different patient groups.

Table 7 Top 5 cited references and citing articles of Cluster #1
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Cluster # 4 on growth promoters had four articles with high centrality, and among them, three articles were published in Nature. Qin et al. [56] depicted Illumina-based macrogenome sequencing, assembly and characterization of 3.3 million irredundant microbial genes from the sequences of 576.7 gigabases derived from fecal samples of 124 European individuals. Arumugam et al. [57] integrated 22 newly sequenced personal fecal macrogenomes from four different countries with previously published datasets and they identified three not nation or continent specific robust clusters. The work of these two articles can be regarded as the basis for FMT. The third article demonstrated that gut microbes interact with the innate immune system as a key epigenetic factor in altering type 1 diabetes (T1D) susceptibility [58].

An alluvial flow visualization of highly co-cited references

Alluvial flow diagrams aim to reveal time patterns in evolutionary networks [59]. To observe the citation changes of top 5 cited references in cluster 1 intuitively, we generated an alluvial map. First, the data were retrieved from CiteSpace, and networks of co-cited references were generated. Because the top 5 cited references were all published in 2010–2021, the networks exported into the alluvial generator (https://www.mapequation.org/apps/AlluvialGenerator.html) were within this timespan. Nodes in the import network that had the longest presence are highlighted by coloring the flows they form. As shown in Fig. 5, the article with the longest presence was published by van Nood et al. and its presence lasted for six years but did not continue until 2021. Two articles from Paramsothy et al. and Cammarota et al. presented a noninterrupted presence to 2021. The former evaluated the efficiency and safety of FMT in patients with UC in a double-blind randomized trial which demonstrated that in patients with active UC, intensive drug administration, multiple donors, FMT induced clinical remission and endoscopic improvement was associated with different microbial changes. The latter is a European consensus conference on FMT, which provided statements on FMT indications; donor selection; clinical management and basic requirements for implementing an FMT center. These most cited articles mentioned above in cluster 1, especially the presence of which continued until 2021, can represent research hotspots of FMT to some extent.

Fig. 5
figure 5

The alluvial flow map of the top 5 co-cited references. Each line represented a study, and colored and continuous lines referred to articles that had been consistently cited

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Analysis of thematic evolution and keyword citation bursts

Keywords can summarize research topics, through the analysis of keywords, we can understand the research hotspots in specific fields. In the present work, the terms from “keywords Plus” based on the Web of Science Core Collection database and keyword citation bursts can be considered emerging topics within this domain. Therefore, thematic evolution analysis of the keywords was performed. Figure 6 clearly shows the research progress in this field. The initial stages of research on FMT involved “immune responses”, “stem-cell transplantation”, and “bacteria”. However, as this area of research matured, the main research hotspots of FMT gradually changed to “obesity”, “probiotics”, and “inflammatory bowel disease”, among others. Recently, the topic of gut microbial metabolites such as “chain fatty acid” and “brain-gut axis” has gradually attracted the attention of scholars. Furthermore, we conducted a keyword citation burst analysis. The top 10 keywords with the most recent bursts are shown in Table 8, among them, “insulin sensitivity” and “Akkermansia muciniphila” both with the strongest citation bursts, indicating that FMT may play an essential role in improving insulin sensitivity and then treating diabetes. Meanwhile, with a spurt of progress in science technology, the role of specific strain in disease such as Akkermansia muciniphila have been confirmed by analyses, which can provide new ideas and therapeutic targets for the treatment of clinical diseases.

Fig. 6
figure 6

Sankey diagram of keywords evolution of fecal microbial transplantation

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Table 8 Top 10 keywords with the strongest citation bursts during 2018–2021
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Discussion

General information

In this study, we analyzed the major knowledge domains and emerging trends in FMT by using bibliometrics. The results showed that the number of annual publications on FMT presented an upward trend and is currently in a stage of rapid expansion. The analysis of active countries and authors showed that the US is not only the most productive country, but also formed close cooperation networks with many other countries, which means that the US is the premier country for FMT research, meanwhile, the University of Minnesota System and University of Michigan which were located in the US also showed higher centrality. China was the second most productive country, Nanjing Medical University was the main representative Chinese institution. Khoruts A, a gastroenterologist at the University of Minnesota, co-author of the first detailed operational guide to FMT, was the author with the most publications and the highest H-index.

The dual-map overlay of journals intuitively reflect the discipline distribution and application areas of FMT. Cited reference burst analysis and alluvial flow visualization can help us find landmark articles for FMT among the thousands of studies. The results of Table 4 and Fig. 5 show that, van Nood et al., who was the first to demonstrate that FMT is generally safe and highly effective in the treatment of RCDI in RCT, making the article became the strongest and most lasting references during 2013–2018.However, strong side effects had been reported after FMT in 2019 [55], perhaps it was the reason for not continuing of the article by van Nood et al. in the last two or three years. Except for the European consensus conference published by Cammarota et al., the remaining articles were RCTs on UC, which indicates that UC may be a new indication for FMT.

Frontier and hotspot analysis

The analysis of references citation bursts in recent years may reflect developments in specific fields. Table 5 and Fig. 4B show articles with the most recent bursts and high-impact contributions from 2019 onward. Their main content can be summarized as follows.

The treatment efficacy of FMT in CDI has already been proven. However, it is uncertain whether the preparation and mode of administration of FMT affect clinical efficacy, so this has become the focus of discussion recently. A systematic review with a meta-analysis showed that FMT is an effective treatment for RCDI, regardless of the preparation method or delivery approach [37]. A randomized controlled trial showed comparative efficacy of FMT observed in subjects receiving fresh or frozen fecal products from the same donors. The efficacy of the freeze-dried product was slightly reduced compared to that of the fresh product but was similar to other treatments in terms of microbial recovery 1 month after FMT [56]. In addition, Costello et al. [19] proved that in patients with mild to moderate UC, treatment with anaerobically prepared donor FMT for 1 week was preferred to result in remission at 8 weeks compared to treatment with autologous FMT. Kao et al. [39] demonstrated that in adults with RCDI, oral capsule FMT was not inferior to colonoscopy in preventing recurrent infections over 12 weeks. Taken together, the correlation between the preparation and delivery method of FMT and clinical efficacy has become a research hot topic, and more convenient methods may appear in the near future, for example, oral FMT [60].

Possible future directions and areas for FMT

With the development of FMT, a number of emerging research areas are becoming the subject of interest for researchers. Keywords represent the research theme and core content of the literature. The analysis of thematic evolution and keyword citation bursts showed that some items had higher burst strengths. Figure 6 and Table 8 show that flora metabolites such as “short-chain fatty acids”, specific strains such as “Akkermansia muciniphila”, “brain” and metabolism-related terminology such as “inulin sensitivity” are emerging as research hotspots.

Microbial metabolites—short-chain fatty acids

SCFAs are carboxylic acids with less than 6 carbon atoms and are the most commonly studied metabolites of the intestinal microbiome [61]. Over 95% of the SCFAs produced in the intestine are acetate, propionate, and butyrate, although small amounts of valerate, isovalerate, propionate, hexanoate, isohexanoate, succinate, isobutyrate, and caproate are also found [62,63,64]. SCFAs are involved in many different host physiological processes, including gastrointestinal function [65], the regulation of blood pressure [66], circadian rhythms [67], and innate and adaptive immune regulation [68]. Therefore, the occurrence of various diseases is accompanied by altered fecal short-chain fatty acid content. The results of our bibliometric analysis also showed that targeted dietary SCFAs may be a mechanism to alter immune profiles, promote immune tolerability, and enhance glucose control for the therapy of T1D [69]. In addition, patients with IBD and PD all exhibited abnormal of SCFAs level in fecal [70,71,72]. All the above indicated that, SCFAs play a major role in metabolic and neurological disorders.

Specific strain of bacteria—Akkermansia muciniphila

Akkermansia muciniphila is a Gram-negative and strictly anaerobic bacterium that was first isolated from the human face in 2004 [73]. Akkermansia muciniphila belongs to the Verrucomicrobia phylum and was found to be abundant in the human intestine [74, 75]. Growing evidence demonstrates that A. muciniphila can effectively improve metabolic disorders and is therefore regarded as a promising “next generation of beneficial microorganisms” [76]. Our findings also indicated that the abundance of A. muciniphila is indeed associated with many diseases, metabolic diseases such as type 2 diabetes (T2D) [77], obesity [78,79,80], Binge eating disorder (BED) [81] and psoriasis [82], which indicates that microecological agents may become an important therapeutic approach in the future.

Microbiota–gut–brain axis

The existence of the “brain–gut axis” was first identified in the mid-nineteenth century by Doctor William Beaumont [83], who found that when his patient was upset or annoyed, it greatly affected the digestive rate, suggesting that the emotional state of an individual can affect their digestion, i.e., the presence of the brain–gut axis. With the emergence of brain imaging in the 1980s, a comprehensive interpretation of the bidirectionality of this axis appeared. Even though the microbiota–gut–brain axis is an emerging concept, it is gradually being accepted that microbial residents can exert considerable influence on host performance [84,85,86,87], and this axis has received increasing attention in the field of investigating the biological and physiological basis of psychiatric, neurodevelopmental, age-related and neurodegenerative diseases [88]. Therefore, some probiotics are widely used in the clinic. Several studies have shown that probiotics are effective in improving mood and cognition and relieving stress and anxiety [89,90,91,92]. In addition, researchers have shown that the microbiota–gut–brain axis is associated with neurological diseases and disease processes, including autism spectrum disorder [27, 93], major depressive disorder [94], anxiety [95, 96] and schizophrenia [97]. The above results from preclinical and clinical studies have opened up the potential for targeting the gut microbiota in the treatment of psychiatric and neurological disorders.

Conclusions

FMT has significant research value and promising applications. The number of studies on FMT generally shows an increasing trend. The US and China are the leaders in this research. Among the research institutions, Harvard Medical School is the institution with the most articles, while its centrality is less than 0.1, which indicated that its collaboration with other institutions should be strengthened. Khoruts A is an excellent pioneer in the field of FMT. Most publications on FMT have been cited in influential international journals, indicating that FMT has received widespread attention. Current research on FMT is focused on microbiota metabolites, specific strains of bacteria, the microbiota–brain–gut axis and the role of FMT in other diseases, which will be the focus of future research.

Although following the principles of certain bibliometrics and comprehensive analysis strategies, there are some inevitable limitations to our current study. First, only articles and reviews from the Web of Science Core Collection databases in a particular time period were used, so this may lead to literature and publishing bias. Second, our search strategy included only some specific terms relating to FMT, therefore, the retrieved publications may contain false positives and false negatives. Finally, to date, there is a lack of adherence to ethically accepted international standards in bibliometric analysis, and the constraints of analytical tools may provide subjective views of an individual's work and contributions. Despite these limitations, due to the sufficient number of documents collected in this analysis, our bibliometric showed the advanced countries, institutions and pioneers in studying FMT and summarized research frontiers, hotspot and landmark articles in the development of FMT adequately. We convinced that what we found about FMT studies can provide a complete picture and contributes to current research and future directions in the field.

Methods

Data source and search strategy

Data were derived from the Web of Science Core Collection which covers the largest and most comprehensive literature and were downloaded on January 3, 2022. The retrieval formula was defined as TS = (fecal microbial transplantation) OR TS = (intestinal microbiota transplantation) OR TS = (fecal bacteriotherapy). According to our search strategy, the literatures before 2000 has little relevance to FMT, so we determined the search time range from January 2000 to December 2021. The search resulted in 4042 records being identified, and 898 irrelevant articles such as “meeting abstracts”, “book chapter”, “editorial materials”, “early access”, “proceeding paper”, “correction” and “letters” were excluded. Finally, 3144 documents include “article” and “review” were exported into a form of all records and references, saved as plain text files and then saved in download_txt format.

Availability of data and materials

The initial contributions discussed in the study are included in the article material, and further queries can be referred directly to the corresponding author.

Abbreviations

SCFAs:

Short-chain fatty acids

LPS:

Lipopolysaccharide

FMT:

Fecal microbial transplantation

RCTs:

Randomized controlled clinical trials

RCDI:

Recurrent Clostridioides difficile infection

IBD:

Inflammatory bowel disease

UC:

Ulcerative colitis

HE:

Hepatic encephalopathy

PSC:

Primary sclerosing cholangitis

GIT:

Gastrointestinal tract

US:

United States

IBS:

Irritable bowel syndrome

CNS:

Central nervous system

ENS:

Enteric nervous system

CD:

Crohn’s disease

COVID-19:

Coronavirus disease 2019

SARS-CoV-2:

Severe acute respiratory syndrome coronavirus 2

T2D:

Type 2 diabetes

BED:

Binge eating disorder

References

  1. Wu X, Xia Y, He F, et al. Intestinal mycobiota in health and diseases: from a disrupted equilibrium to clinical opportunities. Microbiome. 2021;9:60.

    Article  Google Scholar 

  2. Li XV, Leonardi I, Iliev ID. Gut mycobiota in immunity and inflammatory disease. Immunity. 2019;50:1365–79.

    Article  Google Scholar 

  3. Woo V, Alenghat T. Epigenetic regulation by gut microbiota. Gut Microbes. 2022;14:2022407.

    Article  Google Scholar 

  4. Zheng D, Liwinski T, Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res. 2020;30:492–506.

    Article  Google Scholar 

  5. Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med. 2016;375:2369–79.

    Article  Google Scholar 

  6. Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease. Nat Rev Microbiol. 2021;19:55–71.

    Article  Google Scholar 

  7. Jakobsson HE, Abrahamsson TR, Jenmalm MC, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut. 2014;63:559–66.

    Article  Google Scholar 

  8. Rodríguez JM, Murphy K, Stanton C, et al. The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis. 2015;26:26050.

    Google Scholar 

  9. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65.

    Article  Google Scholar 

  10. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–14.

    Article  Google Scholar 

  11. Valdes AM, Walter J, Segal E, et al. Role of the gut microbiota in nutrition and health. BMJ. 2018;361:k2179.

    Article  Google Scholar 

  12. Shafquat A, Joice R, Simmons SL, et al. Functional and phylogenetic assembly of microbial communities in the human microbiome. Trends Microbiol. 2014;22:261–6.

    Article  Google Scholar 

  13. Allegretti JR, Kassam Z, Osman M, et al. The 5D framework: a clinical primer for fecal microbiota transplantation to treat Clostridium difficile infection. Gastrointest Endosc. 2018;87:18–29.

    Article  Google Scholar 

  14. van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368:407–15.

    Article  Google Scholar 

  15. Allegretti JR, Mullish BH, Kelly C, et al. The evolution of the use of faecal microbiota transplantation and emerging therapeutic indications. Lancet. 2019;394(10196):420–31.

    Article  Google Scholar 

  16. Rossen NG, Fuentes S, van der Spek MJ, et al. Findings from a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology. 2015;149:110-118.e4.

    Article  Google Scholar 

  17. Moayyedi P, Surette MG, Kim PT, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. 2015;149:102–9.

    Article  Google Scholar 

  18. Paramsothy S, Kamm MA, Kaakoush NO, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017;389:1218–28.

    Article  Google Scholar 

  19. Costello SP, Hughes PA, Waters O, et al. Effect of fecal microbiota transplantation on 8-week remission in patients with ulcerative colitis: a randomized clinical trial. JAMA. 2019;321:156–64.

    Article  Google Scholar 

  20. Bajaj JS, Fagan A, Gavis EA, et al. Long-term outcomes of fecal microbiota transplantation in patients with cirrhosis. Gastroenterology. 2019;156:1921-1923.e3.

    Article  Google Scholar 

  21. Bajaj JS, Salzman NH, Acharya C, et al. Fecal microbial transplant capsules are safe in hepatic encephalopathy: a phase 1, randomized, placebo-controlled trial. Hepatology. 2019;70:1690–703.

    Article  Google Scholar 

  22. Shah A, Macdonald GA, Morrison M, et al. Targeting the gut microbiome as a treatment for primary sclerosing cholangitis: a conceptional framework. Am J Gastroenterol. 2020;115:814–22.

    Article  Google Scholar 

  23. Mocanu V, Zhang Z, Deehan EC, et al. Fecal microbial transplantation and fiber supplementation in patients with severe obesity and metabolic syndrome: a randomized double-blind, placebo-controlled phase 2 trial. Nat Med. 2021;27:1272–9.

    Article  Google Scholar 

  24. Yu EW, Gao L, Stastka P, et al. Fecal microbiota transplantation for the improvement of metabolism in obesity: the FMT-TRIM double-blind placebo-controlled pilot trial. PLoS Med. 2020;17:e1003051.

    Article  Google Scholar 

  25. Zhao Z, Ning J, Bao XQ, et al. Fecal microbiota transplantation protects rotenone-induced Parkinson’s disease mice via suppressing inflammation mediated by the lipopolysaccharide-TLR4 signaling pathway through the microbiota-gut-brain axis. Microbiome. 2021;9:226.

    Article  Google Scholar 

  26. Hou YF, Shan C, Zhuang SY, et al. Gut microbiota-derived propionate mediates the neuroprotective effect of osteocalcin in a mouse model of Parkinson’s disease. Microbiome. 2021;9:34.

    Article  Google Scholar 

  27. Kang DW, Adams JB, Gregory AC, et al. Microbiota transfer therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: an open-label study. Microbiome. 2017;5:10.

    Article  Google Scholar 

  28. Yang J, Fu X, Liao X, et al. Effects of gut microbial-based treatments on gut microbiota, behavioral symptoms, and gastrointestinal symptoms in children with autism spectrum disorder: a systematic review. Psychiatry Res. 2020;293:113471.

    Article  Google Scholar 

  29. Sorboni SG, Moghaddam HS, Jafarzadeh-Esfehani R, et al. A comprehensive review on the role of the gut microbiome in human neurological disorders. Clin Microbiol Rev. 2022;35:e0033820.

    Article  Google Scholar 

  30. Aria M, Cuccurullo C. Bibliometrix: an R-tool for comprehensive science mapping analysis. J Informetrics. 2017;11:959–75.

    Article  Google Scholar 

  31. Chen C. Searching for intellectual turning points: progressive knowledge domain visualization. Proc Natl Acad Sci USA. 2004;101(Suppl 1(Suppl 1)):5303–10.

    Article  Google Scholar 

  32. Chen C, Dubin R, Kim MC. Emerging trends and new developments in regenerative medicine: a scientometric update (2000–2014). Expert Opin Biol Ther. 2014;14:1295–317.

    Article  Google Scholar 

  33. Gough E, Shaikh H, Manges AR. Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent Clostridium difficile infection. Clin Infect Dis. 2011;53:994–1002.

    Article  Google Scholar 

  34. McDonald LC, Gerding DN, Johnson S, et al. Clinical practice guidelines for Clostridium difficile infection in adults and children: 2017 update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clin Infect Dis. 2018;66:e1–48.

    Article  Google Scholar 

  35. Bakken JS, Borody T, Brandt LJ, et al. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol. 2011;9:1044–9.

    Article  Google Scholar 

  36. Routy B, Le Chatelier E, Derosa L, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 2018;359:91–7.

    Article  Google Scholar 

  37. Quraishi MN, Widlak M, Bhala N, et al. Systematic review with meta-analysis: the efficacy of faecal microbiota transplantation for the treatment of recurrent and refractory Clostridium difficile infection. Aliment Pharmacol Ther. 2017;46:479–93.

    Article  Google Scholar 

  38. Kao D, Roach B, Silva M, et al. Effect of oral capsule– vs. colonoscopy-delivered fecal microbiota transplantation on recurrent Clostridium difficile infection: a randomized clinical trial. JAMA. 2017;318:1985–93.

    Article  Google Scholar 

  39. Cammarota G, Ianiro G, Tilg H, et al. European consensus conference on faecal microbiota transplantation in clinical practice. Gut. 2017;66:569–80.

    Article  Google Scholar 

  40. Kassam Z, Lee CH, Yuan Y, Hunt RH. Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol. 2013;108:500–8.

    Article  Google Scholar 

  41. Surawicz CM, Brandt LJ, Binion DG, et al. Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol. 2013;108(4):478–99.

    Article  Google Scholar 

  42. Gopalakrishnan V, Spencer CN, Nezi L, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 2018;359:97–103.

    Article  Google Scholar 

  43. Kootte RS, Levin E, Salojärvi J, et al. Improvement of insulin sensitivity after lean donor feces in metabolic syndrome is driven by baseline intestinal microbiota composition. Cell Metab. 2017;26:611-619.e6.

    Article  Google Scholar 

  44. Bajaj JS, Kassam Z, Fagan A, et al. Fecal microbiota transplant from a rational stool donor improves hepatic encephalopathy: a randomized clinical trial. Hepatology. 2017;66:1727–38.

    Article  Google Scholar 

  45. Shono Y, Docampo MD, Peled JU, et al. Increased GVHD-related mortality with broad-spectrum antibiotic use after allogeneic hematopoietic stem cell transplantation in human patients and mice. Sci Transl Med. 2016;8:339ra71.

    Article  Google Scholar 

  46. Chen C, Hu Z, Liu S, et al. Emerging trends in regenerative medicine: a scientometric analysis in CiteSpace. Expert Opin Biol Ther. 2012;12:593–608.

    Article  Google Scholar 

  47. Gill SR, Pop M, Deboy RT, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312:1355–9.

    Article  Google Scholar 

  48. Brandt LJ, Aroniadis OC. An overview of fecal microbiota transplantation: techniques, indications, and outcomes. Gastrointest Endosc. 2013;78:240–9.

    Article  Google Scholar 

  49. Kelly CR, Kahn S, Kashyap P, et al. Update on fecal microbiota transplantation 2015: indications, methodologies, mechanisms, and outlook. Gastroenterology. 2015;149:223–37.

    Article  Google Scholar 

  50. Leshem A, Horesh N, Elinav E. Fecal microbial transplantation and its potential application in cardiometabolic syndrome. Front Immunol. 2019;10:1341.

    Article  Google Scholar 

  51. Brandt LJ. Fecal microbiota therapy with a focus on Clostridium difficile infection. Psychosom Med. 2017;79:868–73.

    Article  Google Scholar 

  52. Sokol H, Landman C, Seksik P, et al. Fecal microbiota transplantation to maintain remission in Crohn’s disease: a pilot randomized controlled study. Microbiome. 2020;8:12.

    Article  Google Scholar 

  53. El-Salhy M, Hatlebakk JG, Gilja OH, et al. Efficacy of faecal microbiota transplantation for patients with irritable bowel syndrome in a randomised, double-blind, placebo-controlled study. Gut. 2020;69:859–67.

    Article  Google Scholar 

  54. Cammarota G, Ianiro G, Kelly CR, et al. International consensus conference on stool banking for faecal microbiota transplantation in clinical practice. Gut. 2019;68:2111–21.

    Article  Google Scholar 

  55. DeFilipp Z, Bloom PP, Torres Soto M, et al. Drug-resistant E. coli bacteremia transmitted by fecal microbiota transplant. N Engl J Med. 2019;381:2043–50.

    Article  Google Scholar 

  56. Jiang ZD, Ajami NJ, Petrosino JF, et al. Randomised clinical trial: faecal microbiota transplantation for recurrent Clostridum difficile infection—fresh, or frozen, or lyophilised microbiota from a small pool of healthy donors delivered by colonoscopy. Aliment Pharmacol Ther. 2017;45:899–908.

    Article  Google Scholar 

  57. Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature. 2011;473:174–80.

    Article  Google Scholar 

  58. Wen L, Ley RE, Volchkov PY, et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature. 2008;455:1109–13.

    Article  Google Scholar 

  59. Rosvall M, Bergstrom CT. Mapping change in large networks. PLoS ONE. 2010;5:e8694.

    Article  Google Scholar 

  60. Haifer C, Paramsothy S, Kaakoush NO, et al. Lyophilised oral faecal microbiota transplantation for ulcerative colitis (LOTUS): a randomised, double-blind, placebo-controlled trial. Lancet Gastroenterol Hepatol. 2022;7:141–51.

    Article  Google Scholar 

  61. Yao Y, Cai X, Fei W, et al. The role of short-chain fatty acids in immunity, inflammation and metabolism. Crit Rev Food Sci Nutr. 2022;62:1–12.

    Article  Google Scholar 

  62. Parada Venegas D, De la Fuente MK, Landskron G, et al. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol. 2019;10:277.

    Article  Google Scholar 

  63. Rios-Covian D, González S, Nogacka AM, et al. An overview on fecal branched short-chain fatty acids along human life and as related with body mass index: associated dietary and anthropometric factors. Front Microbiol. 2020;11:973.

    Article  Google Scholar 

  64. Cook SI, Sellin JH. Review article: short chain fatty acids in health and disease. Aliment Pharmacol Ther. 1998;12:499–507.

    Article  Google Scholar 

  65. Gill PA, van Zelm MC, Muir JG, et al. Review article: short chain fatty acids as potential therapeutic agents in human gastrointestinal and inflammatory disorders. Aliment Pharmacol Ther. 2018;48:15–34.

    Article  Google Scholar 

  66. Pluznick JL. Microbial short-chain fatty acids and blood pressure regulation. Curr Hypertens Rep. 2017;19:25.

    Article  Google Scholar 

  67. Tahara Y, Yamazaki M, Sukigara H, et al. Gut microbiota-derived short chain fatty acids induce circadian clock entrainment in mouse peripheral tissue. Sci Rep. 2018;8:1395.

    Article  Google Scholar 

  68. Erny D, de Angelis ALH, Prinz M. Communicating systems in the body: how microbiota and microglia cooperate. Immunology. 2017;150:7–15.

    Article  Google Scholar 

  69. Bell KJ, Saad S, Tillett BJ, et al. Metabolite-based dietary supplementation in human type 1 diabetes is associated with microbiota and immune modulation. Microbiome. 2022;10:9.

    Article  Google Scholar 

  70. Dąbek-Drobny A, Kaczmarczyk O, Woźniakiewicz M, et al. Association between fecal short-chain fatty acid levels, diet, and body mass index in patients with inflammatory bowel disease. Biology. 2022;11:108.

    Article  Google Scholar 

  71. Chen SJ, Chen CC, Liao HY, et al. Association of fecal and plasma levels of short-chain fatty acids with gut microbiota and clinical severity in Parkinson disease patients. Neurology. 2022. https://doi.org/10.1212/WNL.0000000000013225.

    Article  Google Scholar 

  72. De Pablo-Fernandez E, Gebeyehu GG, Flain L, et al. The faecal metabolome and mycobiome in Parkinson’s disease. Parkinsonism Relat Disord. 2022;95:65–9.

    Article  Google Scholar 

  73. Derrien M, Vaughan EE, Plugge CM, et al. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol. 2004;54:1469–76.

    Article  Google Scholar 

  74. Collado MC, Derrien M, Isolauri E, et al. Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl Environ Microbiol. 2007;73:7767–70.

    Article  Google Scholar 

  75. Derrien M, Collado MC, Ben-Amor K, et al. The mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol. 2008;74:1646–8.

    Article  Google Scholar 

  76. Yan J, Sheng L, Li H. Akkermansia muciniphila: is it the Holy Grail for ameliorating metabolic diseases? Gut Microbes. 2021;13:1984104.

    Article  Google Scholar 

  77. Zhang J, Ni Y, Qian L, et al. Decreased abundance of Akkermansia muciniphila leads to the impairment of insulin secretion and glucose homeostasis in lean type 2 diabetes. Adv Sci. 2021;8:e2100536.

    Article  Google Scholar 

  78. Dao MC, Belda E, Prifti E, et al. Akkermansia muciniphila abundance is lower in severe obesity, but its increased level after bariatric surgery is not associated with metabolic health improvement. Am J Physiol Endocrinol Metab. 2019;317:E446–59.

    Article  Google Scholar 

  79. Borgo F, Verduci E, Riva A, et al. Relative abundance in bacterial and fungal gut microbes in obese children: a case control study. Child Obes. 2017;13:78–84.

    Article  Google Scholar 

  80. Thingholm LB, Rühlemann MC, Koch M, et al. Obese individuals with and without type 2 diabetes show different gut microbial functional capacity and composition. Cell Host Microbe. 2019;26:252-264.e10.

    Article  Google Scholar 

  81. Leyrolle Q, Cserjesi R, Mulders MDGH, et al. Specific gut microbial, biological, and psychiatric profiling related to binge eating disorders: a cross-sectional study in obese patients. Clin Nutr. 2021;40:2035–44.

    Article  Google Scholar 

  82. Valentini V, Silvestri V, Marraffa F, et al. Gut microbiome profile in psoriatic patients treated and untreated with biologic therapy. J Dermatol. 2021;48:786–93.

    Article  Google Scholar 

  83. Beaumont W. Nutrition Classics. Experiments and observations on the gastric juice and the physiology of digestion. By William Beaumont. Plattsburgh. Printed by F. P. Allen. 1833. Nutr Rev. 1977;35:144–5.

    Article  Google Scholar 

  84. Cleary JL, Condren AR, Zink KE, et al. Calling all hosts: Bacterial communication in situ. Chem. 2017;2:334–58.

    Article  Google Scholar 

  85. Clemente JC, Ursell LK, Parfrey LW, et al. The impact of the gut microbiota on human health: an integrative view. Cell. 2012;148:1258–70.

    Article  Google Scholar 

  86. Karst SM. The influence of commensal bacteria on infection with enteric viruses. Nat Rev Microbiol. 2016;14:197–204.

    Article  Google Scholar 

  87. Turroni S, Brigidi P, Cavalli A, et al. Microbiota-host transgenomic metabolism, bioactive molecules from the inside. J Med Chem. 2018;61:47–61.

    Article  Google Scholar 

  88. Cryan JF, O’Riordan KJ, Cowan CSM, et al. The microbiota-gut-brain axis. Physiol Rev. 2019;99:1877–2013.

    Article  Google Scholar 

  89. Tillisch K, Labus J, Kilpatrick L, et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology. 2013;144:1394-1401.e14014.

    Article  Google Scholar 

  90. Smith AP, Sutherland D, Hewlett P. An investigation of the acute effects of oligofructose-enriched inulin on subjective wellbeing, Mood and Cognitive Performance. Nutrients. 2015;7:8887–96.

    Article  Google Scholar 

  91. Lew LC, Hor YY, Yusoff NAA, et al. Probiotic Lactobacillus plantarum P8 alleviated stress and anxiety while enhancing memory and cognition in stressed adults: a randomised, double-blind, placebo-controlled study. Clin Nutr. 2019;38:2053–64.

    Article  Google Scholar 

  92. Akbari E, Asemi Z, Daneshvar Kakhaki R, et al. Effect of probiotic supplementation on cognitive function and metabolic status in Alzheimer’s disease: a randomized, double-blind and controlled trial. Front Aging Neurosci. 2016;8:256.

    Article  Google Scholar 

  93. Grimaldi R, Gibson GR, Vulevic J, et al. A prebiotic intervention study in children with autism spectrum disorders (ASDs). Microbiome. 2018;6:133.

    Article  Google Scholar 

  94. Miyaoka T, Kanayama M, Wake R, et al. Clostridium butyricum MIYAIRI 588 as adjunctive therapy for treatment-resistant major depressive disorder: a prospective open-label trial. Clin Neuropharmacol. 2018;41:151–5.

    Article  Google Scholar 

  95. Colica C, Avolio E, Bollero P, et al. Evidences of a new psychobiotic formulation on body composition and anxiety. Mediators Inflamm. 2017;2017:5650627.

    Article  Google Scholar 

  96. Chong HX, Yusoff NAA, Hor YY, et al. Lactobacillus plantarum DR7 alleviates stress and anxiety in adults: a randomised, double-blind, placebo-controlled study. Benef Microbes. 2019;10:355–73.

    Article  Google Scholar 

  97. Castro-Nallar E, Bendall ML, Pérez-Losada M, et al. Composition, taxonomy and functional diversity of the oropharynx microbiome in individuals with schizophrenia and controls. PeerJ. 2015;3:e1140.

    Article  Google Scholar 

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Acknowledgements

We are grateful to Xiyuan Hospital of the Chinese Academy of Traditional Chinese Medicine for their support of this work and the free software Biblioshiny and CiteSpace.

Funding

This work was supported by the National Natural Science Foundation of China (No. 81830118), China Academy of Chinese Medical Sciences Innovation Fund (NO.CI2021A01012), State Administration of Traditional Chinese Medicine Digestive Refractory Disease Inheritance and Innovation Team Project (NO. ZYYCXTD-C-202010), National Natural Science Foundation of China (No.82074420) and Young Elite Scientists Sponsorship Program by CAST (No.2019-QNRC1-02).

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  1. Jing Ma and Ting Chen contributed equally to this work.

Authors and Affiliations

  1. Institute of Digestive Diseases, Xiyuan Hospital of China Academy of Chinese Medical Sciences, Beijing, 100091, China

    Jing Ma, Ting Chen, Xiangxue Ma, Beihua Zhang, Jiaqi Zhang, Jinke Huang, Fengyun Wang & Xudong Tang

  2. Department of Gastroenterology, Shenzhen Hospital of Traditional Chinese Medicine, Shenzhen, China

    Lin Xu

  3. Department of Gastroenterology, Peking University Traditional Chinese Medicine Clinical Medical School (Xiyuan), Beijing, China

    Yifan Wang & Zhihong Liu

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Contributions

JM and TC envisioned this study. JM, LX, YW collected the data. JH and ZL checked the data. JM and BZ analyzed the data. JM wrote the manuscript. XM, JZ, FW and XT reviewed and revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Fengyun Wang or Xudong Tang.

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Ma, J., Chen, T., Ma, X. et al. Comprehensive bibliometric and visualized analysis of research on fecal microbial transplantation published from 2000 to 2021. BioMed Eng OnLine 21, 78 (2022). https://doi.org/10.1186/s12938-022-01046-y

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Keywords

  • Fecal microbial transplantation
  • Bibliometric
  • Visualized analysis
  • Biblioshiny
  • CiteSpace

BioMedical Engineering OnLine

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