Bibliometric analysis of the global research trends of Klebsiella studies from 2000-2019 [version 1; peer review: awaiting peer review]

Background: Klebsiella are major opportunistic bacteria pathogens known to cause a series of severe nosocomial infections. This study reports the global research outputs of Klebsiella research studies and explores the key areas within Klebsiella research studies. Methods: Data in published articles on Klebsiella research studies from 2000 to 2019 were recovered from a scientific data bank known as Web of Science (WoS). Bibliometric tools together with Microsoft Excel 2016 were employed to analyse the top ranked journals, trend topics, title word occurrences, global cited documents, most relevant authors, most relevant countries by corresponding authors, most cited countries, country collaboration networks, title word occurrence, trend topics, most relevant affiliations, and conceptual structural map. Results: An aggregate of 6,047 published papers were retreived from Web of Science (WoS) and the analyses showed that Antimicrobial Agents and Chemotherapy was the top journal in research on Klebsiella with an aggregate of 441 published research documents, followed by Jong G, 2009 as the major global cited article with a total of 1339 citations, Li J as the most relevant author with 72 publications, China as the most relevant country by corresponding author with a total of 1,303 articles and the USA utmost cited research articles, and most significant researchers in Klebsiella research for the studied period (2000-2019).


Introduction
Klebsiella are non-motile, typically encapsulated rod-shaped Gram-negative bacteria that belong to the family Enterobacteriaceae and are generally facultative anaerobic. The genus Klebsiella are significantly opportunistic pathogens connected with several severe nosocomial bacterial infections including pneumonia, septicaemia and urinary tract infections (Chang et al., 2021). Klebsiella species are categorized into four species, and this includes Klebsiella planticola, K. pneumonia, K. terrigena and K. oxytoca. K. pneumonia consist of three subspecies such as K. pneumoniae subsp. Rhinoscleromatis, K. pneumoniae subsp. Ozaenae and K. pneumoniae subsp. pneumoniae (Li et al., 2004). However, the most common species within the genus Klebsiella are K. pneuminia and K. oxytoca (Ebomah and Okoh, 2020) while K. planticola and K. terrigena, are less common species (El Fertas et al., 2013). Among the well-known Klebsiella species, K. pneumoniae and K. oxytoca are the two clinically significant species associated with human infections (Mondal et al., 2019). K. pneumoniae is primarily responsible for healthcare and community associated infections while K. oxytoca is an opportunistic pathogen that causes most hospital acquired infections (Izdebski et al., 2015).
Among illnesses caused by Klebsiella species, K. pneumoniae is accountable for over 70% of these infections (Quansah et al., 2019). For many years, K. pneumoniae has been known as a major opportunistic bacterial pathogen colonizing the skin, respiratory and gastrointestinal tract causing series of severe community-acquired and nosocomial infections such as meningitis, wound, bloodstream as well as urinary tract infections mainly in the elderly, immunocompromised persons, and neonates (Daoud, et al., 2018;Holt et al., 2015). K. pneumoniae is a well-known hospital-acquired pathogen that is associated with the rise in patient illness and death (Cabral et al., 2012). In the hospital setting, Klebsiella infection can spread generally through medical equipment, direct personal contacts, and contaminated environments (Runcharoen et al., 2017). In hospital environments, K. pneumoniae is considered as one of the major agents of infectious diseases and an important menace to public health as a result of their high rates of resistance to antimicrobial agents (Sakkas et al., 2019). In addition to the threat that these pathogens pose to public health in clinical settings, K. pneumonia is regularly found in foods including meat, fish, raw vegetables and powdered infant formula and this microorganism has been classified as a vital food-borne pathogen (Kim et al., 2015;Davis and Price, 2016). According to the World Health Organization (WHO) (2004) guidelines on microbes, K. pneumoniae has been included in the hazard detection category "B" in powdered infant formula. In recent years, a rise in the number of food-borne bacterial outbreak cases caused by K. pneumoniae have been reported in several nations (Calbo et al., 2011;Zhang et al., 2018). Furthermore, reports have also indicated that some of these Klebsiella related infections which sometimes involve antimicrobial-resistant strains are vectored by insect pests including cockroaches and house flies (Davari et al., 2010;Ranjbar et al., 2016). Therefore, bibliometric studies on Klesiella species are vital as it is becoming increasingly challenging to remain up to date with everything that is being published (Briner and Denyer, 2012). Hence, assessing published documents on Klebsiella research is important and such studies are conducted using bibliometric indicators that help recognize or identify popular research topics, countries contributions, international collaboration, and research trends in the field. In general, several publications including the reports of Chou (2009), Khatun and Ahmed (2011) and Loomes and van Zanten (2013) have been conducted using bibliometric tools to assess precise bacteria pathogens research in many parts of the world.
Bibliometrics tools are used in interdisciplinary sciences and assess a knowledge domain through statistical and mathematical approaches (Merigó, 2016). It is a technique used generally to identify the development of a certain field (Železnik et al., 2017). This method of data analysis is used to analyse scientific outputs (Moral-Munoz et al., 2019). In addition, bibliometric analysis plays a key role in strategic planning and development of research in a knowledge domain (Meo et al., 2013) and it also gives an understanding of the size and growth of scientific literature in the discipline of concern within a specified time frame (López-Pinero and Terrada, 1992). The most recognizable advantage of bibliometrics analysis is that it allows researchers to perform detailed investigations of knowledge domains of interest in many areas such as analyzing geographical distribution, co-citations, citations, word frequency and also draw suitable conclusions. To date, bibliometrics analysis has been broadly used in co-authorship analysis (Sweileh et al., 2016), hotspot investigation (Yeung, et al., 2017) and in co-citation study (Merigó and Yang, 2017). This study appears to be the first bibliometric work on Klebsiella studies from 2000-2019.

Methods
Peer-reviewed published studies on Klebsiella and Klebsiella related research between 2000-2019 were mined from the WoS database. The decision to use WoS was made because it's the most frequently used database for bibliometric studies (Huang et al., 2019). The data was analyzed by bibliometric indicators (bibliometrix R-package) in R-studio v.3.4.1 (Ariaa and Cuccurullo, 2012). Searches were completed on July 20, 2020. A search was carried out to extract publications dealing with Klebsiella research articles. For the purpose of this study, published articles on Klebsiella research studies in WoS were retrieved and analyzed. To obtain the required data, we used the following search terms (a) "Klebsiella*" OR "Klebsiella pneumonia*" OR "Klebsiella oxytoca*" in the WoS search engine for our title search; (b) the time span was fixed from 2000 to 2019; (c) the retrieved papers were refined by excluding articles published in meetings, peer reviewed journals, letters, editorial material, corrections and news items; and finally (d) the retrieved data were exported to Excel for data analysis. In this study, the search approach was based on searching for the necessary terms in the article titles to increase accuracy and reduce incorrect results. The search words included "Klebsiella*" OR "Klebsiella pneumonia*" OR "Klebsiella oxytoca*". The asterisk (*) sign was used to retrieve papers with the word Klebsiella or Klebsiella pneumonia or Klebsiella oxytoca and all the documents were saved in a BibTeX file.

Results
A total of 6,047 papers were retrieved from WoS between 2000-2019 with a mean publication of 7.21 documents per year, an average sum of 22.53 citations per document and an average number of 2.566 citations per year per document. Articles (n=5936) were the most retrieved document type followed by article proceedings papers (n=90), article book chapters (n=13), article early access (n=6) and article data papers (n=2). These documents included 21, 213 authors with 37, 307 author appearances, 54 single-authored documents and 21,159 multiple authored publications. Table 1 shows the main information on the recovered articles from WoS on Klebsiella research studies between 2000-2019. The full dataset can be found under Underlying data.

Leading journals
The top leading journals on Klebsiella research outputs retrieved from WoS database with their number of published articles are shown in Table 2    Most relevant authors Table 4  Top 20 most relevant countries in Klebsiella research outputs Table 5

Countries collaboration networks
Countries' collaboration networks on Klebsiella research outputs in the retrieved documents from WoS between 2000-2019 revealed two clusters (blue and red) of collaboration networks with pathways ranging from 3 to 30 (Figure 1). A single node denotes the different country and the diameter of each node signifies the country's collaboration strength with other countries while the strokes/lines indicate collaboration networks between each country. In both clusters, the  United Kingdom had the highest number of collaborations (n=21), followed by China (n=20) while Iran had the least collaborations (n=3). In the blue cluster, the majority of the countries were in Europe and, in the red cluster, South Africa is the only African country on the list.  Case Western University (n=193), University of Pittsburgh (n=189), National Chang Kung University (n=171), University of Sao Paulo (n=162) and National Taiwan University (n=154).

Conceptual structural map
The analysis of the conceptual frame map on Klebsiella research outputs between 2000-2019 by factorial multiple correspondence revealed seven clusters of sizes 13, 12, 8, 5, 4, 3 and 3 with components centered on spread,  dissemination, plasmid, genes, outbreaks, resistant, identification, strains, therapy, colonization, blood stream infection etc. (Figure 3). The clusters explained the mode of identification, seriousness of infection, types of infections, type of bacteria and impact of infection. The blue cluster has polymerase chain reaction (PCR) as an indicator for identification, the red cluster has infection as an indicator of outcome, the purple cluster has Gram negative as a pointer of the class of bacteria, the orange has liver abscess as disease related terms.

Title word occurrence
Title word occurrence was assessed based on the occurrence of each word in the titles of Klebsiella publications between 2000-2019 ( Figure 4). The highest title word that occurred in the recovered articles from WoS showed that Klebsiella (n=6112) had the highest word occurrence, followed by pneumonia (n=4956), isolate (n=805), coli (n=735), Escherichia (n=729), resistance (n=688), and clinical (n=600) etc.

Trend topics
Trend topics are frequently used keywords used over a period of time. The top 30 trend topics in this subject area were obtained along with their year and frequency as showed in Figure 5. The strength of the trend topics are indicated by the frequency of occurrence of the words over time. The top four trend topics based on frequency of occurrence and the year of published articles on Klebsiella research outputs between 2000-2019 are Enterobacteriaceae (n=1233, year=2015), resistance (n=869, year=2013), epidemiology (n=777, year=2014) and infection (n=517, year=2015). In relation to the colour, individual trend topics and years were classified into two colours: blue signifies the years while yellow signifies the rate of occurrence.

Discussion
Bibliometrics analysis is attracting attention in the scientific community (Alvarez-Betancourt and Garcia-Silvente, 2014). Currently, bibliometrics has advanced rapidly and it is applied to various study fields because of its effective approach for measuring the qualities of a designated research (Shang et al., 2015). Furthermore, it is a method that deals with the widespread intersection and combination of mathematics, statistics, information science and philology in a definite area (He et al., 2017). It can also be used to analyze the advancement of a particular research trend which can be shown by bibliometric indicators (Wang et al., 2020). This method of assessment is significant as a result of its distinctive advantages with its vast array of applications in different research areas including sustainable energy (Hache and Palle, 2019), economics and business sciences (Merigo et al., 2016) and vague decision making (Liu and Liao, 2017). Bibliometrics has also been conducted in several fields of research such as tropical medicine and citation evaluation (Flaherty and Browne, 2016), and research topics in periprosthetic joint infection (Li et al., 2020). Bibliometric analysis of retrieved documents from the WoS on Klebsiella research outputs between 2000-2019 was conducted to ascertain the research trends and gaps in research outputs and to direct future research. From the analysis on Klebsiella research outputs between 2000-2019, a total of 6,047 articles were published and the rate of articles published was high compared with the rate of publications in other subject areas. The study found that the leading journals on Klebsiella research outputs were published in credible research journals with increased impact factor such as Antimicrobial Agents and Chemotherapy (n=441), Journal of Antimicrobial Chemotherapy (n=234) and Journal of Clinical Microbiology (n=163). In the same vein, the top most cited published articles on Klebsiella research outputs were published in journals with increased impact factor and the total citations were between 335 and 1,339.
The top most cited articles with 1,339 total citations belong to Yong et al. (2009), who published his research in Antimicrobial Agents and Chemotherapy, followed by Yigit et al. (2001), who published his research in Antimicrobial Agents and Chemotherapy with 960 total citations, Diancourt et al. (2005) published in Journal of Clinical Microbiology with 760 total citations and Tumbarello et al. (2012), published in Clinical Infectious Diseases with total citation of 575 (Table 3). An aggregate number of article citations and the journal impact factors are part of the pivotal criteria that is utilized to rate the scientific quality of a paper (Sobhy, 2016) and citation indices are commonly recognized as an identifiable amount (Tsai et al., 2006). As indicated by statistics assessment, the sum of citations of the top most cited research outputs is vital due to the quality of the articles. The results from the analysis also showed that the top 20 most relevant authors had between 40 and 72 publications and Li J had 72 publications on Klebsiella research outputs in the documents retrieved from WoS followed by Wang Y with 67 publications and Li Y with 64 publications (Table 4).  (2019), the term countries collaborations is used to describe research papers that have been published through the collaboration of researchers from at least two different countries. Figure 1 reveals international collaboration links for 38 selected major countries involved in Klebsiella research. According to Kyvik and Reymert's report (2017), most academic research is carried out in the form of collaborative effort and it is rational that two or more people have the potential or skills to do better work as a group than individually. The results also show that most research societies have already designed a closed collaboration link specifically among the scientific developed nations and our finding is in accordance with Zhang et al.'s (2019) report. This result also supports Van Raan's (2004) research, as they state that research collaboration has a positive influence on published results. Another report from Glynatsi and Knight (2021) also found that research collaboration has a long tradition in experimental sciences, and it has been proven to be productive. The academic success of universities is determined or measured with the number of publications and citations (Taşkın and Al, 2014). Results from the analysis of the most relevant affiliations (Figure 2), shows the top most leading institutions in relation to the number of published articles on Klebsiella research and Zhejiang University (n=243) had the highest number of published articles, followed by Case Western Reserve University (n=193), University of Pittsburgh (n=189), National Cheng Kung University (n=171) and University of Sao Paulo (n=162). The term affiliation was used to describe the authors' collaboration with other authors in other institutions judging from the number of published articles on the study topic via partnership of authors between two or more universities. Furthermore, the evaluation of the conceptual frame map through a co-word assessment indicated seven clusters of thematic links. In essence, the results from this study differ from Galvão et al.'s (2018) study as their results showed three interrelated clusters. In as much as several bibliometrics works have been published, one of the major strengths of this study is that it is the first to report on the global research trends of Klebsiella studies from 2000-2019. There are some drawbacks to bibliometric study as previously reported by Azad and Parvin (2022)

Conclusion
In conclusion, this study provides information on the top ranked journals, most cited research publications, and relevant researchers within published Klebsiella research articles between 2000-2019. It also provides insights into authors' research outputs, countries' collaborations, and important collaborating networks on Klebsiella research. This study also explains and defines the influence of nosocomial infection and Klebsiella research. The benefits of publishing with F1000Research: Your article is published within days, with no editorial bias • You can publish traditional articles, null/negative results, case reports, data notes and more • The peer review process is transparent and collaborative • Your article is indexed in PubMed after passing peer review • Dedicated customer support at every stage • For pre-submission enquiries, contact research@f1000.com