Introduction
Nontuberculous mycobacteria (NTM) are ubiquitous, encompassing over 200 species of mycobacteria [1]. NTM can cause infections and diseases in various body parts, including the lungs, lymphatic system, skin, and soft tissues, and can cause disseminated disease [2,3]. Species causing NTM diseases vary with climate and environmental factors, leading to research efforts across different countries and regions [4,5]. Personal behavior can also affect the risk of NTM disease; the clinical characteristics of patients differ with age and sex [6,7]. Therefore, research regarding NTM is conducted across various fields, warranting an organized approach to gain comprehensive insight.
Bibliometric analysis is a valuable tool that uses published articles to obtain quantitative insight into the characteristics of diseases [8]. This method has been used often in various research fields, such as in cardiology and in the management of infectious diseases, such as tuberculosis (TB) [9-11]. While some studies have analyzed the trends in NTM research [12], none have focused specifically on South Korea. Since diseases caused by NTM vary by region, collecting relevant country-specific information can help identify the hotspots and gaps in current research. This information could guide future efforts to improve the management of diseases caused by NTM in South Korea. Therefore, we aimed to conduct a bibliometric analysis to identify the characteristics of NTM research in South Korea, providing a detailed overview and highlighting key trends and contributions in this area.
Materials and Methods
1. Collected information
We searched the Web of Science database for articles related to NTM authored by Koreans up to March 2023. The search was performed using the following search terms: ‘nontuberculous mycobacteri,*’ ‘non-tuberculous,’ ‘avium,’ ‘intracellulare,’ ‘abscessus,’ ‘kansasii,’ and ‘fortuitum.’ Articles were included if they had at least one Korean author affiliated with a Korean institution, regardless of the author’s position.
For each article, we gathered details on the first and corresponding authors, journal name, year of publication, 5-year impact factor (2022), type of article, study design, research area, total number of citations, citations per year, affiliated research institute, and funding sources.
2. Article classification and analysis
The articles were categorized using an existing classification method [13,14]. They were broadly classified into one of the following categories: (1) basic research, including biochemistry, cell studies, genetic engineering and gene sequencing, genetic studies, animal studies, and material development. The ambiguity in the classification of biochemistry, was addressed by defining this term as the study of biological processes at the molecular level, including the chemical processes within and related to living organisms; (2) clinical research, encompassing case reports, case series, cross-sectional studies, non-comparative studies, before-and-after studies, case-control studies, retrospective or prospective cohort studies, and randomized controlled trials. A non-comparative study was defined as an observational study focused on a single group without comparison to another group; and (3) secondary research, which included reviews and systematic reviews with meta-analyses. Articles that could not be classified were grouped under ‘others.’
Additionally, the articles were further classified based on their research areas using the International Roadmap for TB Research [15] since no specific classification system is available for NTM. These areas included fundamental research, epidemiology, diagnostics, treatment, operational and public health research, and vaccines. Unclassifiable articles were categorized as ‘others.’
The abstracts were read and classified, and in cases of ambiguity, the full text was examined for classifica-tion by two researchers (Geunin Lee and Youngmok Park). Data were analyzed using the Cochran-Armitage trend test. A p<0.05 indicated statistical significance. All statistical analyses were performed using R version 4.2.3 computing software (R Core Team, Vienna, Austria). Ethical approval and consent to participate were not required because this study was a bibliographic analysis of published articles.
Results
1. Article selection
We searched Science Citation Index (Expanded) journals using defined terms and initially identified 28,092 articles, of which 868 were published with the participation of Korean authors. We excluded 167 articles due to duplication or association with conditions such as TB, bronchiectasis, hepatitis, and Enterococcus avium. Finally, we analyzed and categorized 701 articles (Figure 1).
2. Number of publications, study types, and design
The first study of NTM in Korea emerged in 1992, with the number of studies increasing slowly over the next decade until there was a substantial increase in the number of annual publications noted from 2004. In 2019, the number of articles published annually reached a peak of 66 (Figure 2). Except for those concerning vaccines, the p-values for these trends were all below 0.05. When categorized based on publication type [15], the number of articles in the ‘treatment’ category showed the largest increase in 2019, with a growth rate of 1,200%. Basic research constituted 41.3% (n=290) of the published articles, while clinical research represented 44.7% (n=313) (Table 1). Within basic research, biochemistry studies were the most common (n=73, 10.4%), whereas in clinical research, retrospective cohort studies were the most prominent (n=118, 16.8%). When categorized based on the research topic, ‘fundamental research’ constituted the majority of the studies (23.5%), followed by ‘epidemiology’ (17.4%) and ‘treatment’ (17.1%) (Table 2).
3. Research institutes and funding
A total of 54 institutions participated in the research. Table 2 presents the top 10 publishing institutes by research area. The combined number of articles from the top five institutions totaled 498, representing 71% of the overall articles.
There were 557 funding sources, with some articles having multiple funders (Table 3). Excluding duplicates, funding information was available for 371 articles (52.9%). A total of 221 articles (76.2%) reporting basic research and 136 articles (43.6%) reporting clinical research received funding. The National Research Foundation of Korea was the primary funder for NTM research, supporting 181 studies (32.5%). Fundamental research received the most support, accounting for 198 articles (35.5%).
4. Impact of published articles
Excluding meeting abstracts, there were 653 articles, with a median citation count of 10 (interquartile range [IQR], 3 to 13). Of the top 20 cited articles, 12 were regarding clinical research, half of which focused on treatment (Supplementary Table S1). The most-cited article, with 523 citations, pertains to the epidemiology of clinical research, explicitly addressing the geographic diversity of NTM [4]. As the number of published articles increased, the number of articles published in journals with a 5-year impact factor of ≥20 also increased (Figure 3 and Supplementary Table S2).
In basic research, the study design with the highest number of total citations was genetic engineering and gene sequencing (median, 21 [IQR, 17 to 40]). In clinical research, the study design with the highest total citations was randomized controlled trials (median, 109) (Table 1).
Discussion
We analyzed NTM-related publications authored by researchers based in Korea. Over time, there have been continuous improvements in both the quality and quantity of publications, with study topics closely reflecting the characteristics of NTM. However, there is a need for greater diversification in study design, research institutions, and funding sources.
The incidence and prevalence of pulmonary diseases caused by NTM have steadily increased worldwide in recent decades [16]. In South Korea, the annual prevalence surged from 11.4 to 56.7 cases per 100,000 population between 2010 and 2021, respectively [17]. As interest in NTM grows and scientific demand intensifies, research on NTM has correspondingly expanded in Korea. Notably, interest in treatment has also grown significantly. This study showed that in 2019, the highest proportion of publications focused on treatment, which has also shown the largest increase in the number of articles. Over the past two decades, the focus of research has evolved, transitioning from the establishment of basic treatment protocols and the evaluation of outcomes (2004 to 2013) to the development of personalized strategies and the topic of drug resistance (2014 to 2023). This reflects a growing emphasis on optimizing regimens and improving patients’ quality of life.
Notably, the characteristics of diseases caused by NTM are reflected in the focus of research regarding NTM. These diseases are not considered a notifiable condition in many countries, including South Korea [5]. Due to the absence of a central reporting system, numerous epidemiological studies have been published to deepen our understanding of the basic characteristics and clinical presentations of the affected population [7]. In our findings, 17.4% of articles were dedicated to epidemiology, a higher percentage than that of TB research (10.0%) in Korea [10]. Retrospective cohort studies comprised the plurality of clinical research (16.8%), and prospective cohort studies (1.0%) and randomized controlled trials (0.1%) were less common. Conducting prospective studies on NTM diseases presents several challenges. First, these diseases are caused by a variety of mycobacterial species, each with distinct clinical manifestations and treatment responses, necessitating species-specific considerations in diagnosis and management [18,19]. Second, because of the slow progression and prolonged treatment durations associated with NTM diseases, extended follow-ups of the study participants are required to detect significant clinical changes [20,21]. Third, continuous environmental exposure complicates the evaluation of treatment responses [22]. Despite these challenges, future research should prioritize prospective and longitudinal studies over retrospective or single-snapshot studies to improve our understanding of the nature of the diseases and optimize treatment regimens.
The funding landscape revealed that the National Research Foundation of Korea and the Ministry of Health and Welfare play a crucial role in supporting NTM research, together sponsoring over half of the funded studies (51.5%). This underscores the critical importance of national funding bodies in driving scientific inquiry and innovation in the medical field. However, there is a need to diversify funding sources and research institutions, as a small group of entities contributes to a considerable portion of the funding and publications. When funding sources are limited, there is a greater likelihood that only certain types of research will receive support, leading to potential bias in research. Basic research receives 32.6% more funding than clinical research. Thus, it is important to allocate additional funding to clinical research to ensure balanced development between foundational knowledge and practical application.
Several limitations should be considered when interpreting the results of our study. First, our research was conducted using only one electronic medical database; this may limit the comprehensiveness of our findings. However, it covers interdisciplinary scientific fields. Therefore, previous bibliometric analyses have often used the same database [10-12]. Second, the ranking of the research institute was based solely on the number of publications, without accounting for their quality [23]. Third, we only measured the frequency of funding but could not assess the amount. Fourth, neither impact factors nor citation counts can fully capture the scientific impact of research [24]. Moreover, recent publications may have fewer citations simply due to their newer release dates.
In conclusion, this bibliometric analysis showed that both the quality and quantity of research regarding NTM in South Korea have advanced, with research topics closely reflecting the characteristics of NTM. However, research regarding NTM remains concentrated in a limited number of institutions and funding bodies. The scope and impact of future studies should be broadened through greater diversification across institutions and funding sources. Prioritizing prospective study designs over retrospective approaches is crucial for deepening our understanding of diseases caused by NTM and improving treatment strategies. These steps will be vital for advancing research regarding these pathogens and achieving more comprehensive and robust findings.
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