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Original Article

A Bibliometric Analysis on Tuberculosis and Diabetes Mellitus


2: Visualization, Patterns, and Trends
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Carlos Quispe‑Vicuña1, Miguel Cabanillas‑Lazo1, Diego Galarza‑Valencia2, Cesar Mauricio‑Vilchez3, Franco Mauricio2, Fran Espinoza‑Carhuancho4,
Frank Mayta‑Tovalino4
1
Academic Department, Faculty of Medicine, Universidad Nacional Mayor de San Marcos, 2Academic Department, Unidad de Investigación, Innovación y
Emprendimiento, Universidad Nacional Federico Villarreal, 3Academic Department, Faculty of Medical Technology, Universidad Nacional Federico Villarreal, 4Academic
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Department, Grupo de Bibliometría, Evaluación de evidencia y Revisiones Sistemáticas, Human Medicine Career, Universidad Cientifica del Sur, Lima, Peru

Abstract
Background: The convergence of type 2 diabetes mellitus (DM2) and tuberculosis (TB) may lead to increased mortality and complications,
so the underlying mechanism is under investigation. Therefore, a bibliometric analysis was performed to describe the bibliometric indicators
of publications evaluating the relationship between TB and DM2. Methods: A descriptive and observational bibliometric study was conducted
using the Scopus database to identify documents published from 2016–2023, for which free and controlled terms (Medical subject headings
and Emtree) were used. The variables collected comprised the number of published documents, institutions, countries, authors, journals, and
type of collaboration, which were exported to Excel 2016 and analyzed with SciVal. Results: A total of 456 documents, 1624 authors, and
2173 citations were identified, with Medicine and Immunology‑Microbiology being the subcategories with the highest and lowest number of
documents (367 and 80 documents), respectively, with a strong decreasing trend correlation (R2: 0.95; P < 0.5) between the number and year
of publication. While the country with the highest production was China (71 papers), the country with the highest citation was the United
States (952 citations). In terms of authors, the highest production was by the American Venketaraman, and the highest impact was by the
Asian Kimberly To. The institution with the highest number of papers was the Western University of Health Sciences, while Stellenbosch
had the highest impact. Conclusion: Although the scientific productivity of DM2 and TB have reported growth rates of 158.75% and 7.3%,
respectively, our results found a decreasing trend in publications associating these two diseases. The thematic evolution of the concepts in
both diseases suggests that the relationship between them is not yet known, so future studies evaluating the underlying mechanisms of this
comorbidity are suggested.

Keywords: Bibliometrics, diabetes mellitus, tuberculosis

Submitted: 06-Dec-2023 Revised: 11-Jan-2024 Accepted: 19‑Feb‑2024 Published: 15-Mar-2024

Introduction global health concern, being a leading cause of illness and death
worldwide. The disease impacts nearly 11 million individuals
Diabetes mellitus (DM) is one of the major diseases with the
and is responsible for just over a million fatalities globally.[5]
greatest impact on global public health,[1] affecting almost
530 million people worldwide, causing almost two million The convergence of these two diseases raises crucial questions
deaths and being mainly caused by type 2 DM2 (96.0% of about how the presence of DM2 may increase the risk of
cases).[2] Type 2 diabetes has experienced an alarming increase
in recent years worldwide,[3] and this has led to an increase in Address for correspondence: Dr. Frank Mayta‑Tovalino,
the risk of its complications and many infections, which are Av. Paseo de la República 5544, Miraflores 15074, Peru.
E‑mail: fmaytat@cientifica.edu.pe
caused by the immunosuppressive state that DM2 tends to
generate in the population.[4] This has led to the development ORCID:
of tuberculosis (TB) along with the growing trend of DM2. TB, Frank Mayta‑Tovalino: http://orcid.org/0000-0002-3280-0024
often abbreviated as TB, is a persistent bacterial disease triggered
by the bacterium known as Mycobacterium TB. It is a significant This is an open access journal, and articles are distributed under the terms of the Creative
Commons Attribution‑NonCommercial‑ShareAlike 4.0 License, which allows others to
Access this article online remix, tweak, and build upon the work non‑commercially, as long as appropriate credit
Quick Response Code: is given and the new creations are licensed under the identical terms.
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How to cite this article: Quispe‑Vicuña C, Cabanillas‑Lazo M,


DOI: Galarza‑Valencia D, Mauricio‑Vilchez C, Mauricio F, Espinoza‑Carhuancho F,
10.4103/ijmy.ijmy_18_24 et al. A bibliometric analysis on tuberculosis and diabetes mellitus 2: Visualization,
patterns, and trends. Int J Mycobacteriol 2024;13:83-90.

© 2024 International Journal of Mycobacteriology | Published by Wolters Kluwer - Medknow 83


Quispe‑Vicuña, et al.: Tuberculosis and diabetes mellitus 2

developing TB and, in turn, how TB infection may affect Exclusion criteria


metabolic control and diabetes progression. A previous 1. Papers that are not related to TB and DM2
systematic review found that DM2 increases the risk of 2. Opinion articles, editorials, letters to the editor, and
developing latent and active TB by just over two‑fold.[6] In papers that are not original research
addition to that, patients with TB and DM2 have reported 3. Documents that are not written in English
increased odds of death and almost twice the risk of developing 4. Papers that do not have full text available.
drug‑resistant states.[7] This highlights the importance of having
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a clear picture of the interaction of these two diseases and their Search strategy
status in the medical literature. To achieve this, bibliometric An advanced search strategy developed independently by two
studies would be a very good option since they comprise a authors (MCL and CQV) was used. Discrepancies were resolved
quantitative analysis of certain topics, by means of which by consensus by a third author (FMT) to obtain a single strategy.
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the predominant trends in research can be evaluated;[8] they The search strategy was formulated using different MeSH (Medical
also allow us to analyze the authors, journals, and institutions Subject Headings) and Emtree (Embase) terms as the basis. In
with the greatest academic productivity, providing us with a addition to the Boolean operators “OR” and “AND,” the following
complete vision of a specific topic.[9] search strategy was obtained: (TITLE‑ABS (tuberculos * OR
“Kochs Diseas*” OR “Koch × s Diseas*” OR “Koch Diseas*” OR
This data would provide reliable statistics to guide future “TB diseas*” OR “TB infect*” OR “active TB” OR “tuberculous
research and, at the same time, be a tool for the medical infect*” OR “tuberculous lesion”) OR AUTHKEY (tuberculos
community to have a current overview of the topic of interest. * OR “Kochs Diseas*” OR “Koch’s Diseas*” OR “Koch
Regarding DM2 and TB, so far, no bibliometric analysis has Diseas*” OR “TB diseas*” OR “TB infect*” OR “active
been developed that associates both diseases; however, there TB” OR “tuberculous infect*” OR “tuberculous lesion”))
are multiple bibliometric studies that analyze the productivity AND (TITLE‑ABS (diabet * AND (“Noninsulin Dependent” OR
of the diseases as such[10] or associating them with other topics “Ketosis Resistant” OR “Non Insulin Dependent” OR stable OR
such as monitoring, diagnosis, treatment, etc.[11] “ii” OR “Type 2” OR niddm OR “Maturity Onset” OR “Slow
Therefore, a bibliometric analysis was performed with the aim Onset” OR “dm 2” OR “adult Onset” OR “insulin independent”
of describing bibliometric indicators of publications related to OR t2dm)) OR AUTHKEY (diabet * AND (“Noninsulin
the relationship between TB and DM2. Dependent” OR “Ketosis Resistant” OR “Non Insulin Dependent”
OR stable OR ii OR “Type 2” OR niddm OR “Maturity Onset”
OR “Slow Onset” OR “dm 2” OR “adult Onset” OR “insulin
Methods independent” OR t2dm))) AND (LIMIT‑TO (PUBYEAR, 2023)
Ethical statement OR LIMIT‑TO (PUBYEAR, 2022) OR LIMIT‑TO (PUBYEAR,
Because this study used publicly available secondary data from 2 0 2 1 ) O R L I M I T‑ T O ( P U B Y E A R , 2 0 2 0 ) O R
the Scopus database and did not involve humans or animals, LIMIT‑TO (PUBYEAR, 2019) OR LIMIT‑TO (PUBYEAR, 2018)
no ethics committee approval was required. OR LIMIT‑TO (PUBYEAR, 2017) OR LIMIT‑TO (PUBYEAR,
2016)).
This bibliometric study does not need ethical approval as it uses
public anonymous data from Scopus. It poses no ethical issues Selection of information
related to privacy or informed consent. The data are already The sample used in this study included papers published from
published, eliminating confidentiality concerns. 2016 to 2023, without language limitation. We excluded
letters, conference papers, editorials, notes, short surveys,
Study design and database
conference reviews, errata, and articles whose metadata did
An observational and descriptive bibliometric study was
not allow analysis.
formulated, leveraging the Scopus database. This bibliometric
study does not require a sample calculation because it is Data analysis
based on the exhaustive analysis of all articles published in a The gathered data were transferred to Microsoft Excel 2016
database, such as Scopus. This database is renowned for its for further analysis. Bibliometric indicators were derived using
unrestricted access to a broad spectrum of publications, and it the SciVal tool, a Software owned by Elsevier (Netherlands),
supports both rudimentary and sophisticated search strategies which is capable of processing vast amounts of data and
for gathering articles.[12] producing robust bibliometric analyses. The data procured
from SciVal were used to examine several variables: the
Inclusion criteria
number of published documents, institutions, countries,
1. Papers published in the Scopus database from 2016–2023
authors, journals, and the nature of collaboration. The findings
2. Papers using free and controlled terms (Medical subject
were organized and displayed in descriptive Tables. To identify
headings [MeSH] and Emtree) related to TB and type 2
publication trends, a Pearson correlation was conducted.
DM2
3. Papers evaluating the relationship between TB and DM2 Various indicators were utilized to analyze the different variables;[13]
4. Papers providing bibliometric indicators of publications. citations per paper, CiteScore, SCImago Journal and Rank,

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Quispe‑Vicuña, et al.: Tuberculosis and diabetes mellitus 2

Source‑Normalized Impact per Paper, and the type of collaboration Among the 10 authors with the highest number of TB and DM2
of the publications were also analyzed. To illustrate the flow of publications, the American author Vishwanath Venketaraman
normalized relationships by journal‑country‑author, a three‑field had the highest number of publications (13) and citations (218),
graph (Sankey diagram) was used where the largest rectangular while Kimberly To had the highest impact with 26.4 citations
nodes in each category allow visual evaluation of the relationships per paper in her five publications. Most of the authors were
between the elements evaluated. Bibliometrix 3.0 R version 4.2.3 North American (5 of 10 authors) [Table 1].
(Bibliometrix 3.0 R version 4.2.3 [R studio, Italy]) was used to
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analyze scientific production by country and to describe graphically The 10 institutions with the highest number of papers
the thematic evolution of publications over the years. are shown in Table 2. Western University of Health
Sciences (USA) was the institution with the highest
scientific output (13) and citations (218), while Stellenbosch
Results
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University (South Africa) had the highest impact (19.9


During the period 2016–2023, following the process of citations per paper).
inclusion and exclusion of publications, a total of 456 papers,
1624 authors, and 2173 citations were identified [Figure 1] Regarding the journals, Indian Journal of TB and Frontiers
being the subcategories with the highest number of papers in in Immunology from India and Switzerland, respectively, are
Medicine (367 papers), Biochemistry, Genetics and Molecular the journals with the highest number of publications (11)
Biology (80 papers), and Immunology and Microbiology and the journal with the highest number of citations was the
(80 papers) as shown in Figure 1. A strong decreasing trend Journal of Clinical Medicine (186). However, the journal
correlation with a significant P value (R2: 0.95; P < 0.05) was with the highest % of citations and the highest impact is BMC
observed between the number and year of publication [Figure 2]. Infectious Diseases (79% and 22.1 citations per paper with 10
publications) [Table 3].
The countries with the highest production are China
(71 papers), the United States (68 papers) and India According to the metric CiteScore, Table 4 shows the number
(57 papers). However, the order of the countries with the of documents according to the quartile of the journal and
highest number of citations is different with the United States the type of collaboration. During the study period, a great
(952 citations), the United Kingdom (621 citations), and India predominance of high‑quality journals (Q1 and especially
(494 citations) [Figure 3]. Q2) is observed with respect to the rest. Regarding the type

Figure 1: Study selection flowchart

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Table 1: Top 10 authors publishing


Author Total documents Total citation Citations per document H‑index FWCI Country
Venketaraman, Vishwanath 13 218 16.8 1.14 29 United States
Cao, Ruoqiong 8 115 14.4 1 9 United States
Sathananthan, Airani 7 91 13 0.87 13 United States
Ronacher, Katharina 6 100 16.7 0.71 31 Australia
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Zenteno‑Cuevas, Roberto 6 15 2.5 0.28 18 Mexico


Subbian, Selvakumar 5 64 12.8 0.98 31 United States
Govan, Brenda L 5 35 7 0.56 22 Australia
Kupz, Andreas 5 35 7 0.56 18 Australia
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Novita, Bernadette Dian 5 32 6.4 0.54 3 Indonesia


To, Kimberly 5 132 26.4 1.57 6 United States
FWCI: Field‑weighted citation impact

80
74
75 71
Number of Publications

69
70
65
58 R2 = -0.008
60 57
55
50
45 43 42 42
40
35
30
2015

2016

2017

2018

2019

2020

2021

2022

2023

2024

Year

Figure 2: Trend of publications


Figure 3: Top ten productive countries
of collaboration, it is mostly only national (40%) followed
by international (29.8%), which would evidence a greater as authors such as Vishwanath Venketaraman and Ruoqiong
impact and interest of the subject of this study in the world Cao [Figure 5 and 6].
literature.
The thematic evolution in TB and diabetes research has shown Discussion
a remarkable transition over time. Comorbidity, a consistent
A significant trend was found in the decrease of scientific
theme from 2016 to 2020, has shifted its focus to DM in
production per year on TB and DM2 (R2: 0.61). China, the
2021–2022. Inflammation, a pivotal theme in 2016–2018,
has shifted to TB in 2019–2020. The study of Mycobacterium United States, and India are the leading countries in this area,
TB has maintained its relevance but has expanded its focus with almost 43% of the publications. Most of the scientific
to cytokines, TB, and glutathione in 2019–2020. Pulmonary production consisted of original articles published in high
TB, a major topic in 2016–2018, has shifted its focus to quality journals. These works were carried out by North
type 2 diabetes in 2019–2020. TB research has maintained American authors and only had national collaboration.
its relevance but has expanded its focus to diabetes, DM, In the last decade, the scientific productivity of DM2 together
HIV, and metformin in 2019–2020. DM2, a relevant topic with other metabolic diseases, has reported a growth rate of
in 2016–2018, has evolved into TB in 2019–2020. Finally, 158.75%,[14] and the productivity of TB research has reported
diagnostics, a relevant topic in 2019–2020, has evolved to an annual growth rate of 7.3% (10). However, our results
latent TB in 2021–2022. These findings reflect the dynamics found a decreasing trend in publications associating these
and evolution of research in this field, highlighting the two diseases, which would indicate few studies evaluating
importance of comorbidity, inflammation, TB, and DM2 in this relationship. This would be in keeping with the context
the literature on TB and diabetes [Figure 4]. that, although many studies suggest that immunometabolic
In the Sankey diagram, strong relationships were evident changes during diabetes cause increased susceptibility to TB,
between journals such as TB and Journal of Clinical Medicine the mechanisms underlying these changes and effects are not
with countries such as the United States and China, as well well understood.[15]

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Table 2: Top ten productive institutions


Institution Country Documents Total Citations per FWCI
citation document
Western University of Health Sciences United States 13 218 16.8 1.14
London School of Hygiene and Tropical Medicine United Kingdom 11 78 7.1 0.5
Instituto Nacional de Ciencias Medicas y Nutricion Salvador Zubiran Mexico 11 202 18.4 1.03
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Stellenbosch University South Africa 10 199 19.9 1.69


University of the Witwatersrand South Africa 10 117 11.7 1.03
South African Medical Research Council South Africa 10 143 14.3 0.96
University of Queensland Australia 9 118 13.1 0.93
Universitas Airlangga Indonesia 9 34 3.8 0.44
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Instituto Nacional de Enfermedades Respiratorias Mexico 8 43 5.4 0.42


Consejo Nacional de Ciencia y Tecnologia Mexico Mexico 8 95 11.9 0.96
FWCI: Field‑weighted citation impact

Table 3: Bibliometric indicators of production and impact on journals


Journals Country Quartile Scimago Documents Citations Citations per SNIP CiteScore
journal rank (% cited) document 2022
Indian Journal of Tuberculosis India Q3 0.452 11 53 (56) 4.8 0.7 2.6
Frontiers in Immunology Switzerland Q1 2.022 11 138 (74) 12.5 1.49 9.4
Tuberculosis United States Q2 0.71 10 89 (76) 8.9 0.894 4.9
BMC Infectious Diseases United Kingdom Q2 1.055 10 132 (79) 13.2 1.283 6.2
Chinese Journal of Antituberculosis China NR 0 10 5 (NR) 0.5 0 0
PLoS ONE United States Q1 0.885 7 46 (75) 6.6 1.253 6
Frontiers in Cellular and Infection Switzerland Q1 1.308 6 55 (71) 9.2 1.198 6.4
Microbiology
Frontiers in Public Health Switzerland Q1 1.125 6 16 (52) 2.7 1.374 3.8
Journal of Clinical Medicine Switzerland Q1 0.935 6 186 (70) 31 1.179 5.4
International Journal of France Q1 0.966 5 35 (68) 7 0.816 4.1
Tuberculosis and Lung Disease
SNIP: Source‑normalized impact per paper, NR: Not reported

Table 4: Documents published according CiteScore Quartil 2022 and type of collaboration
CiteScore Quartile 2018 2019 2020 2021 2022 2023 Total
Q1 17 11 23 21 21 14 107
Q2 9 24 17 27 25 22 124
Q3 6 8 12 9 14 8 57
Q4 7 9 10 8 7 7 48
Total 39 52 62 65 67 51 336
Type of collaboration Documents (%) Citations Citations per publication FWCI
International collaboration 111 (29.8) 1602 14.4 1.08
National collaboration 149 (40.0) 1144 7.7 0.73
Institutional collaboration 95 (25.5) 425 4.5 0.51
Single authorship 15 (4.0) 155 10.3 1.81
FWCI: Field‑weighted citation impact

More than two‑thirds of the global prevalence of both TB is review that evaluates the susceptibility to pathogens such
usually concentrated in Asian and Middle Eastern countries,[16] as TB caused by an altered immune system that is usually
and similarly, the East Asian region usually concentrates a large found in patients with DM2 due to factors such as advanced
amount of the world’s diabetes burden (3); this may account glycation and constant inflammation caused by a very high
for the fact that countries such as India or China are among glucose concentration.[17] This publication was one of the most
the countries with the highest productivity. cited, with 85 citations, which evidence its importance in the
The author Kimberly To had the highest impact with 26.4 medical literature to understand the association between TB
citations per paper with only 5 publications, highlighting a and DM2.

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Figure 4: Thematic evolution

Figure 5: Three‑field plot

Figure 6: Country collaboration map

Stellenbosch University leads in research impact with 19.9 on the topic of TB worldwide,[19] which would show its great
citations per article. A review highlights the need to study TB impact on TB issues.
and diabetes. Gaps in knowledge about altered immunity in The journal BMC Infectious Diseases was not only the journal
patients with DM2 during TB were identified.[18] In turn, this with the highest impact but also the one with the highest %
institution has previously been reported to have been one of of citations. This journal is a high quartile (Q2), open‑access,
the most collaborative and affiliated institutions with others peer‑reviewed journal that collects articles evaluating all aspects

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of infectious and sexually transmitted diseases in humans and Financial support and sponsorship
animals. In addition, this journal has previously reported high Nil.
productivity in previous bibliometric studies TB.[20,21]
Conflicts of interest
Regarding the thematic evolution, apart from TB and DM2 There are no conflicts of interest.
itself, comorbidity and inflammation are the topics that have
gained most relevance in recent years. This would reinforce
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