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Received: 12 December 2023
-
Accepted: 4 March 2024
DOI: 10.1002/med4.58
ORIGINAL ARTICLE
Visualization analysis of research progress and trends in
coexistence of lung cancer and pulmonary tuberculosis
using bibliometrics
Ling Yang
1,2,3
|Zhaoyang Ye
1
|Linsheng Li
1
|Li Zhuang
1
|Jingzhi Guan
3
|
Wenping Gong
2
1
Hebei North University, Zhangjiakou,
China
2
Beijing Key Laboratory of New
Techniques of Tuberculosis Diagnosis and
Treatment, Senior Department of
Tuberculosis, The Eighth Medical Center
of PLA General Hospital, Beijing, China
3
Senior Department of Oncology, The
Fifth Medical Center of PLA General
Hospital, Beijing, China
Correspondence
Wenping Gong, The Eighth Medical
Center of PLA General Hospital, 17
#
Heishanhu Road, Haidian District,
Beijing 100091, China.
Email: gwp891015@whu.edu.cn
Jingzhi Guan, The Fifth Medical Center of
PLA General Hospital, 8
#
Dongdajie
Road, Fengtai District, Beijing 100071,
China.
Email: jzjz1970@hotmail.com
Funding information
National Natural Science Foundation of
China, Grant/Award Number: 82172902
Abstract
Background: The incidence of lung cancer combined with pulmonary
tuberculosis has been increasing, but there is relatively limited published
literature on the topic of lung cancer combined with tuberculosis (LC‐PTB)
from a bibliometric perspective. Therefore, in this study, we aimed to quan-
titatively analyze the LC‐PTB‐related literature to better understand the cur-
rent status of this eld and identify future research trends.
Methods: We searched for articles related to LC‐PTB using the Web of Sci-
ence Core Collection (SCI‐E) and conducted a visual analysis of publication
quantity, countries, institutions, authors, journals, references, and keywords
using bibliometric software (CiteSpace, VOSviewer, and Scimago Graphica).
Results: As of January 8, 2024, a total of 460 publications related to LC‐PTB
were included for analysis from 3705 retrieved records. The number of pub-
lications has been increasing almost yearly, with most from China (n=123),
followed by the United States (n=77). Taipei Medical University contributed
the most publications (n=11). Jing‐Yang Huang and Yung‐Po Liaw (eight
documents each) ranked rst among the included authors. The Journal of
Thoracic Oncology was the most productive academic journal on LC‐PTB. The
aggregation of key nodes in the co‐citation network and the chronological
sequence indicated that LC‐PTB research has shifted from initial hotspots
such as lung diseases, bronchitis, and exposure to recent areas, including
immunotherapy, immune checkpoint inhibitors, and nivolumab.
Conclusion: In this study, we visualized the current status of LC‐PTB research
as well as future trends using bibliometric methods, providing new insights into
the differential diagnosis of LC‐PTB and its related promoting mechanisms.
Abbreviations: IF, impact factor; JTO, Journal of Thoracic Oncology; LC, lung cancer; LC‐PTB, lung cancer combined with pulmonary
tuberculosis; LTBI, latent tuberculous infection; MTB, Mycobacterium tuberculosis; PTB, Pulmonary tuberculosis; TB, tuberculosis; TLS, total link
strength; WHO, World Health Organization; WoSCC, Web of Science Core Collection.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided
the original work is properly cited.
© 2024 The Authors. Medicine Advances published by John Wiley & Sons Ltd on behalf of Tsinghua University Press.
144
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Med. Adv. 2024;2:144–164. wileyonlinelibrary.com/journal/med4
KEYWORDS
bibliometrics, immunity, lung cancer combined with tuberculosis, lung cancer, pulmonary
tuberculosis
1
|
INTRODUCTION
Lung cancer (LC) is the most common primary malig-
nant tumor of the lung, with most cases originating from
the epithelium of the bronchial mucosa; hence, LC is also
known as bronchogenic carcinoma [1]. According to
statistical data analysis from the American Cancer Soci-
ety in 2024, it is estimated that there will be 2,001,140
new cancer cases and 611,720 cancer deaths in the United
States [2]. This marks the rst time that the annual
number of cancer cases in the United States has exceeded
two million and is equivalent to one person being diag-
nosed with cancer every 15 s [2]. Similarly, according to
statistical data released by the China National Cancer
Center in 2022, there were 2.414 million cancer deaths in
China in 2016, with LC being the leading cause, ac-
counting for 65.7% of the total [3]. Pulmonary tubercu-
losis (PTB) is a global infectious disease caused by
Mycobacterium tuberculosis (MTB) infection [4]. The
Global Tuberculosis Report released by the World Health
Organization (WHO) in 2023 states that approximately
7.5 million new patients were diagnosed with TB globally
in 2022, marking the highest number since the WHO
began in 1995 [5]. Among countries worldwide, China
had the third highest number of new cases, accounting
for 7.1% of the global total, followed by Indonesia (10%)
and India (27%) [5]. It is concerning that in recent years,
there has been a signicant increase in the incidence of
reactivated TB infection or latent tuberculous infection
(LTBI) among patients with LC [6], and the number of
patients with lung cancer combined with tuberculosis
(LC‐PTB) has also increased signicantly [7]. Addition-
ally, studies have found that different patients with can-
cer have varying degrees of increased risk of MTB
infection; hematology or solid tumor patients have a
twofold higher risk compared with that in the general
population, and patients with LC have a six‐fold higher
risk compared with non‐lung cancer patients [8, 9].
Bibliometrics is a scientic discipline that uses statis-
tical software and mathematical and statistical methods to
quantitatively analyze literature [10, 11]. This method in-
tegrates mathematics, statistics, and librarianship,
emphasizing a comprehensive knowledge system centered
on quantitative measurement, focusing on describing or
explaining the characteristics of literature and research
trends in various disciplines through data analysis [11].
The primary analytical objects in bibliometrics are
published information, such as books, journal articles, and
datasets, along with their associated metadata, including
citations, titles, and keywords [12]. In its early develop-
ment, bibliometrics primarily focused on analyzing the
external features of literature, such as citation counts,
authorship patterns, and the distribution of key terms. The
rapid advancements in informatics and articial intelli-
gence technologies have enabled bibliometrics to expand
its scope to analyze units of scholarly knowledge gradually,
explore emerging research topics, and identify future
research directions [13–15]. Moreover, applying biblio-
metrics in medicine enables macro and micro‐level anal-
ysis of many publications and their production patterns,
placing medicine at the forefront of bibliometric knowl-
edge development [16].
Despite such advancements, few in‐depth studies exist
that have thoroughly analyzed and visualized the research
progress and future development trends in LC‐TB using
bibliometrics. Therefore, in this study, we adopted a bib-
liometric approach to analyzing the publication quantity,
countries or regions of publication, publishing institutions,
authors, journals, cited references, research keywords, and
research hotspots related to LC combined with PTB (LC‐
PTB) using the Web of Science Core Collection (WoSCC)
database. We performed cooperative network analysis, co‐
occurrence analysis, citation analysis, literature coupling
analysis, co‐citation analysis, burst analysis, and evolu-
tionary path analysis as well as research frontier analysis.
We further explored the research directions and develop-
ment trends in this eld, aiming to provide practical in-
formation and new strategies for studying LC‐PTB. To our
knowledge, this is the rst comprehensive bibliometric
analysis conducted for LC‐PTB.
2
|
MATERIALS AND METHODS
2.1
|
Denition of terms
The h‐index measures a researcher's combined impact
and productivity by correlating the number of papers
published (Np) with the number of citations received
(Nc). The h‐index is useful for assessing the inuence and
productivity of researchers or national scientic research
[17, 18]. The total link strength (TLS) is used to quantify
network connection strength, and is helpful in analyzing
social and complex networks by measuring link density
MEDICINE ADVANCES
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145
and robustness [19, 20]. Connections can exist between
nodes, such as citations, cooperation, or animosity [21].
The Impact Factor (IF) assesses an academic journal
based on the average citation count of articles published
over a certain time frame [22–24]. Specically, the IF
refers to the average number of times articles published
in a particular journal in the previous 1–2 years are cited
in the current year as follows: (the year being cited)
(IF =number of citations divided by the number of ar-
ticles published).
2.2
|
Data source and retrieval strategy
We compiled our literature dataset from the WoSCC, a
reputable and comprehensive database, selecting SCI‐E for
our analysis [25]. The WoSCC offers extensive data on
publications and authorship compatible with bibliometric
tools like CiteSpace and VOSviewer. The authoritative
WoSCC database is widely recognized and used in biblio-
metric research [26, 27]. The database provides a
comprehensive and curated collection of scholarly publi-
cations, making it a valuable resource for bibliometric
analysis and research evaluation. We used publicly avail-
able databases, ensuring no ethical concerns. Owing to
daily updates, we conducted our data search on a single day
to maintain currency. A comparison of search strategies
resulted in an optimal search string (Supplementary
material 1).
2.3
|
Inclusion and exclusion criteria
The inclusion criteria were as follows: (1) academic articles
related to the coexistence of LC‐PTB, including basic
research, clinical studies, and reviews; and (2) relevant
literature published from 1995 to 2022 in the SCI‐E
database.
Exclusion criteria were as follows: (1) non‐academic
articles such as news reports and commentaries; (2)
duplicate publications, that is, articles reporting ndings
of the same study published in different journals or
conferences; and (3) articles on topics unrelated to the
coexistence of LC‐PTB, such as research on other types of
cancer or infectious diseases.
2.4
|
Data visualization and analysis
The identied search results were analyzed using Micro-
soft Excel 2021 (Microsoft Corporation, Redmond, WA,
USA) and bibliometric tools such as VOSviewer, Cite-
Space, and Scimago Graphica for effective data
visualization [28, 29]. These tools are excellent for graphic
representation, simplifying the comprehension of biblio-
graphic data [30]. VOSviewer by Van Eck and Waltman at
Centre for Science and Technology Studies, Leiden Uni-
versity, allows visualization of various networks and cita-
tions (http://vosviewer.com) [29]. CiteSpace, by Professor
Chaomei Chen at Drexel University, offers extensive
citation and collaboration analyses (https://sourceforge.
net/projects/citespace/) [31]. Scimago Graphica enables
the visualization of collaborative networks across coun-
tries and regions (https://www.graphica.app/) [32].
3
|
RESULTS
3.1
|
Search results and publication
quantity
Owing to the maximum limit of 100,000 publications for
analysis in VOSviewer and CiteSpace software as well as
citation reports in the SCI‐E database, we included
literature published between 1995 and 2022. A total of
3705 records related to LC‐PTB were retrieved from the
SCI‐E database. After excluding irrelevant records, a nal
set of 460 publications were included (Figure 1). Further
analysis of the 460 included entries revealed that these
publications involved 2792 authors distributed among
1547 institutions from 177 countries or regions. Addi-
tionally, from the distribution of publication years, we
found that the number of LC‐PTB‐related publications
showed an overall increasing trend, with minor uctua-
tions between 1995 and 2022 (Figure 2). Notably, the
number of LC‐PTB‐related publications ranged from 40
to 60 annually between 1995 and 2022, with gradual
growth. A marked rise in publications occurred from
2011, peaking at 52 in 2020 before leveling off, likely
owing to advances in information technology and the
global shift toward open access.
3.2
|
Analysis of countries or regions
We imported the information obtained from the 460
entries into VOSviewer for analysis. Furthermore, we
imported the analyzed data into Scimago Graphica to
generate a map of countries or regions based on the
publication data (Figure 3a). The map showed that
China, the United States, South Korea, and Japan had
the highest number of publications in the eld of LC‐
PTB. On the basis of the closeness of cooperation
among countries, all countries or regions can be divided
into six categories. Furthermore, we examined countries
or regions with more than ve publications (Figure 3b)
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MEDICINE ADVANCES
and found that China had the highest number of papers
published on LC‐PTB (n=123), followed closely by the
United States, with 77 publications. South Korea
(n=51), Japan (n=35), India (n=16), Turkey
(n=16), Spain (n=14), the United Kingdom (n=13),
and Singapore (n=12) were ranked next. Building on
this, we analyzed the collaboration relationships among
countries or regions with more than ve publications.
We found that China, the United States, the United
Kingdom, and Japan not only had high publication
numbers but also collaborated closely with each other
(Figure 3c). Interestingly, we also discovered that China
not only ranked rst in terms of number of publications
but also had close collaboration with other countries
(Figure 3c), which may be related to China having a
high burden of LC and PTB.
FIGURE 1 Retrieval strategy and owchart. The search was conducted in the Web of Science Core Collection (SCI‐E) database using
the search strategy as described above, resulting in a total of 3705 records. After further screening based on predened criteria, 460 unique
publications were included for analysis.
FIGURE 2 Distribution of publications by years. From 1995 to 2022, the number of publications related to lung cancer with
pulmonary tuberculosis (LC‐PTB) showed a general increasing trend, peaking in 2002. The vertical axis represents the number of
publications per year, and the horizontal axis represents the year.
MEDICINE ADVANCES
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147
FIGURE 3 Distribution of research on lung cancer with pulmonary tuberculosis (LC‐PTB) by country or region. (a) Visualization map
of publications by country or region. The diameter of each node represents the number of publications, with China, the United States, and
South Korea being the three leading contributors. The strength of collaboration between countries is denoted by different colors, with six
clusters identied. (b) Distribution map of countries or regions with more than ve publications. (c) Visualization analysis regarding the
strength of collaboration between countries or regions. The size of each node represents the number of publications, and the thickness of
the connecting lines represents the strength of collaboration. The minimum collaboration strength among countries or regions with more
than ve publications is 1 (light yellow), and the maximum is 39 (red).
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3.3
|
Analysis of institutions and
collaborative institutions
For the 460 publications on LC‐PTB, 1547 institutions
contributed; we constructed a bar chart and citation fre-
quency chart for institutions with over ve publications
(Figure 4a). Leading institutions by publication count
included Taipei Medical University and Seoul National
University (n=11 each); the National Cancer Institute of
the United States had the highest number of citations
(n=507). These data indicate that institutions such as
Taipei Medical University, Seoul National University, and
the National Cancer Institute have conducted extensive
research on LC‐PTB, with publications from the National
Cancer Institute having a greater impact than those from
other institutions.
We conducted co‐occurrence analysis of institutions
using VOSviewer software, setting the parameter to
include institutions that published at least ve articles on
LC‐PTB. A total of 26 institutions met the inclusion
criteria, with the largest collaboration network
comprising nine institutions (Figure 4b). These nine in-
stitutions can be broadly divided into three groups: a
group primarily represented by Chung Shan Medical
University, Chung Shan Hospital, Fu Jen Catholic Uni-
versity, and Changhua Christian Hospital (red group); a
group mainly represented by Taipei Medical University,
National Taiwan University Hospital, and National
Taiwan University (green group); and a group repre-
sented primarily by Taipei Veterans General Hospital and
National Yang‐Ming University (blue group). We further
analyzed the strength of collaboration among in-
stitutions. We found that research institutions in Taiwan
had the closest collaborations with other institutions,
with Chung Shan Medical University (TLS =32), Chung
Shan Hospital (TLS =30), and Taipei Medical University
(TLS =25) being the leading three in terms of collabo-
ration strength (Table 1).
3.4
|
Analysis of authors
In addition to analyzing countries, regions, and in-
stitutions, we further investigated relevant authors in the
eld. The co‐authorship network revealed the involvement
of more than 2792 authors in LC‐PTB‐related research. In
the co‐authorship network, nodes represent authors, and
the appearance of node labels represents the publication
threshold for authors [33]. We set the publication
threshold for authors at N≥2, with 53 authors meeting this
threshold (Figure 5a). Accordingly, we visually observed
that the authors with the highest number of publications in
the eld of LC‐PTB were Jing‐Yang Huang and Yung‐Po
Liaw, with eight documents each. We further compiled a
list of the 10 leading authors according to publication
count, as shown in Table 2. Although curves represented
the collaboration relationships among authors (Figure 5a),
these were unclear. Therefore, we imported the data into
VOSViewer to further explore the strength of collaboration
relationships among the authors (Figure 5b).
Our data indicated that the visualization map of author
collaboration network's most extensive links can be
divided into ve clusters. The “red cluster” is primarily
represented by Wei‐Juin Su, Jia‐Yih Feng, and Shiang‐Fen
Huang; the “yellow cluster” is mainly represented by Yuh‐
Min Chen, Chieh‐Hung Wu, and Yu‐chin Lee; the “green
cluster” is primarily represented by Jing‐Yang Huang,
Chia‐Chi Lung, and Yung‐Po Liaw; the “blue cluster” is
mainly represented by Wen‐Tsen Fang, Chih‐Yi Chen,
and Kuan‐Yu Chen; and the “purple cluster” is mainly
represented by Kun‐ta Chou, Sheng‐Wei Pan, and Tzeng‐
Ji Chen. As shown in Figure 5b, Jing‐Yang Huang and
Yung‐Po Liaw ranked rst with TLS =68, followed closely
by Chien‐Chang Ho, Zhi‐Hong Jian, Chia‐Chi Lung,
Oswald Ndi Nfor, Hui‐Hsien Pan, and others, with
TLS =66. Kai‐Ming Jhang ranked third with TLS =39.
3.5
|
Journal analysis
Journals play a crucial role in disseminating knowledge as
publishers of scientic manuscripts. We analyzed the
publishing journals for 460 publications and identied 205
journals involved. These journals were then categorized
based on the number of publications, revealing the 10
leading journals in terms of publication count (Table 3).
Notably, the Journal of Thoracic Oncology (JTO) had the
highest number of publications in this eld (n=22). The
JTO, an ofcial publication of the International Associa-
tion for the Study of LC, was established in 2006 as a
partially open‐access medical journal focusing on detect-
ing, preventing, diagnosing, and treating thoracic malig-
nancies [34]. Emphasizing a multidisciplinary approach,
the JTO holds importance in terms of epidemiology,
medical oncology, radiation oncology, thoracic surgery,
radiology, and pathology. Over the past 8 years, the jour-
nal's IF has shown a consistent upward trend, reaching
20.4 in the latest 2022–2023 IF rankings. The European
Respiratory Journal (n=21) and Respirology (n=18) fol-
lowed the JTO in publication count. Subsequently, we
processed the data using VOSViewer software to generate a
co‐citation network map of publishing journals (Figure 6a)
and compiled a ranking of the frequency of journal cita-
tions (Table 4). Surprisingly, PLoS One surpassed the JTO,
claiming the top position with 518 citations, followed
closely by the International Journal of Cancer with 515
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FIGURE 4 Distribution of institutions with studies on lung cancer with pulmonary tuberculosis (LC‐PTB). (a) Distribution map of
institutions with more than ve publications. (b) Network map of collaborative institutions. On the basis of the total link strength (TLS),
institutions are divided into three clusters: red, green, and blue.
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MEDICINE ADVANCES
citations. Journal of Thoracic Oncology secured the third
position with 382 citations. The frequency of citations for
these journals could be further visualized through a
network density map based on the overall link strength
between the journals (Figure 6b).
Journals with higher citation frequencies display a
deeper red color, indicating higher density, whereas
journals with fewer citations appear lighter, signifying
lower density [35]. CiteSpace software was also used to
analyze the thematic and disciplinary domains of the
citing and cited journals, resulting in a combined map of
citing and cited journals in the LC‐PTB eld (Figure 6c).
The cited journals, primarily related to molecular biology,
immunology, medicine, and clinical studies, are posi-
tioned on the left side, and the cited journals, predomi-
nantly associated with medicine, nursing, molecular
biology, and genetics, are on the right side. The colored
paths between the two sides represent citation relation-
ships [36]. Notably, two green paths and one orange path
can be visually observed. The green paths indicate that
journals in medicine, clinical research, neurology, and
related disciplines frequently cite molecular biology, ge-
netics, hygiene, and nursing journals. The orange path
signies frequent citations of journals focused on mo-
lecular biology, genetics, and associated elds by molec-
ular biology, genetics, and immunology journals.
3.6
|
Evolutionary path analysis
In the analysis, we also delved into citation references of
the 460 included publications to understand the evolution
of research in the LC‐PTB eld. This approach was adopted
because co‐citation analysis of references can assist in
clustering publication types to a certain extent so as to
further explore their primary components [37]. The
resulting data were input into CiteSpace with the following
parameter settings: the timeline ranged from 1995 to 2022,
with a slicing interval of 5 years. The research node type
was selected as cited references, with the g‐index criteria
(k=25) and no trimming. This yielded a co‐citation clus-
tering diagram (Figure 7a) and a timeline map (Figure 7b).
In Figure 7a, the co‐citation network nodes (N) amounted
to 350, categorizing the research areas into seven clusters.
Among these, the clusters formed included anti‐
programmed cell death, MTB, confusing mass, incidence
mortality, and dual nature.
We also observed that the predominant themes within
these clusters revolved around confusion in the diagnosis
of LC and PTB, increasing mortality rates associated with
both diseases, and the resistance to programmed cell death.
In Figure 7b, the evolving relationship between the pri-
mary content of research areas and time became increas-
ingly prominent. Notably, the nodes not only represented
the cited references but also depicted the evolution of
research directions through varying shades of color, with
the curves between nodes indicating co‐citation relation-
ships among references [38]. As a result, we inferred that
the scholarly themes of co‐cited references regarding the
topic of anti‐programmed cell death within the LC‐PTB
domain have remained consistently prominent over time,
and the study of incidence mortality in the context of the
combined diseases has also emerged as a sustained area of
interest in recent years.
We conducted an analysis of the 10 most frequently
cited publications [8, 39–47] (Table 5), revealing that the
publication entitled “Increased LC risk among patients
with PTB: a population cohort study,” published in the
TABLE 1Ten leading institutions in terms of cooperation strength.
Rank Organization Location TLS
a
Documents
b
Citations
c
1 Chung Shan Medical University Taiwan, China 32 10 107
2 Chung Shan Hospital Taiwan, China 30 10 115
3 Taipei Medical University Taiwan, China 25 11 153
4 Fu Jen Catholic University Taiwan, China 19 8 106
5 Changhua Christian Hospital Taiwan, China 19 5 50
6 National Yang‐Ming University Taiwan, China 18 9 381
7 Taipei Veterans General Hospital Taiwan, China 12 9 268
8 National Taiwan University Hospital Taiwan, China 11 9 186
9 National Taiwan University Taiwan, China 10 6 111
10 Sungkyunkwan University Seoul, South Korea 7 7 103
a
Total link strength (TLS) is a measure of the strength of links in a network, in this case the strength of collaborative relationships between institutions.
b
Documents refer to the number of publications from each institution.
c
Citations are the frequency of citations for publications issued by the institution.
MEDICINE ADVANCES
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JTO in 2011, garnered the highest number of citations
(n=26) [39]. This multicenter cohort study included a
cohort of 716,872 cancer‐free individuals aged 20 years
and above, comprising 4480 patients with TB and 712,392
individuals without TB (followed up to 2007). The study
compared the incidence of LC between the two cohorts
and measured the associated risks. The results indicated
that the incidence rate of LC among patients with TB
(2.41 per 10,000 person‐years) was approximately 11
times higher than that of the non‐TB cohort (26.3 per
10,000 person‐years), with a risk ratio of 4.37 (95% con-
dence interval: 3.56–5.36) [39]. This research provided
evidence regarding an increased risk of developing LC in
patients with PTB, establishing itself as a classic publi-
cation in the eld.
3.7
|
Analysis of research trends and
frontiers
In this study, we extracted 1524 keywords from the 460
included publications and generated a word cloud using
Scimago Graphica software (Figure 8a). The results
revealed that “Lung cancer,” “Tuberculosis,” “Pulmonary
tuberculosis,” and “Diagnosis” had the highest frequency
of occurrence. In VOSviewer software, with a threshold
FIGURE 5 Distribution of authors conducting research related to lung cancer with pulmonary tuberculosis (LC‐PTB). (a) Distribution
map of authors with two or more publications from 1995 to 2022. (b) Co‐occurrence map of collaboration strength among authors in LC‐
PTB‐related research from 1995 to 2022. The map categorizes collaborative relationships into ve clusters: red, yellow, green, blue, and
purple clusters.
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minimum occurrence of two keywords, a total of 386
keywords met this criterion (Figure 8b). Among these
keywords, “Tuberculosis” (160 occurrences), “Lung can-
cer” (140 occurrences), and “Pulmonary tuberculosis” (80
occurrences) were the leading three. By clustering these
keywords in chronological order, we observed that in the
early stages, keywords such as “lung diseases,” “bron-
chitis,” and “exposure” were predominant (purple group).
Conversely, in recent years, keywords such as “immuno-
therapy,” “immune checkpoint inhibitors,” and “nivolu-
mab” have taken precedence (yellow group). Interestingly,
in the author keyword co‐occurrence map (Figure 8c), the
trends in author keywords from the early stages (purple
group) to the present (yellow group) closely matched the
evolution of publication keywords. These ndings indicate
that the recent research in the LC‐PTB eld has primarily
focused on immune mechanisms and immunotherapy.
This suggests a shift from macro‐level individual studies to
micro‐level investigations into the immunological aspects
of these diseases, driven by scientic and technological
advancements. Additionally, the analysis of keywords with
the most substantial citation bursts (Figure 8d) revealed
that “inammation” (n=4.67, 2010–2014), “Fludeox-
yglucose Positron Emission Computed Tomography”
(n=4.1, 2002–2009), and “reactivation” (n=3.98, 2019–
2022) ranked among the leading three keywords. Inter-
estingly, in recent years, “cell,” “reactivation,” and “risk”
have become important research keywords. These data
suggest that studies focusing on cellular‐level mecha-
nisms, stress responses, and risks associated with the co‐
occurrence of both diseases may become leading topics
in LC‐PTB research.
TABLE 3Ten journals with the most publications.
Rank Journal Country Document ISSN E‐ISSN IF H‐index
1Journal of Thoracic Oncology USA 22 1556‐0864 1556‐1380 20.4 133
2European Respiratory Journal United Kingdom 21 0903‐1936 1399‐3003 7.636 216
3Respirology Australia 18 1323‐7799 1440‐1843 6.9 72
4International Journal of Tuberculosis France 17 1027‐3719 1815‐7920 4 101
5Lung Cancer Netherlands 16 0169‐5002 1872‐8332 5.3 114
6American Journal of Respiratory and
Critical Care Medicine
USA 15 1073‐449X 1535‐4970 24.7 343
7Medicine USA 14 0025‐7974 1536‐5964 1.6 135
8Chest USA 13 0012‐3692 1931‐3543 9.6 267
9PLoS One USA 9 1932‐6203 NA 3.7 268
10 Journal of Thoracic Disease China 8 2072‐1439 2077‐6624 2.5 45
Abbreviations: IF, impact factor; NA, not available.
TABLE 2Ten authors with the most publications.
Rank Author Country Year
a
Document Published organization H‐index
1 Huang, Jing‐Yang China 2014 8 Chung Shan Medical University and University Hospital 69
2 Liaw, Yung‐Po China 2014 8 Chung Shan Medical University and University Hospital 29
3 Ho, Chien‐Chang China 2015 7 Fu Jen Catholic University 16
4 Jian, Zhi‐Hong China 2015 7 Chung Shan Medical University 22
5 Ku, Wen‐Yuan China 2015 7 Chung Shan Medical University 9
6 Lung, Chia‐Chi China 2015 7 Chung Shan Medical University 19
7 Nfor, Oswald Ndi China 2015 7 Chung Shan Medical University 15
8 Pan, Hui‐Hsien China 2015 7 Chung Shan Medical University 10
9 Porcel, Jose M Spain 2016 6 Arnau de Vilanova University Hospital 29
10 Wu, Ming‐Fang China 2014 5 Chung Shan Medical University Hospital 27
a
Year of the author's rst publication.
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FIGURE 6 Co‐citation network, co‐citation density analysis, and dual‐map overlay of citing and cited journals. (a) Co‐citation
network map based on the total link strength (TLS) divided into eight groups. (b) Visualization of the co‐citation network density.
International Journal of Cancer and Journal of Thoracic Oncology (JTO) exhibit the most robust co‐citation density. (c) Dual‐map overlay
analysis of citing and cited journals. The cited journals mainly cover molecular biology, immunology, medicine, and clinical studies; the
cited journals primarily focus on medicine, nursing, molecular biology, and genetics.
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4
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DISCUSSION
Lung cancer and PTB are seemingly unrelated diseases
that are actually closely related [42]. Lung cancer and
PTB have become serious global public health issues,
claiming millions of lives annually [2, 5]. However, owing
to the similarity in symptoms between LC and PTB, ac-
curate diagnosis can be challenging under certain cir-
cumstances, particularly during the early stages of these
diseases [48]. Numerous studies have identied factors
such as chronic inammation, genomic changes, and
brosis in patients with TB that may promote the
development and progression of LC, as well as the
treatment of patients with LC and use of immune
checkpoint inhibitors, which may induce reactivation of
LTBI [49]. Therefore, the study of LC‐PTB co‐morbidity is
important for early warning, precise diagnosis, and
individualized treatment.
As a discipline that reveals the development patterns
and trends of scientic research, bibliometrics plays a
crucial role in the study of LC and PTB [50, 51]. However,
a comprehensive bibliometric analysis of the LC‐PTB
domain has not been conducted to date. To address this
gap, in the present study, we conducted a bibliometric
analysis of relevant research on LC‐PTB using the SCI‐E
database over the past 28 years (1995–2022) and visual-
ized the ndings. After applying specic selection
criteria, the search yielded 460 publications authored by
2792 individuals from 1547 institutions across 177
countries or regions. Subsequently, various bibliometric
analytic tools were applied to construct and visually
analyze networks related to LC‐PTB publications. Herein,
we summarize the current research status in this eld
and predict future research trends.
The annual number of publications in a specic eld
can intuitively reect the research activity and popularity
in that eld. Our results showed that, in terms of annual
publications, there was a general trend of increasing
publication numbers over the years, reaching a peak in
2020. This trend can be attributed to several factors. In
2018, two pivotal studies on immunotherapy—
KEYNOTE‐189 and KEYNOTE‐407—demonstrated the
efcacy of pembrolizumab combined with chemotherapy
as a rst‐line treatment for all patients with advanced LC
[52, 53]. Additionally, a 2019 study by Tony S K Mok
et al., known as KEYNOTE‐042, shifted the focus toward
“non‐chemotherapy” regimens for patients with
advanced LC [54]. This study proposed pembrolizumab
as a potential rst‐line treatment for patients with locally
advanced or metastatic non‐small cell lung cancer with a
PD‐L1 tumor proportion score ≥1% and no epidermal
growth factor receptor (EGFR)/anaplastic lymphoma ki-
nase mutations [54]. The following publication of the
study results, the Food and Drug Administration
approved pembrolizumab as the rst‐line treatment in
April 2019. Furthermore, a new 2019 study by Johnson
et al. identied a group of novel chemical inhibitors
capable of eliminating MTB [55]. This study used the
novel PROSPECT high‐throughput drug discovery
approach to identify promising candidate drugs, offering
a potential pathway to address the urgent need for new
antibiotics to combat global TB drug resistance [55].
A global perspective regarding the annual publication
count provides a visual representation of research activity
in the LC‐PTB eld. However, this view does not offer
specic analysis at the country or regional level. There-
fore, the aim of this study was to enhance the precision of
analysis and further explore the LC‐PTB research
TABLE 4Ten most‐cited journals.
Rank Journal Country ISSN E‐ISSN IF H‐index Citations
1PLoS One USA 1932‐6203 NA 3.7 268 518
2International Journal of Cancer Switzerland 0020‐7136 1097‐0215 6.4 212 515
3Journal of Thoracic Oncology USA 1556‐0864 1556‐1380 20.4 133 382
4Chest USA 0012‐3692 1931‐3543 9.6 267 380
5Lung Cancer Netherlands 0169‐5002 1872‐8332 5.3 114 374
6International Journal of Tuberculosis France 1027‐3719 1815‐7920 4 101 356
7Medicine USA 0025‐7974 1536‐5964 1.6 135 189
8BMC Cancer United Kingdom 1471‐2407 NA 3.8 111 104
9American Journal of Respiratory and
Critical Care Medicine
USA 1073‐449X 1535‐4970 24.7 343 80
10 Journal of Thoracic Disease China 2072‐1439 2077‐6624 2.5 45 79
Abbreviations: IF, impact factor; NA, not available.
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landscape from the perspectives of countries and regions.
Our data indicated that both the number of publications
and the strength of collaboration were predominantly led
by China. China ranked rst in terms of the number of
publications and intensity of collaboration in the eld of
LC‐PTB research, primarily owing to its large population
and high incidence rates of LC and PTB [56]. For many
years, China has been grappling with a heavy burden of
PTB, maintaining a persistently high prevalence rate.
Despite concerted efforts, including the implementation of
TB control programs, improvements in health care ser-
vices, and heightened public awareness, which have led to
FIGURE 7 Analysis of references in research related to lung cancer with pulmonary tuberculosis (LC‐PTB). (a) Cluster map of
references. Clustering of the main content of cited references related to LC‐PTB from 1995 to 2022 resulted in clusters, including “anti‐
programmed cell death,” “mycobacterium tuberculosis,” “confusing mass,” “incidence mortality,” and “dual nature.” (b) Timeline map of
references. The nodes represent cited references, and their position indicates the rst time that they were cited. The diameter of the nodes
is closely related to the frequency of citations, and the color (red) represents not only the centrality of references but also the shift in their
research direction. Furthermore, the connecting lines between the nodes represent the co‐citation relationships. In the map, the topic of
anti‐programmed cell death related to LC‐PTB remains predominant; research on the incidence mortality of the two diseases has also been
a popular topic in recent years.
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a gradually declining trend in the prevalence rates of TB,
challenges remain in effectively controlling and eradi-
cating PTB, particularly in rural and underdeveloped
western regions [4, 57–60]. Additionally, the incidence of
LC in China is on the rise, mainly attributable to factors
such as smoking, air pollution, and occupational hazards
[61]. More worryingly, LC and PTB have become major
public health problems in China, and the incidence of LC‐
PTB is now on the rise globally [6, 7, 61]. Despite China's
leading position in terms of volume of publications in the
LC‐PTB eld, it is crucial to note the impact of these
publications. Citation frequency serves as an indicator for
assessing the inuence of research publications [10, 62].
Our analysis of the citation frequencies of publications
related to LC‐PTB from various countries revealed that
publications by Chinese authors have a lower citation
frequency than those by authors from Europe and the
United States. This indicates that further in‐depth
research is needed in China, together with increased in-
ternational collaboration to enhance the impact of its
research in this eld. These trends have compelled the
Chinese government to continue investing in preventive
measures, early diagnosis, and comprehensive treatment
strategies to alleviate the burden of LC‐PTB in the country.
After conducting an analysis based on the annual
publication count and from country or regional per-
spectives, we further enhanced the precision of analysis
by exploring the LC‐PTB research eld from the per-
spectives of authors and journals. This allows for a
more detailed understanding of the researchers and
publications contributing to the LC‐PTB domain [10].
We found that the authors with the most publications
were Jing‐Yang Huang and Yung‐Po Liaw, both with
eight documents, indicating their high research pro-
ductivity and activity in this eld. Both of these authors
are from China, a populous nation with a high inci-
dence of TB [63]. The progress of TB prevention and
control in China is encouraging under current circum-
stances. However, the persistent presence of pathogen
resistance presents new challenges for epidemic control.
China's continuous research on LC‐PTB can be regar-
ded as a coping strategy to better respond to the
changing situation of TB and the potential trend of
these two diseases merging.
As vehicles for scientic publication, journals play an
important role in scientic dissemination and interna-
tional scholarly cooperation and exchange [64, 65]. In this
study, we also analyzed LC‐PTB‐related research from the
perspectives of journals and international collaboration.
We found that most authors and institutions publishing in
top‐tier journals are from Europe and the United States,
regardless of the number of publications or the citation
strength of the journals. This is potentially owing to the
long‐standing history and rich academic research tradi-
tions in European and North American countries, the
substantial investment of resources and funding in scien-
tic research, and active participation in international
research collaboration and exchange [66, 67]. Further-
more, in terms of journal themes, most of the 10 leading
journals in terms of publication quantity are focused
on clinical aspects (such as the JTO and European Respi-
ratory Journal). In comparison, comprehensive journals
predominate among the 10 most‐cited journals (such as
PLoS One), aligning with the disciplinary distribution
presented in the dual graph overlay. This also indicates that
the research direction of LC‐PTB mainly encompasses
TABLE 5Ten most frequently cited references.
Rank
First author and
reference
Publish
time Source Citations
a
Total
citations
b
1 Yu YH [39] Jan 2011 Journal of Thoracic Oncology 26 160
2 Fujita K [40] Dec 2016 Journal of Thoracic Oncology 24 98
3 Picchi H [41] Mar 2018 Clinical Microbiology and Infection 22 108
4 Wu CY [42] Feb 1, 2011 Cancer 20 134
5 Anastasopoulou A [43] Sept 4, 2019 Journal for Immunotherapy of Cancer 18 69
6 Cheng MP [8] Mar 1, 2017 Clinical Infectious Diseases 18 79
7 Chu Yi‐Chun [44] Aug 2017 Journal of Thoracic Oncology 18 77
8 Barber DL [45] Jan 16, 2019 Science Translational Medicine 17 125
9 Ho JCM [46] Aug 2018 Lung Cancer 17 48
10 Elkington PT [47] Dec 1, 2018 American Journal of Respiratory and Critical Care
Medicine
16 46
a
Citation frequency in search results.
b
Total citation frequency in the WoSCC database.
MEDICINE ADVANCES
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157
basic and translational research from basic science to
clinical application.
To further delineate the research hotspots in the eld
of LC‐PTB, we conducted a study of the co‐citation
references in the 460 included publications [68]. We
found that the 10 leading co‐cited references primarily
pertain to the mutual promotion of LC and TB. For
instance, a cohort study by Yang‐Hao Yu et al. published
FIGURE 8 Keyword analysis of LC‐PTB‐related studies. (a) Word cloud map of keywords used two or more times in 460 publications.
(b) Keyword network visualization map of publications. We visualized and analyzed keywords with a minimum frequency of occurrence
more than two in chronological order, with 13 clusters. (c) Author keyword network visualization map. We visualized and analyzed
keywords with a minimum frequency of occurrence greater than two in chronological order, with 13 clusters. (d) Ten keywords with the
strongest citation bursts.
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in the JTO revealed that the incidence of LC in a TB
patient cohort was approximately 11 times higher than
that among patients without TB [39]. That study provides
compelling evidence demonstrating the increased risk of
LC in patients with TB. Among the ve leading co‐cited
references, an article entitled “Anti‐PD1 Antibody
Treatment and the Development of Acute PTB” focuses
on the potential of LC immunotherapy to lead to the
FIGURE 8 (Continued)
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159
occurrence of TB [40]. Immune escape is the process by
which tumor cells evade the immune system, and it is
also an important factor in the reactivation of MTB
infection or LTBI in patients with LC [61, 69–72].
Furthermore, of these 10 highly cited articles, six are
related to the study of immune mechanisms associated
with abnormal immune toxicity (immune‐related adverse
events) caused by immune checkpoint inhibitors for the
treatment of LC. The mechanism of this correlation may
be related to immunity, further indicating the mutual
inuence of and promotion between LC and PTB. This
may become an important research trend in the future
that may help to reduce the incidence of LC‐PTB.
The increase in drug resistance poses an emerging
and challenging issue in the treatment of TB and LC,
with growing evidence suggesting a potential correlation
between this phenomenon and the coexistence of TB and
lung cancer (LC‐PTB comorbidity). Patients with drug‐
resistant TB or with LC often exhibit gene mutations
associated with drug resistance, which may promote the
occurrence of LC‐PTB comorbidity. For instance, previ-
ous studies have revealed a potential link between TB
and EGFR gene mutations leading to LC drug resistance
[73, 74]. In drug‐resistant populations, signicant in-
creases in phosphatase and tensin homolog mutations,
which inhibit the tumor suppressor phosphatidylinositol
3‐kinase (PI3K) pathway, have been observed. This
alteration triggers activation of the PI3K pathway, exac-
erbating the transition from LTBI to active PTB and
fostering the proliferation of MTB [75, 76]. The immune
system in patients with drug‐resistant PTB or LC also
shows signs of dysregulation, which may further promote
the occurrence of LC‐PTB comorbidity. In both patients
with drug‐resistant PTB and those with LC, reduced
inltration levels and functional exhaustion of immune
effector cells have been observed, leading to immuno-
suppression and mediating immune escape [77]. Chronic
inammation and pulmonary brosis are also factors that
may contribute to the development of LC in patients with
drug‐resistant TB. Both PTB and LC involve damage to
the parenchymal tissue of the lungs, and chronic
inammation can gradually lead to the depletion of im-
mune cells [6, 78]. Concurrently, pulmonary brosis has
been recognized as a risk factor for LC, and its cumula-
tive effect together with inammation may promote the
formation and progression of LC [6, 78]. The treatment
regimen for patients with drug‐resistant PTB typically
requires the combined use of multiple anti‐TB drugs. This
combination of drugs not only suppresses lymphocytes of
the immune system but also induces the proliferation of
macrophages and affects antibody production, potentially
promoting the carcinogenic process. In summary,
although evidence on the relationship between drug
resistance and LC‐PTB comorbidity is still insufcient,
existing data already suggest that drug resistance may
play a facilitative role in the formation and progression of
this comorbidity.
Keywords are essential indicators of research hotspots
or cutting‐edge areas as they evolve [79]. As shown in
Figures 8b and c, the evolution of keywords over the past
28 years demonstrates the continuous progress in
research in the eld of LC‐PTB [80]. In conjunction with
current studies, we observed that immunotherapy, im-
mune checkpoint inhibitors, and nivolumab have been
the main keywords used in recent years. Specically,
“nivolumab” primarily refers to its association with
cancer immunotherapy as a PD‐1 inhibitor among im-
mune checkpoint inhibitors. Cancer immunotherapy is a
relatively new and promising treatment modality that has
emerged in recent years [81]. Although this therapy can
yield positive clinical outcomes, further research is
needed to determine its efcacy in patients with con-
current PTB [82–84]. Therefore, a systematic and detailed
understanding of the immunological mechanisms in LC‐
PTB can contribute to developing immunotherapeutic
approaches for these comorbidities, representing a new
research focus in the eld.
The above is our analysis of all relevant publications
in the eld of LC‐PTB from 1995 to 2022, which provides
important information regarding the status of clinical
research in LC‐PTB. First, clinical researchers can use
this information to guide their investigations and assess
the quality and impact of clinical research through the
frequency of publication citations and IFs of published
journals, thereby setting new directions in this area of
research. Second, this information can help researchers
to evaluate the research performance of individual in-
vestigators and institutions, thereby identifying potential
collaborators and collaborating institutions for clinical
research projects. Finally, for clinical researchers in the
eld of LC‐PTB, this information can help to reveal the
immune adverse events caused by immune‐related
treatments, thereby guiding clinical drug discovery.
This study is the rst comprehensive bibliometric
analysis to provide an intuitive, objective, and accurate
examination of LC‐PTB‐related publications, countries
and regions, institutions and their collaboration intensity,
author distribution and their collaboration intensity,
journals, evolutionary paths, and research trends. Various
bibliometric software tools, including CiteSpace, VOS-
viewer, and Scimago Graphica, were used to analyze the
complex relationships from multiple dimensions, enabling
researchers to gain insight into the research trends in this
eld.
This study has some unavoidable limitations. (1) The
included publications may not be exhaustive owing to our
160
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MEDICINE ADVANCES
reliance on data from the WoSCC (SCI‐E), thereby
excluding data from other important databases such as
PubMed, Embase, and Ovid. (2) The study's scope was
limited by the pre‐dened timeframe (1995–2022),
potentially missing the inuence of high‐quality articles
published before 1995 or after 2023. (3) Bibliographic
analysis has inherent limitations. One critical measure in
bibliometrics is the citation count, which is used to gauge
the inuence of a publication. However, citation counts
can be inuenced by various factors such as academic
popularity, citation bias, and self‐citation [85]. Thus,
relying solely on citation counts may not comprehen-
sively and accurately reect the quality and impact of a
publication. Additionally, bibliometrics predominantly
focuses on quantitative measures such as citation counts
and publication output, neglecting factors such as
research content quality, method reliability, and the
actual effect of research outcome [86]. Therefore, a
comprehensive assessment of the quality and impact of
research cannot rely solely on bibliometric analysis.
5
|
CONCLUSIONS
Our study ndings revealed that China is a leader in
terms of the number of publications, institutional inu-
ence, and international collaboration in the eld of LC‐
PTB, signifying a substantial contribution to its
advancement. Conversely, publications from the United
States demonstrated the highest citation frequency,
emphasizing the important impact of research originating
from Western countries. Furthermore, our analysis indi-
cated that the recent research in the LC‐PTB domain
primarily centers on immune mechanisms and immu-
notherapy. It is crucial to note that the use of immuno-
therapeutic agents in LC treatment has been linked to
immune‐related toxicities, which is an important factor
contributing to TB occurrence in patients with LC.
Therefore, attaining a comprehensive understanding of
the immunological mechanisms in LC‐PTB could
potentially facilitate the development of immunothera-
peutic strategies for these comorbidities, representing a
prospective research direction in the LC‐PTB eld.
AUTHOR CONTRIBUTIONS
Conceptualization: Wenping Gong and Jingzhi Guan.
Methodology: Ling Yang, Zhaoyang Ye, Linsheng Li, Li
Zhuang and Wenping Gong. Data Analysis: Ling Yang and
Wenping Gong. Software: Ling Yang and Wenping Gong.
Writing Original Manuscript: Ling Yang. Review and
Revising Manuscript: Wenping Gong and Jingzhi Guan.
Funding Acquisition: Wenping Gong and Jingzhi Guan.
All authors reviewed and approved the nal manuscript.
ACKNOWLEDGMENTS
We sincerely thank the reviewers and editors who pro-
vided review and editing services for this study.
CONFLICT OF INTEREST STATEMENT
The authors declare no conicts of interest. The funders
had no role in the design of the study, in the collection,
analyses, or interpretation of data, in the writing of the
manuscript, or in the decision to publish the results.
DATA AVAILABILITY STATEMENT
All data generated or analyzed during this study are
included in the published article.
ETHICS STATEMENT
Not Applicable.
INFORMED CONSENT
Not Applicable.
ORCID
Wenping Gong
https://orcid.org/0000-0002-0333-890X
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SUPPORTING INFORMATION
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in the Supporting Information section at the end of this
article.
How to cite this article: Yang L, Ye Z, Li L,
Zhuang L, Guan J, Gong W. Visualization analysis
of research progress and trends in coexistence of
lung cancer and pulmonary tuberculosis using
bibliometrics. Med Adv. 2024;2(2):144–64. https://
doi.org/10.1002/med4.58
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